Ciencia y Tecnología AlimentariaSociedad Mexicana de Nutrición y Tecnología de Alimentossomenta@gmail.com ISSN (Versión impresa): 1135-8122ISSN (Versión en línea): 1696-2443MÉXICO

2007

E. Alvarez Parrilla / L. A. de la Rosa / N. R. Martínez / G. A. González Aguilar

TOTAL PHENOLS AND ANTIOXIDANT ACTIVITY OF COMMERCIAL AND WILD

MUSHROOMS FROM CHIHUAHUA, MEXICO

Ciencia y Tecnología Alimentaria, año/vol. 5, número 005

Sociedad Mexicana de Nutrición y Tecnología de Alimentos

Reynosa, México

pp. 329-334

Red de Revistas Científicas de América Latina y el Caribe, España y Portugal

Universidad Autónoma del Estado de México

http://redalyc.uaemex.mx

TOTAL PHENOLS AND ANTIOXIDANT ACTIVITY OF COMMERCIAL AND WILDMUSHROOMS FROM CHIHUAHUA, MEXICO

AbstractThree wild edible mushrooms (Agaricus sp., Boletus sp., and Macrolepiota sp.) from the North of Mexico (Chihuahua

state) and two commercial species (Agaricus bisporus white strain and Portabella: Agaricus bisporus brown strain) were

analyzed to determine their proximate composition, total phenols and antioxidant activity. Wild mushrooms presented lower

humidity values with respect to commercial species. Other proximate parameters such as total protein, lipids, ashes and

carbohydrates were similar to those reported for edible mushrooms. Total phenols and antioxidant activity (Ferric Reducing/

Antioxidant Power assay, FRAP) were determined from 80 % methanol extracts. Wild Mushrooms had higher phenol content

and antioxidant capacity than commercial mushrooms. A direct correlation between phenols and antioxidant activity (r2 =

0.986) was observed. Due to these characteristics, wild mushrooms could be considered as a complement in the diet for the

health benefits they present.

ResumenSe analizó la composición proximal, fenoles totales y capacidad antioxidante, de tres hongos silvestres (Agaricus

sp., Boletus sp., and Macrolepiota sp.) del norte de México (Chihuahua) y dos comerciales (Agaricus bisporus cepa blanca

and Portalella: Agaricus bisporus cepa café). Los hongos silvestres presentaron valores menores de humedad que los

comerciales. Los demás parámetros proximales (proteínas, lípidos, cenizas y carbohidratos totales) fueron similares a los

reportados para hongos silvestres. La concentración de fenoles totales y actividad antioxidante (Ferric Reducing/Antioxidant

Power assay, FRAP) se determinaron a partir de extractos con metanol al 80 %. Los hongos silvestres presentaron valores

más altos en fenoles totales y actividad antioxidante, frente a los hongos comerciales. Se observó una correlación directa

(r2 = 0,986) entre fenoles totales y actividad antioxidante. Estas características de los hogos silvestres hacen que puedan

ser considerados, como complemento de la dieta ya que puede presentar buenos beneficios en la salud.

Keywords: Edible mushrooms, proximate composition, polyphenols, antioxidant activity, FRAP

Palabras clave: Hongos comestibles, análisis proximal, polifenoles, actividad antioxidante, FRAP

FENOLES TOTALES Y CAPACIDAD ANTIOXIDANTE DE HONGOS COMERCIALES Y SILVESTRES DECHIHUAHUA, MÉXICO

Alvarez-Parrilla, E.1*; de la Rosa, L. A.1; Martínez, N. R.1; González Aguilar, G. A.2

1Departamento de Ciencias Básicas, Universidad Autónoma de Ciudad Juárez (UACJ), Instituto de Ciencias

Biomédicas, Anillo Envolvente del PRONAF y Estocolmo s/n, Ciudad Juárez, Chihuahua, CP 32310, México. 2Centro

de Investigación en Alimentación y Desarrollo, A. C. (CIAD, A. C.), Dirección de Tecnología de Alimentos de Origen

Vegetal, Carretera a la Victoria Km 0.6, La Victoria, Hermosillo, Sonora, CP 83000, México

Recibido/Received 11-06-2007; aceptado/accepted 07-08-2007

*Autor para la correspondencia/Corresponding author. E-mail: ealvarez@uacj.mx

329

INTRODUCTION

Reactive oxygen species (ROS) are formed during

the normal cellular metabolism, however, when the

concentration increase, they overcome the physiologic

antioxidant mechanisms and become toxic. Epidemiological

studies correlate high ROS values with DNA damage, heart

diseases, cancer and other chronic and degenerative

diseases (Tesoriere et al., 2004). There are several cellular

defenses against elevated levels of free radicals, such as

the enzymes superoxide dismutase, catalase or glutathione

peroxidase, which protect the organism against ROS.

