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Wild Mediterranean Plants as Traditional Food: A Valuable Source of Antioxidants Paola Vanzani, Monica Rossetto, Veronica De Marco, Linda E. Sacchetti, Maurizio G. Paoletti, and Adelio Rigo

C: Food Chemistry

Abstract: Some wild Mediterranean plants used as traditional food are an extraordinary source of antioxidants. We tested

some properties of 10 of these herbaceous plants, used in Liguria (Northwest Italy) to prepare a traditional dish known as “prebuggiun.” A total of 9 of them were found to have a polyphenol content and antioxidant properties similar or better than those of red chicory and blueberry, which are, in the case of vegetables and fruits, among the richest of antioxidants. Keywords: antioxidant activity, edible herbs, lipid peroxidation, polyphenols, radical scavenging activity

Practical Application: In this article, we reported a study on wild plants growing in the Mediterranean area. These herbs

have been neglected and this study aimed to revalue these plants because they are an extraordinary source of antioxidants. The increasing demand for natural antioxidants (additives in the food industry too) justifies the search for new sources of natural antioxidants. The revaluation of these plants will be interesting for: (1) consumer health, rediscovering a vegetable source of high antioxidant power; (2) possibility of producing new commercial products, such as food supplements of high quality and low cost; (3) pharmacological applications.

Introduction Epidemiological data indicate that cardiovascular diseases are low in the Mediterranean area where plant foods rich in antioxidants make up a considerable portion of the diet (Willett and others 1995; La Vecchia 2009). These observations are supported by recent field studies. For instance, significantly higher values of total antioxidant activity and of fibrinogen were measured in plasma of elderly women living in rural region of Crete and were correlated with high wild green plant consumption (Manios and others 2005). To this regard, in the Mediterranean basin, wild plants rich of antioxidants are harvested and are eaten seasonally; however, it is important to know more about their contribution to healthy diets. Furthermore the increasing demand for natural antioxidants justifies the search for new sources of these compounds (Herrero and others 2006; Mohamed and others 2007; Gruenwald 2009; Huber and Rupasinghe 2009; Mustafa and others 2010). In this regard, attention has recently been paid to the possible health benefits of foods characterized by high free-radical trapping activity since some of these radicals are involved in human diseases and in particular in cardiovascular and neurological pathologies (Lee and others 2004; Rossetto and others 2008; Tosetti and others 2009). Among these foods, blueberries and chicories (wild Cichorium intybus, and cultivated, that is, red chicories) rank at the top for their antioxidant activity (Rossetto and others 2005; Sal-

MS 20100495 Submitted 5/7/2010, Accepted 10/13/2010. Authors Vanzani, Rossetto, De Marco, and Rigo are with Dept. of Biological Chemistry and authors Sacchetti and Paoletti are with Lab. of Agroecology and Ethnobiology, Dept. of Biology, Univ. of Padova, via G. Colombo 3, 35131 Italy. Authors Vanzani, Rossetto, and Rigo are also with Consortium INBB, Section of Padova, viale Medaglie d’Oro 305, 00136 Roma, Italy. Direct inquiries to author Rigo (E-mail:


Journal of Food Science r Vol. 76, Nr. 1, 2011

vatore and others 2005). Therefore, the radical trapping properties of the Mediterranean flora, comprising more than 10000 plant species with various properties (antiinflammatory, diuretic, and so on), deserve further investigation. To this respect, we considered a traditional food from Liguria region (Northwest Italy, especially in the province of Genova) called “prebuggiun” or “preboggion,” which consists of dozens of wild herbs. The new leaves and shoots of these herbs are usually harvested from early spring to summer and are used raw, or boiled for a few minutes, as key ingredients for soups, stuffing for pies, and vegetable raviolis (the typical pansotti) or simply as “a side-dish” (Bisio and Minuto 1999). In particular, prebuggiun is a “mixture” of wild or semidomesticated herbs collected in farmed or uncultivated land. These herbs belong to 15 families, more than half of which from the Compositae family (Bisio and Minuto 1999). According to some researchers a variety of phenolics such as hydroxycinnamic acids, benzoic acids, flavonols, flavones, anthocyans beyond cumarins, terpenes, alkaloids, and carotenoids, are present in some of prebuggiun plants (Paoletti and others 1995; Mimaki and others 2001; el-Mousallamy 2002; Vlcek and others 2002; Ayoub 2003; Zeghichi and others 2003; Parejo and others 2004; Galvez and others 2005; Heinrich and others 2005; Adam and others 2009; Conforti and others 2009). However, despite the richness of phenolic compounds of some of these plants, homogeneous and quantitative data on the antioxidant activity and phenolic composition have not been reported yet. We examined 10 of these herbs for polyphenol content, their antioxidant properties, including iron reducing power and their capacity and efficiency in trapping peroxyl radicals (LOO◦ ), and found that almost all of these plants show antioxidant features similar or better than those characterizing red chicories and blueberries, which are at the top among vegetables and fruits for antioxidant activity (Rossetto and others 2005).  C


