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Antioxidant properties of phenolic compounds occurring in edible mushrooms

I. Palacios
a
, M. Lozano
a
, C. Moro
a
, M. DArrigo
a
, M.A. Rostagno
a
, J.A. Martnez
a,b
, A. Garca-Lafuente
a
,
E. Guillamn
a
, A. Villares
a,
a
Centro para la Calidad de los Alimentos, Instituto Nacional de Investigacin y Tecnologa Agraria y Alimentaria (INIA), Campus Duques de Soria, c/ Jos Tudela s/n, 42004 Soria, Spain
b
Universidad de Navarra, Dpto. de Fisiologa y Nutricin, Edicio de Investigacin, c/ Irunlarrea, 1, 31008 Pamplona, Spain
a r t i c l e i n f o
Article history:
Received 16 September 2010
Received in revised form 26 January 2011
Accepted 21 March 2011
Available online 25 March 2011
Keywords:
Phenolic
Flavonoid
Antioxidant
Mushroom
a b s t r a c t
Total phenolic and avonoid contents occurring in eight types of edible mushrooms (Agaricus bisporus,
Boletus edulis, Calocybe gambosa, Cantharellus cibarius, Craterellus cornucopioides, Hygrophorus marzuolus,
Lactarius deliciosus and Pleurotus ostreatus) have been respectively evaluated by the FolinCiocalteau
assay and by the colorimetric reaction with NaNO
2
and AlCl
3
in a basic media. Generally, the assayed
mushrooms contained between 1 and 6 mg of phenolics per gram of dried mushroom, depending on
the species, while the avonoid concentrations ranged between 0.9 and 3.0 mg per gram of dried matter.
The prole and concentration of individual phenolics was determined by means of high performance
liquid chromatography. Homogentisic acid was the free phenolic acid signicantly present in all mush-
rooms although the content varied considerably among the analysed species. Flavonoids, such as myrice-
tin and catechin were also detected in the mushrooms studied. The antioxidant properties of the
methanolic extracts from mushrooms were evaluated by monitoring the linoleic acid autoxidation, and
all the mushrooms species showed inhibition, with C. cibarius being the most effective against lipid oxi-
dation (74% of inhibition) and A. bisporus the species with lowest antioxidant activity (10% of inhibition).
2011 Elsevier Ltd. All rights reserved.
1. Introduction
In recent times, amounts of consumed mushrooms have risen
greatly, involving a large number of species, due to continuous
developments in cultivation, harvest, postharvest, processing and
storage treatments, which facilitates the consumption throughout
the year. Besides the nutritional properties (Barros, Baptista, Estev-
inho, & Ferreira, 2007; Manzi, Aguzzi, & Pizzoferrato, 2001), mush-
rooms have been demonstrated to possess healthy properties
(Lindequist, Niedermeyer, & Julich, 2005) and they have proved
to be effective as antiinammatory, antitumour, antibacterial, anti-
oxidant and antiviral agents (Barros, Baptista, Estevinho, et al.,
2007; Barros et al., 2007; Chen, Wang, & Wu, 2009; Dore et al.,
2007; Faccin et al., 2007; Garca-Lafuente et al., 2010); further-
more, they show antiallergic, antiatherogenic, hypoglycemic and
haematological properties (Guillamn et al., 2010; Hossain et al.,
2003; Yoshino et al., 2008); and they are involved in immunomod-
ulating therapies (Wasser, 2002). Among the biologically active
substances present in mushrooms, phenolics have attracted much
attention due to their superb properties as antioxidant, antiinam-
matory or antitumour agents, among others (Puttaraju, Venkate-
shaiah, Dharmesh, Urs, & Somasundaram, 2006). Phenolic
compounds are aromatic hydroxylated compounds, possessing
one or more aromatic rings with one or more hydroxyl groups.
They include a large number of subclasses, such as avonoids, phe-
nolic acids, including hydroxybenzoic acids and hydroxycinnamic
acids, stilbenes, lignans, tannins, and oxidised polyphenols, dis-
playing a great diversity of structures (Cote, Caillet, Doyon, Sylvain,
& Lacroix, 2010; DArchivio, Filesi, Vari, Scazzocchio, & Masella,
2010).