Ingestion of exogenous antioxidants through fruit and

vegetable rich diets can also help neutralize these free

radicals, and consequently decrease the prevalence of

several diseases (Ferreira et al., 2007). For this reason,

during the last decade, an increase in the consumption of

antioxidants-rich foods such as fruits and vegetables has

been observed.

Among the antioxidant compounds, polyphenols

have gained importance due to their large array of

biological actions that include free radical scavenging,

metal chelation and enzyme modulation activities,

inhibition of LDL oxidation, among others (Rodrigo and

Bosco, 2006). The term polyphenol refers to a complex

group of compounds that includes in their structure an

aromatic ring bearing one or more hydroxyl groups. They

include simple phenols such as phenolic acids and

derivatives, as well as complex structures such as flavones,

flavonoids, anthocyanins, among others.

Cienc. Tecnol. Aliment. 5(5) 329-334 (2007)

www.somenta.org/journal ISSN 1135-8122SOMENTASociedad Mexicana de Nutrición

y Tecnología de los Alimentos

CIENCIA Y

TECNOLOGÍA

ALIMENTARIA

330

Mushrooms have been used as traditional foods

and medicines in different parts of the world, including

Asia, Africa and America. In Mexico, wild edible

mushrooms have been part of the diet, especially among

ethnic groups. They have nutritional relevance due to their

high fiber, minerals and protein content, as well as low fat

content (León-Guzmán et al., 1997). Moreover, in the last

few years, an increasing interest in the consumption of

mushrooms has arisen, due to their elevated polyphenol

concentration, which correlates with an elevated

antioxidant activity. Several studies analyzing the total

phenols and antioxidant activity of fresh and cooked wild

and commercial mushrooms have been published (Mau et

al., 2001; Hsu et al., 2002; Mau et al., 2002; Yang et al.,

2002; Lakshmi et al., 2004; Lo and Cheung, 2005; Choi et

al., 2006; Ferreira et al., 2007). However, as far as we know,

characterization of species grown in different regions of

México has not been reported.

The objective of this study was to evaluate the

proximate composition, total phenols and antioxidant

activity of wild and commercial edible mushrooms from the

State of Chihuahua, in the north of Mexico.

MATERIALS AND METHODS

SamplesWild mushrooms (wild champignon: (Champignon

w) Agaricus sp., Boletus sp, and Macrolepiota sp.) were

collected at the end of the rain season at a Holm oak forest,

near Namiquipa (29°15’ latitude, 107°25’ longitude, and 1828

m over sea level), Chihuahua, Mexico, during September

2004. Five to ten mushrooms of each species (100 g to 1

kg, depending of the species) were collected and kept on

ice 4-6 h for transportation to the laboratory. Mushrooms

were classified only to genus, using macroscopic

characteristics. Especial care was taken not to collect toxic

specimens. We used this classification having in mind that

when people from the region collect wild mushrooms, they

usually collect different non toxic species of the same

genus, assuming that they are the same mushroom.

Commercial mushrooms (Champignon (champignon c):

Agaricus bisporus white strain and Portabella: Agaricus

bisporus brown strain) were purchased at a local

supermarket in Ciudad Juarez. Wild and commercial

mushrooms were cut, weighted and frozen at -80 °C for 1

day, lyophilized for 48 h (Labconco Freeze dry/shell freeze

system), milled and stored at -80 °C. In order to minimize

variability between individuals from the same species, all

mushrooms from the same specie were homogenized.

Proximate analysisMoisture content was determined by lyophilization

(48 h) in order to prevent polyphenol and antioxidant

activity losses. Protein, ash and fat were determined

according to the AOAC (2000) procedures. For protein

determination, a conversion factor of 4.38 was used, in

accordance with León-Guzmán et al., (1997). Total fat was

determined by Soxhlet extraction with hexane and total

carbohydrates were calculated by difference. Total energy

was calculated according to equation 1 (Manzi et al., 2004):

Energy (kcal) = 4(g protein + g carbohydrate) + 9(g fat) (1)

Total phenols determinationMushroom extracts were obtained according to the

methodology proposed by Kähkönen et al. (1999). Briefly,

0.1 g of powdered dried mushrooms was weighted into a

test tube. 5 mL of 80 % methanolic solution was added,

stirred and sonicated for 15 min in the dark. Then extract

was centrifuged (3000 g) for 10 min at 4 °C, and the

supernatant was collected. Extraction was repeated and a

total volume of 10 mL was obtained. This extract was used

for determination of total phenols and antioxidant activity.

