comparative activity of antioxidants from wheat sprouts, morinda citrifolia ...

Comparative activity of antioxidants from wheatsprouts, Morinda citrifolia, fermented papaya andwhite tea

ISABELLA CALZUOLA, GIAN LUIGI GIANFRANCESCHI, &

VALERIA MARSILI

Dipartimento di Biologia Cellulare e Ambientale, Universita di Perugia, Italy, and Centro di

Eccellenza Materiali Innovativi e Nanostrutturati (CEMIN), Universita di Perugia, Italy

AbstractHydroalcoholic extracts from wheat sprouts, white tea, Morinda citrifolia and fermented papayawere analysed to determine their reducing power and antioxidant activity. The results show thatthe micromoles of potassium ferricyanide reduced by a quantity of extract corresponding to 1 gof the various dehydrated starting tissues are: 12.919/0.83 (wheat sprouts), 10.669/1.22 (M.citrifolia ), 17.069/1.24 (white tea), and 1.059/0.09 (fermented papaya). In addition the resultsshow a strong oxygen superoxide scavenging activity in the extracts from white tea, M. citrifoliaand wheat sprouts. The activity of the fermented papaya extract is the lowest. The thin-layerchromatography and UV spectrophotometry of the extracts show in each source a mixture ofantioxidant compounds probably belonging to the families of reducing glycosides andpolyphenols. The chromatographic pattern of the antioxidant compounds and the UV spectrumare quite different in the various sources.

Keywords: Antioxidants, radical scavenger activity, wheat sprouts, white tea, Morinda

citrifolia, fermented papaya

Introduction

An imbalance in the oxidant/antioxidant status of the cell is associated with oxidative

stress, and this has been related to aging and to several diseases (Droge 2002). In

particular there is evidence that reactive oxygen species production may be involved in

the pathogenesis of diabetes mellitus, atherosclerosis, neurodegenerative diseases and

cancer. Moreover, the radical-mediated oxidative damage will contribute to the

progress of the aging process (Harman 1981). Great interest has consequently been

focused on the study of natural products with antioxidant activity. The beneficial

effects of fruits and vegetables are mostly supported by epidemiological research

(Eicholzer et al. 2001; Chylack et al. 2002; Mayne 2003). However the activity of

antioxidants has been also directly demonstrated in animals carrying oxidative stress-

related diseases. Successful treatment of severe atopic dermatitis-complicated cataract

with a natural product antioxidant has been reported (Niwa et al. 1998). De la Fuente

(2002), together with other authors, has shown that dietary antioxidants supplemen-

Correspondence: Valeria Marsili, Universita di Perugia, Dipartimento di Biologia Cellulare e Ambientale,

Via Elce di Sotto, 06123 Perugia, Italy. Tel: 39 75 5855766. Fax: 39 75 5855762. Email:[email protected]

ISSN 0963-7486 print/ISSN 1465-3478 online # 2006 Informa UK Ltd

DOI: 10.1080/09637480600658328

International Journal of Food Sciences and Nutrition,

May/June 2006; 57(3/4): 168�177

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tation preserve an adequate function of immune cells against homeostatic distur-

bances caused by oxidative stress, such as that involved with age. Diets containing

high levels of antioxidants such as vitamins C and E seem able to reduce, in the

laboratory, age-related immune dysfunctions and arteriosclerosis in animals (Miquel

2002). Moreover, diet supplementation with coenzyme Q10, a-lipoic acid and the

glutathione precursors thioproline and N-acethylcysteine may protect the mitochon-

dria against respiration-linked oxygen stress (Miquel 2002).

It is also evident from the literature on the subject that the beneficial activity of

antioxidants has been frequently demonstrated in experiments performed with

mixtures of antioxidant molecules rather than with single compounds. In this context

we showed that wheat seeds synthesize a powerful mixture of antioxidants during

germination (Calzuola et al. 2004). Moreover we reported that a synergic effect, by

the different antioxidant compounds present in wheat sprouts, may be hypothesized,

keeping in mind that the antioxidant activity of a compound is dependent on its redox

potential. Therefore, the presence of a series of compounds with different redox

potentials could strengthen the ability to protect against an oxidative insult. The low

molecular weight antioxidant molecules present in the wheat sprouts are mainly

represented by reducing glycosides and polyphenolic compounds. In this paper we

report the results of a research project carried out to compare the activity of the

mixture of antioxidant compounds isolated from wheat sprouts with that of claimed

sources of antioxidants such as Morinda citrifolia (Sang et al. 2001a), fermented

papaya (Imao et al. 1998) and white tea (Yen and Chen 1995). Superoxide scavenging

and total reducing activities have been measured. The classes of compounds

potentially involved in the antioxidant activity were studied by thin-layer chromato-

graphy (TLC) and UV spectrophotometry of the extract obtained from each source.