Among the protective actions in biological systems, phenolic
compounds exhibit antioxidant activity. Thus, phenolics can be
classied as free radical inhibitors (chain breaker), peroxide
decomposers, metal inactivators or oxygen scavengers (Dziezak,
1986; Yagi, 1970). Biological antioxidant capacity can be measured
by controlling the inhibition of induced lipid oxidation (Watanabe,
Nakajima, & Konishi, 2008). These methods induce the autoxida-
tion of linoleic acid or low-density lipoproteins (LDL) by Cu(II) or
an azo initiator and control the formation of conjugated diene per-
oxides. Free radicals, generated by the initiator, react with oxygen
species yielding peroxide radicals which attack the lipids to form
the conjugated diene peroxides. Therefore, the scavenging of free
radicals or peroxide radicals by an antioxidant agent may avoid
the lipid oxidation in biological systems.
The antioxidant activity of phenolic-rich extracts is commonly
correlated with the total phenolic content, evaluated by means of
the FolinCiocalteau assay; nevertheless, individual phenolic com-
pounds could show markedly different antioxidant effects as a re-
sult of synergism, antagonism, co-antioxidation and the presence
of oxidation retarders (Becker, Nissen, & Skibsted, 2004). Therefore,
0308-8146/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodchem.2011.03.085

Corresponding author. Tel.: +34 975 233204; fax: +34 975 233205.
E-mail address: villares.ana@inia.es (A. Villares).
Food Chemistry 128 (2011) 674678
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it is desirable to carry out a thorough study of the mushrooms phe-
nolic prole in order to identify and quantify the active substances.
Although phenolic content has been evaluated for medicinal and
edible mushrooms by the FolinCiocalteau assay by several
authors (Barros, Baptista, Correia, Morais, & Ferreira, 2007; Barros,
Ventuizini, Baptista, Estevinho, & Ferreira, 2008; Ferreira, Baptista,
Vilas-Boas, & Barros, 2007; Ramrez-Anguiano, Santoyo, Reglero, &
Soler-Rivas, 2007), studies concerning the individual prole of phe-
nolic compounds in edible mushrooms are quite scarce.
In this work, we describe, apparently for the rst time, the anal-
ysis of the phenolic content occurring in edible mushrooms, both
cultivated and wild, and the identication and quantication of
the individual phenolic compounds responsible of the antioxidant
activity in terms of the inhibition of the linoleic acid oxidation.
2. Materials and methods
2.1. Samples
Wild mushrooms (Boletus edulis, Cantharellus cibarius, Craterel-
lus cornucopioides, Calocybe gambosa, Hygrosphorus marzuolus and
Lactarius deliciosus) and cultivated mushrooms (Agaricus bisporus
and Pleurotus ostreatus) were purchased from local market and
they came from different regions from Spain. The mushrooms
were immediately lyophilised (Telstar Cryodos), and kept at 4 C
in hermetically vacuum-sealed plastic bags (Tecnotrip) up to
analysis.
2.2. Standards and reagents
FolinCiocalteau phenol reagent, linoleic acid, 2,2
0
-azobis-(2-
amidinopropane)-dihydrochloride (ABAP), NaCO
3
, NaNO
2
, AlCl
3
and NaOH were analytical grade (Sigma Chemical Co.). Acetonitrile
99.9%, methanol 99.8% and glacial acetic acid 100% were of HPLC-
grade from BDH Prolabo Pestinorm (VWR International). The water
was treated in a Milli-Q water purication system (Advantage A10
purier from Millipore). The standards (caffeic acid, catechin,
chlorogenic acid, p-coumaric acid, ferulic acid, gallic acid, gentisic
acid, homogentisic acid, p-hydroxybenzoic acid, myricetin, proto-
catechuic acid and pyrogallol) were purchased from Sigma Chem-
ical Co. The standard stock solutions (0.251 lg/ml) were made
with methanol (HPLC-grade).