2010 Institute of Food Technologists doi: 10.1111/j.1750-3841.2010.01949.x Further reproduction without permission is prohibited

Materials and Methods Chemicals Rac1-lauroylglycerol and AlCl3 hexahydrate was obtained from Sigma-Aldrich (Milano, Italy). Linoleic acid, deoxycholic acid sodium salt monohydrate, sodium acetate, FeSO4 , FeCl3 , and 2,4,6-Tri(2-pyridyl)-5-triazine were purchased from Fluka (Buchs, Switzerland). 2,2 -azobis(2-[2-imidazolin-2-yl]propane) dihydrochloride (ABIP) was a kind gift of Wako Chemicals (Neuss, Germany). Folin–Ciocalteu phenol reagent was obtained from Sigma-Aldrich. Chlorogenic acid, gallic acid, cyanidin3-glucoside, and quercetin were purchased from Extrasynth`ese (Genay Cedex, France). Quartz distilled water was used to prepare all the aqueous solutions. Buffers were equilibrated in batch with Chelex-100 (BioRad, Richmond, Calif., U.S.A.) to minimize the concentration of heavy metal ions.

Harvesting and sample preparation Each of the wild herbaceous plant was harvested in 4 different areas of the seaside hills east of Portofino (Genova, Italy) in spring, when they are particularly good for eating. The plants were processed within 48 h from the harvesting. Verona red chicory, wild chicory (Chicory intybus), and blueberry (Vaccinium myrtillus), used as comparison, were obtained from local markets in Padova. The extracts of the plants were prepared using about 100 g of edible part (leaves) of this plant from each area. The raw herbs, randomly sampled, 400 g, were homogenized in 1 L of ethanol/water solution (85 : 15, v/v) containing 0.12 M HCl (Rossetto and others 2005). The homogenates were centrifuged and the supernatants were stored at −80 ◦ C until measurements. Spectrophotometric characterization and quantification of various families of antioxidant Plant extracts (5 and 180 mg fresh weight per milliliter in ethanol/water solution, 85 : 15, v/v, containing 0.12 M HCl) were analyzed spectrophotometrically in the 250 to 800 nm UVVis range. Total hydroxycinnamic acid content. Hydroxycinnamic acid content was determined measuring the optical absorption of the complex of hydroxycinnamic acids with aluminium (III) (Zaporozhets and others 2003). Appropriately diluted extracts were mixed with a solution of AlCl3 in sodium acetate buffer, (50 mM Al[III] final concentration). Optical density was measured at 365 nm. Chlorogenic acid was used as a standard, and the results were expressed as millimoles of chlorogenic acid per kilogram of vegetable fresh weight. Total anthocyanin content. Anthocyanin content was determined according a pH-differential method (Yang and Zhai 2010). Briefly, absorbances of the hydro-alcoholic extract (0.1 M HCl), and of the extract buffered at pH 4.5 (with sodium acetate) were measured at 530 and 700 nm, respectively. The absorbance due to anthocyanins was calculated as Abs = (Abs530 − Abs700 ) pH 1 − (Abs530 − Abs700 ) pH 4.5 and the anthocyanin concentration was calculated using cyanidin 3-glucoside as standard compound. Anthocyanin concentration was express as millimoles of cyanidin 3-glucoside per kilogram of vegetable fresh weight.