Materials and methods

Reagents

All reagents were of pure analytical grade. Hypoxanthine, xanthine oxidase from

bovine erythrocytes, phosphomolybdic acid, 5,5?-dithiobis-2-nitrobenzoic acid, po-

tassium ferricyanide and nitrotetrazolium blue chloride were obtained from Sigma

Chemical Co. (St Louis, MO, USA).

Materials utilized for the study of the antioxidant activity

Wheat (from organic agriculture) sprout powder, prepared as previously reported

(Calzuola et al. 2004), was obtained from Germinal Life S.r.l. (Perugia, Italy). M.

Citrifolia dry extract (Noni) was obtained from Sangalli S.r.l. (Treviglio (Bg), Italy).

Fermented papaya powder was obtained from the commercial product Immun’Age

(produced by OSATO International, Inc., Ibi-gun Gifu, Japan), which is composed of

100% fermented papaya powder. White tea was purchased in a drug store.

Preparation of the extracts

Two grams of the aforementioned materials were suspended and homogenized (by

means of a Waring Blendor) with 40 ml water�ethanol (30/70, v/v) and centrifuged at

10,000�/g for 30 min at 48C. After storage at 48C for 24 h, the extract was again

Comparative activity of antioxidants 169

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centrifuged at 10,000�/g for 30 min at 48C. The ethanol was then removed by

evaporation and the aqueous residue lyophilized. All of the dried extracts, after

lyophilization, were resuspended in 2 ml water (water-soluble compounds [WSC]

extract). The residual water-insoluble material was collected by centrifugation, dried

under vacuum and extracted with 2 ml ethanol (ethanol-soluble compounds [ESC]

extract).

Nitrotetrazolium blue chloride (superoxide scavenging assay)

Scavenging activity of the superoxide radical generated ‘in vitro ’ by the hypoxanthine�xanthine oxidase system was measured following the inhibition of nitrotetrazolium

blue chloride reduction, using the method described by Kirby and Schmidt (1997).

Details of some changes we made were reported previously (Calzuola et al. 2004).

Total reducing power

The total reducing power of the extracts was measured by utilizing potassium

ferricyanide as the reagent, following the method of Yen and Chen (1995). Details of

some changes we made were reported previously (Calzuola et al. 2004).

Thin-layer chromatography

TLC was performed on silica gel plates using as solvent systems either propanol/water

70/30 (v/v) or ethylacetate/acetone/chloroform/formic acid/water 55/30/15/10/10 (v/

v). After drying, the plates were sprayed with 10% phosphomolybdic acid solution in

ethanol (w/v) and heated at 1208C until spot formation was obtained (Krebs et al.

1969). Phosphomolybdic acid in the presence of reducing substances is transformed

into molybdenum blue, which is visible on the TLC sheet as a blue spot. In some

experiments, the plates were sprayed with ninhydrin reagent to detect free amino

groups or with Folin�Ciacolteu reagent to detect phenols or orcinol�ferric chloride�sulphuric acid and p-anisaldehyde�sulphuric acid reagent to show the presence of

monosaccharides and oligosaccharides.

UV spectrophotometry

The extracts obtained from the various sources following suitable dilution in water

were analysed by UV spectrophotometry from 200 to 400 nm, utilizing a Varian, Cary

100, spectrophotometer.

Results

TLC analysis

TLC analysis (solvent, propanol/water 70/30, v/v) of the WSC extract from wheat

sprouts shows, after staining with phosphomolybdic acid, a main spot (Rf�/0.65)

(Figure 1a). We previously reported that this compound is represented by an

antioxidant glycoside with molecular weight 688 (Calzuola et al. 2004). This molecule

is more soluble in water than in ethanol; accordingly, the TLC of the ESC extract

performed in the same conditions shows a spot with the same Rf value (0.65) but of

less intensity (Figure 1b). Thin layer chromatographies of WSC and ESC extracts

170 I. Calzuola et al.

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from wheat sprouts were repeated by utilizing another solvent system (ethylacetate/

acetone/chloroform/ formic acid/water 55/30/15/10/10 (v/v)). The main hydrophilic

antioxidant compound (WSC extract) as already described shows a small spot (Rf�/

0.55) (Figure 1c) because a main portion of the compound remains near the starting

point while this solvent, on the contrary, clearly demonstrates in the ESC extracts

more hydrophobic compounds with a high Rf value, probably represented by

polyphenols (Figure 1d).