2.3. Phenolic compounds extraction
Samples were freeze-dried and nely milled. Mushroom
powder (0.20 g) was extracted by stirring with methanol
(2 ml) at 65 C for 24 h. Then, the mixture was centrifugated
at 3000 rpm for 10 min. The residue was re-extracted twice
and the methanolic extracts were combined and evaporated to
dryness under vacuum. Samples were redissolved in methanol
and ltered through a 0.20 lm disposable LC lter disk prior
to HPLC analysis.
2.4. Total phenolic content
The phenolic compounds content in the mushroom methano-
lic extracts was estimated by means of the FolinCiocalteau as-
say described by Singleton and Rossi with minor modications
(Singleton & Rossi, 1965). Gallic acid was used to calculate the
standard curve (0.010.7 mM; r
2
> 0.999). Estimation of the phe-
nolic compounds was carried out in sixtuplicate (n = 6). The re-
sults were expressed as mg of gallic acid equivalents per gram
of dried mushroom.
2.5. Total avonoid content
The avonoid compounds concentration in the methanolic ex-
tracts from the mushrooms was evaluated by the colorimetric as-
say previously described (Balbaa, Zaki, & Elshamy, 1974) with
some modications. Catechin was employed to calculate the stan-
dard curve of the described method (0.031.00 mM; r
2
> 0.999).
Estimation of the avonoids was six times repeated (n = 6). The re-
sults were expressed as mg of catechin equivalents per gram of
dried mushroom.
2.6. Analysis of phenolic compounds
The phenolic extracts were analysed using an Alliance

HPLC
system 2695 (Waters). Separation was achieved on a Symmetry
(Waters) reverse phase C
18
column (3.5 lm, 75 mm, 4.6 mm i.d.)
thermostatted at 25 C. The sample volume injection was 10 ll. A
solvent system consisting of 0.1% acetic acid in water (solvent A)
and acetonitrile (solvent B) was used with the following gradient:
starting with 100% A and installing a gradient to obtain 5% B at
2 min, 40% B at 20 min and 80% B at 22 min, according to the meth-
od previously described with slight modications (Kim et al.,
2008). The solvent ow rate was 1 ml/min.
Phenolic compounds were identied on the basis of the reten-
tion times of standard materials and the quantication was
achieved by the absorbance recorded in the chromatograms rela-
tive to external standards, at 280 nm for catechin, cinnamic acid,
gallic acid, homogentisic acid, p-hydroxybenzoic acid, proto-
catechuic acid and pyrogallol; and 320 nm for caffeic acid, chloro-
genic acid, p-coumaric acid, ferulic acid, gentisic acid, myricetin
and naringin. All standard calibration curves showed high degrees
of linearity (r
2
> 0.99).
2.7. Inhibition of ABAP-induced lipid peroxidation
Linoleic acid solutions (0.25 M) were treated with 50 ll of the
methanolic extracts from edible mushrooms and 50 ll of 2,2
0
-azo-
bis-(2-amidinopropane)-dihydrochloride (ABAP) were added while
stirring. Changes in absorbance at 234 nm with time were mea-
sured by means of a Jenway 6305 spectrophotometer. Methanol
was employed as blank according to previously described methods
(Pryor et al., 1993).
2.8. Statistical analysis
The analysis of phenolic compounds contents in each mush-
room species was carried out six times (n = 6) and the results ex-
pressed as mean values standard deviation (SD).
3. Results and discussion
The total phenolic contents for the analysed edible mushrooms
evaluated by the FolinCiocalteau method are shown in Fig. 1. Re-
sults are expressed as mg of gallic acid equivalents per gram of
dried mushroom. Among the studied species, B. edulis presents
the highest contents of phenolics, A. bisporus also shows a large
content while other studied species have lower phenolic concen-
trations, with H. marzuolus presenting the lowest amount.