Total phenol content The total phenol content (TP) was measured according to the Folin–Ciocalteu method (Lee and others 2003). The absorbance measurements were carried out by a Varian Cary 50 spectrophotometer at 770 nm after incubation of the reaction mixture for 60 min at room temperature. The TP of extracts was expressed as millimoles of gallic acid per kilogram of plant fresh weight. The ferric reducing antioxidant power (FRAP) The ferric reducing antioxidant power (FRAP assay) of the ethanolic extracts was estimated according to the procedure described by Benzie and Strain (1996). This method is based on the electron transfer between the antioxidant molecules and Fe3+ ions. The change of absorbance of the FRAP reagent (prewarmed at 37 ◦ C) was monitored at 596 nm after 10 min of reaction. A Varian Cary 50 UV-Vis spectrophotometer was used. Solutions of FeSO4 of known concentration were used for calibration. Measurement of the peroxyl radical scavenging activity The peroxyl radical scavenging activity of various ethanolic extracts was calculated by measuring their ability to inhibit the peroxidation of linoleic acid in a micellar system (Zennaro and others 2007). The oxygraphic method that we have used on the basis of a rigorous kinetic model permits obtaining the peroxyl radical trapping capacity (PRTC) and the equivalent peroxyl radical trapping efficiency (ePRTE) of the extracts. PRTC is expressed as millimoles of LOO◦ trapped by 1 kg of plant fresh weight and ePRTE is the efficiency of food in trapping LOO◦ expressed as millimoles of Trolox in 1 kg of plant fresh weight. The rate of peroxidation of linoleic acid was measured from the rate of O2 disappearance by a Metrohm 663 VA stand equipped with a Yellow Spring Oxygen electrode, inserted into a thermostated oxygraphic cell. The current study was recorded by a personal computer equipped with a data acquisition board (DAQ PCI-6221, M series, Natl. Instruments, Austin, Tex., U.S.A.). The working electrode was poised at −800 mV against Ag/AgCl. The experimental oxygraphic traces were automatically processed by means of a computational procedure to obtain oxygen consumption rates from which the PRTC and PRTE values were calculated (Zennaro and others 2007). The reaction mixture was prepared by evaporating the solvent from a solution of Rac1-lauroylglycerol in dichloromethane and by dissolving the resulting film in 20 mM phosphate buffer, pH 7.4, containing 5 mM deoxycholic acid sodium salt, to obtain 0.5 mM final concentration of Rac1-lauroylglycerol. Linoleic acid (2 mM final concentration) was then added and the solution vigorously vortexed. The micelle containing solution was equilibrated with atmospheric oxygen in the oxygraphic cell thermostated at 37 ± 0.1 ◦ C. After thermal equilibrium, ABIP, 4 mM final concentration, was added as a constant source of LOO◦ , which start lipid peroxidation and the plant extracts were injected (at a final concentration 0.1 to 0.01 g/mL) 1 min after the ABIP addition. Statistical analysis The measurements were usually carried out in quadruplicate and values are expressed as means ± standard deviations (SD). The Student’s t-test was used to compare data of raw and boiled herbs. Analysis of variance (ANOVA) was performed and differences between means were considered statistically significant at P ≤ 0.05 according to Fisher’s least significant difference (LSD test). Multiple linear regressions were carried out to correlate important phenolic constituents to antioxidant activity tests. Vol. 76, Nr. 1, 2011 r Journal of Food Science C47

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Wild plants as source of antioxidants . . .

Wild plants as source of antioxidants . . .

C: Food Chemistry

All statistical analyses were performed using SigmaStat 3.1, Ad- are spectroscopic features of hydroxycinnamic acids. In Figure 1C we have reported the spectra of the concentrated extracts of some visory Statistics for Scientists. prebuggiun herbs together with that of cyanidin-3-glucoside in the Results and Discussion 450 to 650 nm region, where the anthocyanins absorb. In all the extracts, with the exception of those of Sanguisorba minor L. and Wild herbs used as food The wild Mediterranean plants examined in this study are listed Foeniculum vulgare, the presence of a peak around 535 nm was in Table 1 together with their traditional properties. All these found which could be attributed to anthocyanins. The confirmation of the presence of these important families plants may be eaten raw or boiled for a few minutes and, according to popular belief, most of them present a varieties of properties of antioxidants was carried out according to validate and selecsuch as depurative, diuretic, antiinflammatory, analgesic, digestive, tive colorimetric methods using specific reagents (see Materials cicatrizing, and so on (Trichopoulou 2001; Guarrera 2003; Herold and Methods) and the results obtained are reported in Table 2. According to these methods, the large presence of hydroxycinand others 2003; Garc´ıa-Lafuente and others 2009). namic acids in the prebuggiun plants was confirmed with the Spectrophotometric characterization of polyphenols exclusion of Rumex crispus and of Sanguisorba minor where this present in the plant extracts family of phenols was found in negligible amount. However, only Figure 1A and B show the UV-Vis spectra in the region 250 in the case of these 2 plants, a significant amount of flavonoids to 500 nm of the acid hydroalcoholic extracts obtained from the was found according to the flavonoid test of Tabart and others wild herbs. For sake of comparison in Figure 1A, the spectra of (2010). blueberry (l) and of wild (f) and red chicory (h) extracts together Furthermore anthocyanins, which are present in a large amount with that of chlorogenic acid (i), a hydroxycinnamic acid, are also in blueberry and Verona Red Chicory came out to be present in reported. a very small amount (< 1/100 of the total amount of polypheMost of these spectra are characterized by the presence of a nols) in the prebuggiun plants we have examined, see Table 2, last peak at 335 nm and of a shoulder at about at 300 nm, which column. Table 1–Characteristics of some Mediterranean herbaceous plants (prebuggiun) used as food in Liguria region. Scientific name

Common name

Hyoseris radiata L. Reichardia picroides (L.) Roth

Wild chicory Compositae French Scorzonera Compositae

leaves boiled and/or eaten raw in salads leaves boiled and/or eaten raw in salads

Plantago lanceolata L.