TLC in propanol/water (70/30, v/v) was subsequently performed with WSC

extracts of wheat sprouts, white tea, M. citrifolia and fermented papaya. As expected,

the silica gel plates after staining with phosphomolybdic acid show in the WSC extract

from each source several antioxidant molecules but the chromatographic patterns are

quite different. It is noteworthy that the extract of fermented papaya shows the lowest

content of compounds stained by phosphomolybdic acid (Figure 2a). The main spot

of WS detectable in Figure 2a, different from that of white tea, is also present in Figure

2c. The ninhydrin staining demonstrated that significant amounts of NH2 free groups

are present only in white tea and wheat sprouts. TLC of ESC extracts from white tea,

M. citrifolia and fermented papaya does not show detectable compounds following

staining with phosphomolybdic acid (data not shown).

Radical scavenging activity

The kinetics of radical scavenging activity by the extracts from the various sources is

reported in Figure 3. This activity is expressed as nmoles of scavenged oxygen

superoxide that can be computed from the absorbance decrease at 550 nm of the

reaction mixture, as previously reported (Calzuola et al. 2004). The results show a

strong radical scavenging activity in the extracts from white tea, M. citrifolia and wheat

sprouts. The activity of the fermented papaya extract is remarkably lower. In this

Figure 1. Ascendant TLC chromatography on silica gel plates (10�/20 cm) of WSC extract (a and c) and

ESC extract (b and d) from wheat sprouts. Solvent systems: (a) and (b) propanol/water 70/30(v/v), (c) and

(d) ethylacetate/acetone/chloroform/formic acid/water 55/30/15/10/10 (v/v). The plates were stained with

phosphomolybdic acid.


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context we repeated the experiments with fermented papaya by utilizing a twice higher

extract concentration and also an aqueous extract obtained by homogenizing the

papaya powder only with water. This taking into consideration the possibility that

the antioxidant compounds from fermented papaya could be not completely soluble in

the hydroalcoholic solvent (water/ethanol, 30/70, v/v). The results (Figure 4) are

comparable with those reported in Figure 3.

Figure 2. Ascendant TLC chromatography on silica gel plates (10�/20 cm) of WSC extract from white tea

(WT), M. citrifolia (MC), wheat sprouts (WS), and fermented papaya (FP). Solvent system: propanol/water

70/30 (v/v). The plates were stained with (a) phosphomolybdic acid, (b) ninhydrin, or (c) p -anisaldehyde/

sulphuric acid reagent.

0

2

4

6

8

10

12

14

16

0 20 40 60 80

time (min)

O2- s

cave

ng

ed (

nm

ole

s)

Figure 3. Kinetics of O2� scavenging activity of extracts from white tea (�/), M. citrifolia (^), wheat sprouts

(k), and fermented papaya (I). The values are expressed as nmoles of O2� radical scavenged by the

antioxidant compounds extracted from 10 mg of the various dehydrated vegetal tissues.


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0

0.5

1

1.5

2

2.5

3

0 10 20 30 40 50 60 70

time (min)

O2- s

cave

ng

ed (

nm

ole

s)

Figure 4. Kinetics of O2� scavenging activity of extracts from fermented papaya (FP). The values are

expressed as nmoles of O2� radical scavenged by the antioxidant compounds isolated in the hydroalcoholic

or aqueous extract. Aqueous extract from 10 mg (^) or 20 mg (�/) FP; hydroalcoholic extract from 10 mg

(k) or 20 mg (I) FP.

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

2

Wheat sprout Morinda Citrifolia White Tea Fermented Papaya

µmo

les

of

red

uce

d f

erri

cyan

ide

Figure 5. Total reducing power measured by potassium ferricyanide reagent. The values are expressed as

micromoles of ferricyanide reduced by WSC extract from white tea, M. citrifolia , wheat sprouts, and

fermented papaya. The amount of extract utilized in this assay corresponds to 100 mg of the various

dehydrated starting materials. The results represent the mean of three different experiment9/ standard

deviation.


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Reducing activity

The reducing power of the extracts from the various sources is reported in Figure 5.

This activity is expressed as micromoles of reduced potassium ferricyanide that can be

computed from the absorbance at 700 nm of the reaction mixture, as previously

reported (Calzuola et al. 2004). The data demonstrate that the extracts from white

tea, M. citrifolia and wheat sprouts contain high levels of molecules able to perform

the reduction of potassium ferricyanide. The reducing power of fermented papaya is

much lower.

UV spectrophotometry

The UV spectrum from 200 to 400 nm of the extracts from the various sources is

reported in Figure 6. The extracts, from white tea, M. citrifolia and wheat sprouts were

diluted 1:400 with water (v/v). The spectrum of the fermented papaya extract was

performed at a dilution of 1:5 with water (v/v). The analysis of the UV spectra shows,

0

0.5

1

1.5

2

2.5

3

3.5

200 240 280 320 360 400nm

Abso

rban

ce

1

2

3

4

Figure 6. Absorption spectra from 200 to 400 nm of WSC extracts from M. citrifolia (1), white tea (2),

fermented papaya (3), and wheat sprouts (4). Before the spectrophotometric analysis the extracts obtained

from M. citrifolia , white tea and wheat sprouts as described in Materials and methods were diluted 1:400 in

water (v/v); the extract from fermented papaya was diluted 1:5 in water (v/v).