In order to obtain more information about the nature of the
phenolic substances occurring in the mushrooms, the total avo-
noid content was measured. Flavonoids form red complexes with
aluminium chloride in alkaline media (Turner, 1952). The determi-
nation is highly selective for the avonoid structure since the iso-
avone derivatives give no colour with aluminium chloride (Balbaa
et al., 1974). Total avonoid content of the studied mushrooms is
I. Palacios et al. / Food Chemistry 128 (2011) 674678 675
shown in Fig. 2. The data are depicted as mg of catechin equiva-
lents per gram of dried mushroom. To the best of our knowledge,
total avonoid content of edible mushrooms has not been evalu-
ated yet. The concentration varies depending on the mushroom
species and the total avonoid content does not correlate with
the phenolic concentration. Thus, L. deliciosus has the higher
amount and A. bisporus, P. ostreatus and C. gambosa present the
lower avonoid content.
The FolinCiocalteu assay is highly sensitive for monohydric
phenols, polyphenols, avonoids and tannins; however, the meth-
od could overestimate the total phenolic content since other read-
ily oxidised substances, such as sugars, ascorbic acid, aminoacids
(tyrosine, trytophan), etc. could interfere by reacting with the col-
orimetric reagent (a mixture of phosphotungstic and phosphomo-
libdic acids). Furthermore, phenolics with more than one hydroxyl
group are expected to double the molar colour yield; however, ste-
ric effects or substitutions in the aromatic ring could modify the
expected response since the hydroxyl groups are not accessible
for the chromophore reagent.
The individual prole of phenolic compounds can be obtained
by high-performance liquid chromatography coupled to photodi-
ode array detector (HPLC-DAD). Fig. 3A depicts a typical HPLC
chromatogram of the phenolic acids (caffeic acid, catechin,
chlorogenic acid, p-coumaric acid, ferulic acid, gallic acid, gentisic
acid, homogentisic acid, p-hydroxybenzoic acid, myricetin,
protocatechuic acid and pyrogallol) recorded at 280 nm. Phenolics
occurring in edible mushrooms were identied by comparison of
the absorption spectrum and the retention time with the corre-
sponding standards. Fig. 3B shows a representative HPLC chro-
matogram of the C. cornucopioides mushroom monitored at
280 nm and the phenolics content of the studied mushrooms is
shown in Table 1.
Homogentisic acid was the only free phenolic acid signicantly
present in all mushrooms although the content varies considerably
among species. Thus, B. edulis, A. bisporus and C. gambosa contain
between 2.5 and 4.5 mg of homogentisic acid per gram of dried
mushroom while C. cornucopioides, P. ostreatus, L. deliciosus, H. mar-
zuolus and C. cibarius contain less than 1 mg/g. Gallic acid, possibly
conjugated, is also present in all mushrooms, although less abun-
dant than homogentisic, it is the second main component of the
phenolic acids in the studied mushrooms (0.10.3 mg/g). Conju-
gated pyrogallol is present in A. bisporus and C. gambosa (approxi-
mately 0.25 mg/g) and also detected in C. cornucopioides, C.
cibarius, and L. deliciosus in lower amounts. Protocatechuic and p-
hydroxybenzoic acids occur in all mushroom species in similar
concentrations (ca. 0.03 mg/g, varying from 0.005 to 0.04 mg/g) ex-
cept in B. edulis where the protocatechuic acid content is consider-
ably higher (0.17 mg/g). All mushrooms, except A. bisporus and C.
cornucopioides, contain gentisic acid, showing P. ostreatus and H.
marzuolus the higher contents. Chlorogenic acid is present in A.
bisporus, C. gambosa, B. edulis and L. deliciosus in comparable con-
centration (ca. 0.06 mg/g). Other phenolic acids, such as caffeic,
p-coumaric and ferulic are also detected (less than 0.02 mg/g). Fi-
nally, the studied edible mushrooms present low quantities of
myricetin (around 0.02 mg/g) except H. marzuolus that does not
contain this avonoid and C. cornucopioides whose content is
0.035 mg/g. Other avonoids are detected in the edible mushroom
such as catechin, which is found in very low quantity in A. bisporus
and C. cibarius.