Ribwort Plantain


leaves boiled. Taste: slightly bitter

Sonchus oleraceus L.

Sow Thistleg


Foeniculum vulgare Miller

Wild fennel


Sanguisorba minor L.

Salad Burnet


Centranthus ruber (L.) DC.

Red Valerian


Rumex crispus L.

Curled Dock


leaves boiled and/or eaten raw in salads. Taste: slightly bitter, with hazelnut flavour leaves and stem boiled and/or eaten raw in salads leaves boiled and/or eaten raw in salads. Taste: slightly bitter leaves boiled; young leaves are eaten raw in salads boiled leaves

Ranunculus ficaria L.

Lesser Celandine


boiled leaves

Silene vulgaris (Moench) Garcke Bladder Campion



Caryophyllaceae boiled leaves and/or eaten raw in salads

Traditional properties blood depurative diuretic, depurative, analgesic against toothache antiinflammatory, cicatrizant action, lenitive astringent, tonic, laxative, cholagogue aperitive, digestive astringent, digestive, cough-relieving nervine, antispasmodic antiinflammatory, cicatrizant action, tonic, ristorative, antiseptic, astringent revulsive and cicatrizant action, against haemorrhoids remineralizing

Figure 1–UV-Vis spectra of the acid hydroalcoholic extracts. A and B: 5 mg of fresh weight per milliliter of a, Reichardia picroides (L.) Roth; b, Sonchus oleraceus L.; c, Plantago lanceolata L.; d, Hyoseris radiata L.; e, Foeniculum vulgare Miller; f, wild Cichorium intybus; g, Centranthus ruber (L.) DC.; h, 40 μM chlorogenic acid; i, Verona Red Cichory; l, blueberry; and m, Sanguisorba minor L.; n, Rumex crispus L.; o, Silene vulgare (Moench) Garcke; p, Ranunculus ficaria L. C: 0.18 g of fresh weight per milliliter, of some Prebuggiun herbs; q, 5 μM cyanidin 3-glucosyde.

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Antioxidant properties Plant extracts were examined for the TP, for the electron exchange properties (FRAP) and for the capacity (PRTC), and efficiency (ePRTE) in trapping LOO◦ , measured according to the oxygraphic method previously described (Zennaro and others 2007). PRTC represents the amount of peroxyl radical trapped by a given amount of food, while ePRTE represents the reactivity by which LOO◦ are trapped and is correlated with the kinetic rate constant of the inhibition reaction. The obtained values are reported in Table 2. Although the red chicory and blueberry are characterized by a high content of polyphenols (some millimoles of gallic acid per kilogram fresh weight) in the case of the prebuggiun herbs that we have examined, the TP content is similar or higher. The amount of polyphenols present in Sanguisorba minor L. is particularly high. In fact this content is many times higher than the polyphenol content in wild blueberry. In column 4 of Table 2, the results of ferric iron reducing antioxidant power measured according to the FRAP assay on the herb extracts are also

reported. The FRAP values of prebuggiun herbs are only in 2 cases (Sanguisorba minor L. and Rumex crispus L.) remarkable higher than those of reference plants (wild and cultivated chicory and blueberry), while in the other cases the FRAP values are similar to the reference value. It is interesting to observe the linear relationship between the TP and FRAP values of the prebuggiun herbs (r > 0.97) if the Sanguisorba minor L. value is excluded. For these herbs a ratio FRAP/TP = 1.5 ± 0.3 was calculated, while this ratio in the case of Sanguisorba minor L. and of red chicory and blueberry was 2.8 ± 0.3 (see Table 3). Regarding the ePRTE and PRTC, the values of these parameters are in most of the herbs we have examined similar or higher than those we have found for blueberries and red chicories, see Table 2. In particular, the PRTC values of all the herbs, with the exception of Ranunculus ficaria L., are significantly higher than the PRTC of blueberry. Low linear correlation was found between the ePRTE and PRTC values (r = 0.47), as expected for kinetic and stoichiometric parameters. Also, the linear relationship