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in the extract from each source, at suitable dilution, one or two characteristic peaks:

M. citrifolia , 252 nm�/290 nm (Figure 6b); white tea, 272 nm (Figure 6a);

fermented papaya, 263 nm�/302 nm (shoulder) wheat sprouts, 266 nm (Figure 6c);

(Figure 6d).

Discussion

According to the experimental procedure described in Materials and methods, the

hydroalcoholic extracts from the various sources, following ethanol evaporation, were

lyophilized and the dried material was resuspended in water (WSC extract). The

majority of the material appears soluble in water. The small residual water-insoluble

material was solubilized in ethanol (ESC extract). In addition, the analysis of the

radical scavenging and reducing activities shows that the majority of the antioxidant

compounds (�/90%) are recovered in the WSC extracts (data not shown). Following

these observations the comparative analysis of the antioxidant activity, here reported,

concerns the activity performed by the WSC extracts.

All the results described in this paper demonstrate that the mixture of antioxidant

compounds extracted from wheat sprouts, M. citrifolia and white tea shows a strong

activity both for superoxide radical scavenging and for potassium ferricyanide

reduction. All the UV absorbance spectra reported in Figure 6 are consistent with

glycoside or polyphenolic structures (He et al. 1996; Marin et al. 2004) even if they do

not allow us to identify specific compounds. The TLC chromatographic pattern of the

extract from wheat sprouts is represented by a main compound belonging to the

reducing glycoside class. It is noteworthy that this compound together with other

more hydrophobic molecules characterizes the germination of wheat sprouts. The

antioxidant activity observed with the wheat sprout extracts is in agreement with

previously reported results according to which wheat sprout extract contains

antioxidant compounds active in the protection of DNA against the oxidative stress

induced by the Fenton reaction (Fe2�/H2O2). A 50% protective effect on strand

breakage of pBR322 plasmid DNA (10 mg/ml) induced by hydroxyl radicals formed

via the Fenton reaction (10 mM Fe2� and 100 mM H2O2) was obtained with 0.5 mg/

ml wheat sprouts extract (Falcioni et al. 2001). This result may be also related to the

antimutagenic effect demonstrated with aqueous wheat sprout extracts (Peryt et al.

1988, 1992; Tudek et al. 1988). As far as the study of the antioxidant compounds

from tea is concerned, at first white tea was selected because it represents the sprouts

of tea (Santana-Rios et al. 2001) and it is dehydrated by air drying process without

involving treatment at high temperature. Consequently it appears very interesting that

the TLC patterns of wheat sprouts and white tea following staining with ninhydrin are

rather similar (Figure 2b). Ninhydrin reacts with proteinaceus material that also

includes cellular structural molecules; therefore some similarities between wheat

sprout cells and white tea cells may be taken for granted, even if the TLC patterns of

the antioxidant compounds from these two sources are different (Figure 2a). The

strong antioxidant activity, shown by the extract from M. citrifolia, is in agreement

with the complex mixture of antioxidant compounds observed in Figure 2a. This may

be related to polyphenolic or in any case to aromatic structures shown also by the

absorption spectrum between 240 and 300 nm, and it is in agreement with the

previously reported presence in this plant of iridoid glycosides (Sang et al. 2001b) and

flavonolglycosides (Sang et al. 2001a).


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Surprisingly, the antioxidant activity shown by the extracts from fermented papaya

is clearly lower than that obtained with the extracts from the other sources utilized in

this study. Of course this observation is restricted to the antioxidant activities that can

be measured by the methods we used in this study. Moreover, the discrepancy with the

result of Imao et al. (1998) could only be apparent because the scavenging activity on

the hydroxyl radicals was obtained by these authors with a high concentration of

fermented papaya (IC50, 12.5 mg/ml). In addition they also reported that fermented

papaya extract exerts slight scavenging activity for superoxide radicals (Imao et al.

1998). The results reported in this paper provides a sharp indication that the mixture

of powerful antioxidant compounds found in several vegetal tissues may be a potent

protection for man against the pathologies linked to oxidative stress. In this context we

stress the importance of natural sources that not only supply a series of natural

antioxidant compounds, but supply them in natural ratios between themselves.

Moreover, evidence for the intestinal absorption of low molecular antioxidant

compounds that contain an aromatic moiety has been reported (Day et al. 1998;

Boyle et al. 2000; Yamashita et al. 2002). In this context we have underlined the

nutritional relevance of wheat sprouts in order to strengthen antioxidant defence

(Marsili et al. 2004).

Acknowledgements

The authors would like to thank Mrs Barbara Urquhart for the English revision of this

paper.

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