There are few studies concerning the individual proles of
phenolic compounds in edible mushrooms. Cultivated species
are better known in terms of composition; however, wild mush-
rooms are scarcely studied and, to the best of our knowledge, the
phenolic composition of the species C. cornucopioides, C. gambosa,
and H. marzuolus has not been previously described. For the
other species (A. bisporus, B. edulis, C. cibarius, L. deliciosus and
P. ostreatus), the experimental data are comparable to those re-
ported in bibliography (Barros, Duenas, Ferreira, Baptista, & San-
tos-Buelga, 2009; Ferreira, Barros, & Abreu, 2009; Kim et al.,
2008; Valentao et al., 2005), bearing in mind that the specic
and characteristic composition of each mushroom may be associ-
ated with the environmental factors of their harvest conditions.
The proportion of homogentisic acid, however, is higher than in
all above-cited mushrooms from different geographical origins
(Kim et al., 2008).
In Fig. 4 the rate of linoleic acid oxidation is depicted with and
without the methanolic extracts from edible mushrooms. The oxi-
dation increases signicantly during the rst minute and then it
reaches a constant value. When methanolic extracts from edible
mushrooms are added, the oxidation yield decreases in a different
percentage depending on the mushroom studied. The percent inhi-
bition was calculated using the following expression:
%Inhibition 100 A A
extract
=A
A is the absorbance of the control (without the extract) and A
ex-
tract
is the absorbance of the test sample (methanolic extracts from
edible mushrooms). Results are shown in Fig. 5. Methanolic
extracts from C. cibarius and C. cornucopioides show the higher
inhibition of the linoleic acid oxidation, 74% and 70%, respectively;
L. deliciosus, C. gambosa and H. marzuolus inhibit approximately
50% of the oxidation (50%, 48% and 46%, respectively) and B. edulis
Fig. 1. Concentrations of total phenolic compounds in eight edible mushrooms, A.
bisporus, B. edulis, C. gambosa, C. cibarius, C. cornucopioides, H. marzuolus, L. deliciosus
and P. ostreatus, expressed as mg of gallic acid equivalents per gram of dried
mushroom. Vertical bars indicate the standard deviation (n = 6).
Fig. 2. Concentrations of total avonoids in eight edible mushrooms expressed as
mg of catechin equivalents per gram of dried mushroom. Vertical bars indicate the
standard deviation (n = 6).
676 I. Palacios et al. / Food Chemistry 128 (2011) 674678
and P. ostreatus inhibit 36% of the lipid oxidation. Finally, A.
bisporus is the species with the lowest antioxidant activity (10%
of inhibition). Phenolic compounds are responsible for the antiox-
idant activity; however, the inhibition extent does not correlate
nor with the total phenolic amount nor with the avonoid content,
which may indicate that each phenolic compound or a group of
them must possess different antioxidant activity. Homogentisic
acid, in spite of being the most abundant compound, does not cor-
relate with the antioxidant efciency of the mushrooms, which
indicates that the activity of this compound is not signicant. C.
cibarius and C. cornucopioides show the greatest antioxidant effect.
Regarding to the phenolic compounds occurring in the mushrooms
studied, C. cornucopioides contains the highest myricetin amount
and C. cibarius shows greater amounts of caffeic acid and catechin
with respect to other species. This fact could indicate that these
phenolic compounds may show greater antioxidative power than
the others detected in these mushrooms since even relatively
low quantities inhibit the linoleic acid oxidation to a greater extent
than other compounds which are more abundant. The methanolic
extracts from L. deliciosus, C. gambosa and H. marzuolus inhibit
approximately 50% of the linoleic acid oxidation which can be cor-
related with the synergism among the different phenolics, avo-
noids and phenolic acids, occurring in the mushrooms. B. edulis
and P. ostreatus show lower antioxidant effect regarding the other
species. Apart from the homogentisic acid, the main phenolic com-
pounds found in P. ostreatus are p-coumaric, gallic and gentisic acid
while B. edulis contains p-hydroxybenzoic and protocatechuic acid.
The fact that methanolic extracts from both species show similar
antioxidant efciencies could be explained in terms of the occur-
ring phenolic acids activity, which may be comparable because
the chemical structure of these acids is quite similar and the mech-
anism involved in the antioxidant effect should be comparable. A.
bisporus inhibits 10% linoleic acid oxidation and it presents the
highest chlorogenic acid content, which could indicate that this
phenolic acid may inhibit to a lower extent the oxidation with re-
spect to the other phenolics studied.