Table 2–Antioxidant properties of some wild plants (prebuggiun) and comparison to reference plants. Prebuggiun plants Hyoseris radiata L. Reichardia picroides (L.) Roth Plantago lanceolata L. Sonchus oleraceus L. Foeniculum vulgare Miller Sanguisorba minor L. Centranthus ruber (L.) DC. Rumex crispus L. Ranunculus ficaria L Silene vulgaris (Moench) Garcke Reference plants Chicorium intybus L. (Verona Red Chicory) Vaccinium myrtillus (wild blueberry) Chicorium intybus L. (wild chicory)

ePRTEa (mmol/kg)

PRTCb (mmolLOO◦ /kg)

FRAPc (mmolFe2+ /kg)

TPd (mmol/kg)

Hydroxy-cinnamic acidse (mmol/kg)

Anthocyaninsf (mmol/kg)

105 ± 2.0a 103 ± 4.8a

171 ± 10c 153 ± 9.4d

31.1 ± 2.0e 38.9 ± 1.6d

19.8 ± 1.1def 22.9 ± 1.5d

17.5 19.3

0.027 0.025

91.1 ± 5.2b 88.3 ± 5.2b 72.3 ± 3.6c 69.9 ± 1.6c 43.1 ± 2.0d

223 ± 11a 129 ± 5.5e 105 ± 4.1f 212 ± 10b 99.2 ± 7.3f

43.8 ± 1.4d 31.8 ± 2.2e 27.9 ± 0.7e 257 ± 12a 26.3 ± 0.5e

27.6 ± 1.9c 18.6 ± 1.7ef 17.8 ± 1.1f 98.2 ± 4.6a 20.6 ± 1.6de

14.4 13.4 14.0 < 0.5 12.0

0.012 0.080 < 0.01 < 0.01 0.012

35.4 ± 6.8e 7.7 ± 0.5f 5.7 ± 1.1f

N.M. 33.2 ± 1.7l N.M.

131 ± 5.8b 12.8 ± 1.0f 27.4 ± 0.6e

61.8 ± 2.0b 11.0 ± 0.4g 26.8 ± 1.6c

< 0.5 5.1 6.5

0.051 0.019 0.025

92.7 ± 7.0b

74.3 ± 2.0h

38.1 ± 1.3d

13.5 ± 0.6g


102 ± 4.8a

62.3 ± 5.0i

64.5 ± 4.5c

21.0 ± 2.4d

37.8 ± 2.8de

87.3 ± 5.0g

16.9 ± 0.83f

12.6 ± 0.6g






All the values are referred to the fresh weight of plants. a ePRTE, equivalent Peroxyl Radical Trapping Efficiency. Values are expressed in terms of millimoles of Trolox equivalent present in 1 Kg of food. b PRTC, Peroxyl Radical Trapping Capacity. Values are expressed in term of millimoles of peroxyl radicals (LOO◦ ) trapped by 1 Kg of food. c FRAP = ferric reducing antioxidant power. Values are expressed in term of millimoles of iron reduced by 1 kg of food. d TP, Total Phenols content from Folin-Ciocalteu method. Values are expressed as millimoles of gallic acid equivalent per kilogram of food. e Quantified as chlorogenic acid. f Quantified as cyanidin 3-glucoside. N.M. = not measurable. Statistical difference between plants were analyzed by ANOVA (LSD, P ≤0.05). Means with the same letter within a column were not significantly different (a to l).

Table 3–Comparison of antioxidant properties of prebuggiun plants. Prebuggiun plants Hyoseris radiata L. Reichardia picroides (L.) Roth Plantago lanceolata L. Sonchus oleraceus L. Foeniculum vulgare Miller Sanguisorba minor L. Centranthus ruber (L.) DC. Rumex crispus L. Ranunculus ficaria L Silene vulgaris (Moench) Garcke Chicorium intybus L. (Verona Red Chicory) Vaccinium myrtillus (wild blueberry) Chicorium intybus L. (wild chicory)







5.3b 4.5bc 3.3d 4.7b 4.1c 0.7f 2.1e 0.6fg 0.7fg 0.2g 6.9a 4.9b 3.0d

8.6a 6.7b 8.1a 6.9b 5.9c 2.2f 4.8d – 3.0e – 5.5c 3.0e 6.9b

0.61d 0.67dc 0.41e 0.68c 0.69c 0.33f 0.43e – 0.23g – 1.25b 1.64a 0.43e

1.6de 1.7d 1.6d 1.7d 1.6de 2.6b 1.3f 2.1c 1.2fg 1.0g 2.8b 3.1a 1.3ef

0.30d 0.38d 0.48d 0.36d 0.39d 3.68b 0.61d 3.70b 1.66c 4.83a 0.41d 0.63d 0.45d

0.18h 0.25ef 0.20fgh 0.25efg 0.27e 1.21a 0.27e – 0.39d – 0.51c 1.04b 0.19gh

Different letters within a column (a to h) indicate significant difference, analyzed by LSD test, P ≤ 0.05.