Total phenols were determined according to the method

Cienc. Tecnol. Aliment. 5(5) 329-334 (2007) ISSN 1135-8122 ©2007 SOMENTA

Table 1. Proximate composition (%, fresh weight) of commercial and wild mushrooms. Means with different letters in the same row are

significantly different (LSD test, P < 0.05).

Tabla 1. Análisis proximal (% peso fresco) de los hongos comerciales y silvestres. Valores promedio con letras diferentes indican diferencia

significativa (prueba DMS, P< 0,05).

Portabella Commercial champignon

Macrolepiota Boletus Wild champignon

Moisture 91.13 ± 0.20a 90.63 ±2.04

a 86.08 ± 0.61

b 84.2 ± 2.96

b 77.57 ± 0.68

c

Ash 0.13 ± 0.002a 0.96 ± 0.03

b 0.50 ± 0.02

c 0.22 ± 0.03

d 1.17 ± 0.05

e

Total fat 0.70 ± 0.09a 0.29 ± 0.04

b 0.76 ± 0.11

a 0.62 ± 0.04

a 1.31 ± 0.06

c

Protein 2.32 ± 0.16a 3.16 ± 0.10

b 1.80 ± 0.20

c 2.62 ± 0.15

a 4.42 ± 0.16

d

Total

carbohydrates

5.72 4.96 10.86 12.34 15.52

Energy

(Kcal/100g FW)

38.4 35.0 57.5 65.4 91.6

331

reported by Georgé et al. (2005), with the Folin-Ciocalteu

reagent, using caffeic acid in methanol (80 %) as standard.

Absorbance at 760 nm was determined by using a BioRad

Benchmark Plus microplate reader, and results were

expressed as mg of caffeic Acid (CAE)/ 100 g fresh weight.

Antioxidant capacityAntioxidant capacity was determined by the ferric

reducing/antioxidant power assay (FRAP) according to

Benzie and Strain (1996) and modified by Alvarez-Parrilla

et al. (2005), with slight modifications. FRAP reagent was

daily prepared and kept at 37 °C, by mixing 0.3 M acetate

buffer, pH 3.6 with 10 mM 2,4,6-tripyridyl-s-triazine (TPTZ,

Acrôs Organics, USA) solution in 40 mM HCl plus 20 mM

FeCl3·6H

2O, at a 10:1:1 ratio. Assay solutions were prepared

by mixing 180 µL of FRAP reagent with 24 µL of 3: 1 water:

sample mixture, standard or 80% methanol (blank).

Methanolic solutions of Fe2+ (80%) in the range of 100-

3000 µM were prepared from a 3000 µM FeSO4·7H2O stock

solution to obtain the calibration curves. All measurements

were carried out at 37 °C. Absorbance was measured at

595 nm, every 30 s, during 60 min, using a BioRad

Benchmark Plus microplate reader. Results are reported as

mM Fe2+/100 g fresh mushroom.

Statistical analysisValues are presented as the mean ± SD of four

replicates. ANOVA and LSD analyses were performed in

order to determine differences between mushrooms, using

the commercial software SPSS 13.0 (SPSS Inc.

Headquarters Chicago, Illinois, USA).

RESULTS AND DISCUSSION

Proximate compositionMoisture was determined by lyophilization to

prevent polyphenol degradation and minimize antioxidant

activity loss. Table 1 shows the proximate composition of

wild and commercial mushrooms. Moisture values ranged

from 77.57 to 91.13 %. Commercial samples presented

statistically higher moisture values than wild samples. The

moisture values varied in the order Portabela > commercial

champignon > Macrolepiota > Boletus > wild champignon.

This may be explained by considering that wild mushrooms

were collected at the end of the raining season, when some

dehydration may have occurred. Exposure to different

ambient conditions of wild mushrooms affected

considerably moisture content. Meanwhile the growth of

commercial mushrooms is carried out at controlled

atmospheres and humidity. The higher moisture of

Portabella as compared to commercial champignon may be

explained considering that the former mushrooms are sold

in plastic packages, with moisture controlled atmosphere,

meanwhile, the later is sold in bulk, and consequently some

dehydration occurs. All mushrooms, except wild

champignon, which showed clear signs of dehydration,

had moisture values in the 85-92 % range. These results

are similar to those reported by other authors for fresh

mushrooms (León-Guzmán et al., 1997; Choi et al., 2006).

As expected, fat levels were low (0.29 to 1.13 % fresh

weight, FW; 3.05-7.85 % dried weight, DW), and similar to

those reported for several species of commercial and wild

mushrooms studied elsewhere (León-Guzmán et al., 1997;

Manzi et al., 2001; Manzi et al., 2004). Commercial and wild

champignon presented the lowest and highest fat levels,

respectively. Commercial champignon showed fat content

similar to those reported by Manzi et al. (2001) for raw and

canned champignon.