Fig. 3. Chromatogram of phenolic compounds analysis by HPLC: (A) standard mixture of phenolics and (B) methanolic extract from C. cornucopioides. 1, pyrogallol; 2, gallic
acid; 3, homogentisic acid; 4, protocatechuic acid; 5, p-hydroxybenzoic acid; 6, catechin; 7, chlorogenic acid; 8, caffeic acid; 9, p-coumaric acid; 10, gentisic acid; 11, ferulic
acid; and 12, myricetin.
Table 1
Concentration of phenolic compounds found in eight edible mushrooms, A. bisporus, B. edulis, C. gambosa, C. cibarius, C. cornucopioides, H. marzuolus, L. deliciosus and P. ostreatus.
Results are expressed as lg of phenolics per gram of dried mushroom and the standard deviation is indicated in brackets (n = 6).
A. bisporus B. edulis C. cibarius C. cornucopioides C. gambosa H. marzuolus L. deliciosus P. ostreatus
Caffeic acid 15.54 15.09 16.34 n.d. 14.92 14.59 15.51 n.d.
(0.42) (1.07) (0.30) (0.02) (0.07) (0.51)
Catechin 0.51 n.d. 5.82 n.d. n.d. n.d. n.d. n.d.
(0.01) (0.74)
Chlorogenic acid 63.73 62.79 n.d. n.d. 63.04 n.d. 62.70 n.d.
(0.74) (0.70) (0.62) (0.21)
p-Coumaric acid 10.38 0.87 n.d. n.d. n.d. 4.69 n.d. 11.15
(0.10) (0.01) (0.19) (0.85)
Ferulic acid 16.37 n.d. 10.38 14.03 14.52 n.d. 11.43 20.16
(1.89) (0.40) (0.57) (0.55) (0.85) (0.16)
Gallic acid 94.90 212.96 161.83 118.78 113.24 165.20 162.42 290.34
(4.50) (8.25) (3.78) (2.01) (2.84) (3.48) (10.09) (3.61)
Gentisic acid n.d. 60.85 53.97 n.d. 38.55 158.46 57.67 292.62
(3.97) (1.31) (2.50) (2.48) (1.89) (3.42)
p-Hydroxybenzoic acid 15.39 24.07 15.68 6.28 11.30 5.49 21.40 4.69
(0.71) (0.89) (1.03) (0.27) (0.33) (0.48) (1.64) (1.59)
Homogentisic acid 3444.30 2290.97 316.76 851.86 4280.11 340.71 366.80 629.86
(15.87) (13.90) (9.46) (9.77) (7.03) (3.17) (7.91) (1.54)
Myricetin 22.26 17.98 23.27 35.91 20.75 n.d. 20.86 21.99
(1.72) (0.76) (0.29) (0.98) (0.39) (0.86) (0.89)
Protocatechuic acid 16.21 168.46 42.79 5.31 36.96 14.59 18.64 19.32
(4.78) (5.60) (1.42) (0.25) (2.54) (0.80) (0.32) (0.84)
Pyrogallol 258.70 n.d. 91.09 92.34 240.07 n.d. 26.28 n.d.
(3.95) (0.83) (1.69) (3.38) (0.30)
n.d.: not detected.
I. Palacios et al. / Food Chemistry 128 (2011) 674678 677
Acknowledgement
The authors are grateful to Ministerio de Ciencia e Innovacin
and INIA (projects AT07-003 and RTA2009-00049-00-00) for nan-
cial support of this work. M. Lozano, C. Moro and I. Palacios
acknowledge the award of their FPI INIA grants.
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Fig. 4. A representative UV trace of the inhibited autoxidation of linoleic acid
measured at 234 nm with and without the methanolic extracts from edible
mushrooms.
Fig. 5. Inhibition of linoleic acid oxidation by methanolic extracts from the studied
edible mushrooms. Results are expressed as % of inhibition with respect to
autoxidation without extract from mushrooms. Vertical bars indicate the standard
deviation (n = 4).
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