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between the PRTC and FRAP values, which reflects the relationship between the H and the electron exchange ability of the plants we have examined, is poor (r = 0.51). To this regard, the strong electron donating ability of Sanguisorba minor L. appears to be not paralleled to it by H-donation ability. In fact, the value of the ratio FRAP/PRTC is the highest among those of the plants we have examined. The large variations of the ratios ePRTE/TP and of PRTC/TP, see Table 3 columns 2 and 3, are an indication of the different quality of the polyphenols present in the wild herbs we have studied. Multiple linear regression test indicate that the antioxidant properties of the plants we have reported in Table 2 can be predicted from a linear combination of important phenolic constituents (TP, hydroxycinnamic acids, anthocyanins, which were considered as independent variables and are expressed as millimoles per kilogram of fresh weight). The obtained multiple linear regression equations are the following:

In this case, the independent variables TP and hydroxycinnamic acids appear to account for the ability to predict PRTC being P = 0.002, 0.011, 0.64 for TP, hydroxycinnamic acids, anthocyanins, respectively. FRAP = −25.7 + 2.75 ∗ TP + 0.11 ∗ hydroxycinnamic acids + 4.81 ∗ anthocyanins; r = 0.99.

In this case, the independent variables TP and anthocyanins appear to account for the ability to predict FRAP being P < 0.001, 0.89, 0.038 for TP, hydroxycinnamic acids, and anthocyanins, respectively. In particular, from this analysis it appears that the important role of hydroxycinnamic acids and of anthocyanins is to determine the ePRTE of TP and of hydroxycinnamic acids to determine the PRTC and of TP to determine FRAP values. It is worth underlining that the radical trapping activities (measured by ePRTE and PRTC values) of the prebuggiun herbs were assessed in a system that mimics the conditions occurring in the upper small intestine, where peroxidation of the poly-unsaturated fatty acids present in foods may easily occur and where the antioxePRTE = −29.1 + 0.93 ∗ TP + 6.23 ∗ hydroxycinnamic acids idants present in these plants provide a real protection, since there are no bioavailability problems. + 14.9 ∗ anthocyanins; r = 0.89. It is interesting to compare the antioxidant characteristics of In this case, all the independent variables appear to contribute boiled prebuggiun (a mixture containing 20 g of each wild herbs to the prediction of ePRTE being P = 0.008, <0.001, < 0.001 of Table 1) with those of some vegetables which are usually eaten boiled. In general, according to Figure 2, it appears that about 70% for TP, hydroxycinnamic acids, and anthocyanins, respectively. or more of the original activity of these vegetables is present in the PRTC = −16.9 + 2.35 ∗ TP + 7.52 ∗ hydroxycinnamic acids cooking water, while from 30% to 44% of this activity is retained by boiled prebuggiun, and in much lower amount (in some case + 2.77 ∗ anthocyanins; r = 0.90. practically disappeared) by boiled spinach (Spinacea oleracea L.) and

Figure 2–Antioxidant properties of raw and boiled Spinacea oleracea L., Cichorium intybus L. var. foliosum and Prebuggiun plants. Black bars represent the raw herbs, light grey bars represent boiled herbs (15 min at 100 ◦ C), dark grey bars represent the cooking water (12.4 mL/g of fresh weight). Values are the mean ± SD (n = 4).

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catalogna (Cichorium intybus L. var. foliosum). As a consequence, the antioxidant properties of the boiled prebuggiun are significantly higher than those of boiled spinach and of boiled Cichorium intybus L. var. foliosum (P < 0.001). Furthermore, 2 more consideration can be done: (1) the antioxidant properties of boiled prebuggiun are higher than that of fresh spinach and of fresh Cichorium intybus L. var. foliosum (P < 0.007); (2) in the case of these latter vegetables the ePRTE, PRTC, and FRAP values after boiling (boiled vegetable + cooking water) are below to that of fresh vegetables (P < 0.05), while in the case of prebuggiun after boiling (boiled vegetable + cooking water) ePRTE (P = 0.017) and TP (P = 0.001) values appear significantly higher than those of fresh vegetables. This behavior may indicate that, during boiling, hydrolytic processes may occur increasing the antioxidant activity. The valuable antioxidant activity of some plants of prebuggiun is very high with respect of other plants of Mediterranean area. In fact Salvatore and others (2005) examined wild plants of Sicily very rich of antioxidant and found that Cichorium intybus (wild chicory), which has been used from immemorial time as vegetable in the Mediterranean area, has a significant high total antioxidant activity value with respect to other wild green herbs frequently eaten of this region, such as Sinapsis incana, Sinapsis nigra, Diplotaxis erucoides, Asparagus acutifolious, and Borrago officinalis. In the case of prebuggiun, herbs it appears that 7 or more of these plants present antioxidant parameters higher to that of wild Cichorium intybus that we have examined.

Conclusions For the first time, the antioxidant properties of prebuggiun were studied. These properties appear very relevant with respect to those of other wild plants of the Mediterranean flora and to those of red chicory and blueberry, which are, in the case of vegetables and fruits, among the richest of antioxidants. Therefore these properties, and in particular those related to capacity and efficiency in trapping LOO◦ characterizing some wild herbs present in prebuggiun, appear important given the extremely limited number of plants used in modern diets, which may be improved if more antioxidant-rich plants are considered as possible food.

References Adam M, Dobias P, Eisner A, Ventura K. 2009. Extraction of antioxidants from plant using ultrasonic methods and their antioxidant capacity. J Sep Sci 32(2):288–94. Ayoub NA. 2003. Unique phenolic carboxylic acids from Sanguisorba minor. Phytochemistry 63(4):433–6. Benzie IFF, Strain JJ. 1996. The Ferric Reducing Ability of Plasma (FRAP) as a measure of ‘Antioxidant Power’: the FRAP assay. Anal Biochem 239(1):70–6. Bisio A, Minuto L. 1999. The prebuggiun. In: Pieroni A, editor. Erbi boni, Erbi degli streghi. Good weeds, witches’ weeds. Cologne: Experiences Verlag Koln. p 34–46. Conforti F, Sosa S, Marrelli M, Menichini F, Statti GA, Uzunov D, Tubaro A, Menichini F. 2009. The protective ability of Mediterranean dietary plants against the oxidative damage: the role of radical oxygen species inflammation and the polyphenol, flavonoid and sterol contents. Food Chem 112(3):587–94. El-Mousallamy AMD. 2002. Polyphenols of Egyptian Rosaceae plants: two new flavonoid glycosides from Sanguisorba minor Scop. Pharmazie 57(10):702–4. Galvez M, Martin-Cordero C, Houghton PJ, Ayuso MJ. 2005. Antioxidant activity of methanol extracts obtained from Plantago species. J Agric Food Chem 53(6):1927–33.

Garc´ıa-Lafuente A, Guillam´on E, Villares A, Rostagno MA, Mart´ınez JA. 2009. Flavonoids as anti-inflammatory agent: implications in cancer and cardivascular disease. Inflamm Res 58(9):537–52. Gruenwald J. 2009. Novel botanical ingredients for beverages. Clin Dermatol 27(2):210–6. Guarrera PA. 2003. Food medicine and minor nourishment in the folk traditions of Central Italy (Marche, Abruzzo and Latium). Fitoterapia 74(6):515–44. Heinrich M, Leonti M, Nebel S, Peschel W, Pieroni A, Smith F, Rivera D, Obon C, Inocencio C, Verde A, Fajardo J, Llorach R, Muller WE, Eckert GP, Schaffer S, Schmitt-Schillig S, Antonopoulou S, Kypriotakis Z, Manios Y, Nomikos T, Kaliora A, Sidossis L, Galli C, Visioli F, Grande S, Bogani P, de Saizieu A, Fluhmann B, D’Orazio D, Fowler A, Koj A, Bereta J, Dulak J, Guzdek A, Kapiszewska M, The local Food-Nutraceuticals Consortium. 2005. Understanding local Mediterranean diets: a multidisciplinary pharmacological and ethnobotanical approach. Pharmacol Res 52(4):353–66. Herold A, Cremer L, Calug˘aru A, Tamas V, Ionescu F, Manea S, Szegli G. 2003. Antioxidant properties of some hydroalcoholic plant extracts with anti-inflammatory activity. Roum Arch Microbiol Immunol 62(3–4):217–27. Herrero M, Cifuentes A, Ibanez E. 2006. Sub- and supercritical fluid extraction of functional ingredients from different natural sources: plants, food-by-products, algae and microalgae. A review. Food Chem 98(1):136–48. Huber GM, Rupasinghe HPV. 2009. Phenolic profiles and antioxidant properties of apple skin extracts. J Food Sci 74(9):C693–700. La Vecchia C. 2009. Association between Mediterranean dietary patterns and cancer risk. Nutr Rev 67(S1):S126–9. Lee KW, Kim YJ, Lee HJ, Lee CY. 2003. Cocoa has more phenolic phytochemicals and a higher antioxidant capacity than teas and red wine. J Agric Food Chem 51(25):7292–5. Lee J, Koo N, Min DB. 2004. Reactive oxygen species, aging, and antioxidative nutraceuticals. Compr Rev Food Sci F 3(1):21–33. Manios Y, Antonopoulou S, Kaliora AC, Felliou G, Perrea D. 2005. Dietary intake and biochemical risk factors for cardiovascular disease in two rural regions of Crete. J Physiol Pharmacol 56:171–81. Mimaki Y, Fukushima M, Yokosuka A, Sashida Y, Furuya S, Sakagami H. 2001. Triterpene glycosides from the roots of Sanguisorba officinalis. Phytochem 57(5):773–9. Mohamed R, Pineda M, Aguilar M. 2007. Antioxidant capacity of extracts from wild and crop plants of the Mediterranean region. J Food Sci 72(1):S59–63. Mustafa RA, Abdul Hamid A, Mohamed S, Abu Bakar F. 2010. Total phenolic compounds, flavanoids, and radical scavenging activity of 21 selected tropic plants. J Food Sci 75(1):C28–34. Paoletti MG, Dreon AL, Lorenzoni GG. 1995. Pistic, traditional food from Western Friuli, NE Italy. Econ Bot 49(1):26–30. Parejo I, Jauregui O, S´anchez-Rabaneda F, Viladomat F, Bastida J, Codina C. 2004. Separation and characterization of phenolic compounds in fennel (Foeniculum vulgare) using liquid chromatography-negative electrospray ionization tandem mass spectrometry. J Agric Food Chem 52(12):3679–87. Rossetto M, Lante A, Vanzani P, Spettoli P, Scarpa M, Rigo A. 2005. Red chicories as potent scavengers of highly reactive radicals: a study on their phenolic composition and peroxyl radical trapping capacity and efficiency. J Agric Food Chem 53(21):8169–75. Rossetto M, Vanzani P, De Marco V, Zennaro L, Scarpa M, Rigo A. 2008. Fast and simple method for the simultaneous evaluation of the capacity and efficiency of food antioxidants in trapping peroxyl radicals in an intestinal model system. J Agric Food Chem 56(10):3486–92. Salvatore S, Pellegrini N, Brenna OV, Del Rio D, Frasca G, Brighenti F, Tumino R. 2005. Antioxidant characterization of some Sicilian edible wild greens. J Agric Food Chem 53(24):9465–71. Trichopoulou A. 2001. Mediterranean diet: the past and the present. Nutr Metab Cardiovasc Dis 11(4S):1–4. Tabart J, Kevers C, Pincemail J, Defraigne JO, Dommes J. 2010. Evaluation of spectrophotometric methods for antioxidant compound measurement in relation to total antioxidant capacity in beverage. Food Chem 120(2):607–14. Tosetti F, Noonan DM, Albini A. 2009. Metabolic regulation and redox activity as mechanisms for angioprevention by dietary phytochemicals. Int J Cancer 125(9):1997–2003. Vlcek J, Klejdus B, Kuban V. 2002. Determination of phenolic substances in plant materials by capillary electrophoresis and liquid chromatography. Chem Listy 96(1):39–44. Willett WC, Sacks F, Trichopoulou A, Drescher G, Ferroluzzi A, Helsing E, Trichopoulos D. 1995. Mediterranean diet pyramid: a cultural model for healthy eating. Am J Clin Nutr 61(6):S1402–6. Zeghichi S, Kallithraka S, Simopoulos AP, Kypriotakis Z. 2003. Nutritional composition of selected wild plants in the diet of Crete. World Rev Nutr Diet 91:22–40. Zennaro L, Rossetto M, Vanzani P, De Marco V, Scarpa M, Battistin L, Rigo A. 2007. A method to evaluate capacity and efficiency of water soluble and H-donor antioxidants as peroxyl radical scavengers. Arch Biochem Biophys 462(1):38–46. Zaporozhets OA, Krushinsksya EA, Barvinchenko VN, Lipkovskaya NA, Pogorelyi VK. 2003. Spectrophotometric determination of hydroxycynnamic acid and related compounds in Echinacea preparations. Pharm Chem J 37(12):632–6. Yang Z, Zhai W. 2010. Identification and antioxidant activity of anthocyanins extracted from the seed and cob of purple corn (Zea mays L.). Innov Food Sci Emer Technol 11(1):169–76.

Vol. 76, Nr. 1, 2011 r Journal of Food Science C51

C: Food Chemistry

Wild plants as source of antioxidants . . .

Wild Mediterranean Plants as Traditional Food: A Valuable Source of Antioxidants