Protein content in the analyzed mushrooms ranged

from 1.8 to 4.42 % FW (12.95-33.73 % DW). These values

are higher to those reported by León-Guzman et al. (1997)

for wild mushrooms collected in Queretaro, Mexico (13.2-

17.5 % DW), but in the range of the commercial Italian fresh

mushrooms reported by Manzi et al. (2001, 2004).

Portabella (26.2 % DW) and commercial champignon

(33.73% DW) showed lower protein content than those

reported by Dikeman et al. (2005) for the same mushrooms

(42.4 and 37.5 %, respectively). However, the mushrooms

studied by Dikeman et al. (2005) presented lower moisture

content which affects directly protein content.

Total carbohydrate content, calculated by

difference, varied from 15.52 to 4.96 % FW (52.9-78.1 %

DW). These values are in the range of the commercial

Italian fresh mushrooms reported by Manzi et al. (2001;

2004). From the proximate composition, the energy

provided by 100 g of fresh samples was calculated and

ranged from 38.4 and 91.6 Kcal for Portabella and wild

champignon, respectively. These values are similar to those

reported by Manzi, et al. (2001, 2004) for Italian commercial

mushrooms. As already discussed, the higher energy value

of the champignon samples is due to the low water content

of this mushroom. From the low fat content and energy

value, it can be concluded that wild and commercial

mushrooms can be considered good alternatives for low

fat/energy diets.

Antioxidant activityIt is well known that polyphenols are one of the

major contributors to the antioxidant activity of fruits,

vegetables and mushrooms (Ferreira et al., 2007). For this

reason, in this study, total phenols concentration, and

antioxidant activity of commercial and wild mushrooms

were determined, from methanol:water (80:20) extracts. In

the literature, total phenolics of different plant tissues have

been reported either as Gallic Acid Equivalent (GAE) or as

pyrochatecol equivalent. In the present study, caffeic acid

was used as standard, since it has been reported as one of

the major phenolic compounds present in some wild and

commercial mushrooms (Valentão et al., 2005).

Figure 1 shows the total phenol concentration of

mushrooms, expressed as mg of caffeic acid equivalents

SOMENTA ©2007 Alvarez-Parrilla et al.: Total phenols and antioxidant activity of …

332

(CAE)/ 100 g of fresh weight. Phenolic concentration

ranged from 45.6 mg CAE/ 100 g FW for commercial

champignon to 308.3 mg CAE/ 100 g FW for wild

champignon. Figure 1 shows that both commercial species

presented statistically the same phenolic concentration,

and slightly lower than that for Macrolepiota. Boletus

presented a total phenol concentration of 169.6 ± 26.7 mg

CAE/100 g FW. The higher phenolic concentration

observed for wild champignon can be partially explained

considering its low water content due to dehydration. Wild

mushrooms presented, in general, statistically higher

phenolic concentration than commercial ones. The total

phenolic concentration of the samples analyzed in the

present study (4.87 to 13.74 mg CAE/ g DW) were higher

than those reported by Mau et al. (2002), and Choi et al.

(2006), but in the range of those reported by Lo and Cheung

(2005), Cheung et al. (2003), Yang et al. (2002), and Ferreira

et al. (2007) for different commercial and wild mushrooms

found world widespread.

The antioxidant activity of wild and commercial

mushrooms has been determined by several methods, such

as 2,2-diphenyl-1-pycrilhydracyl radical, DPPH (Mau et al.,

2001; Mau et al., 2002; Cheung et al., 2003; Lakshmi et al.,

2004; Ribeiro et al., 2006; Turkoglu et al., 2007), TEAC

(Lakshmi et al., 2004), conjugated diene method (Mau et

al., 2001; Mau et al., 2002), Ferricyanide reducing power

(Mau et al., 2001; Mau et al., 2002), and ferric reducing/

antioxidant power assay, FRAP (Lakshmi et al., 2004),

among others.

In the present work, antioxidant activity was

measured by the FRAP method, which measures the

capacity of an antioxidant to reduce a Fe3+-TPTZ complex

to Fe2+-TPTZ. In this way, a higher Fe3+-TPTZ reduction

means a higher antioxidant activity.

The original FRAP methodology proposed by

Benzie and Strain (1996) established a 4 min interval before

the determination of the FRAP value. However, as shown

in Figure 2a, and in agreement with Pulido et al. (2000) and

Alvarez-Parrilla et al. (2005), the reduction of Fe3+ to Fe2+

in the presence of the mushroom extract follows a slow

kinetic mechanism, and even after 30 min the reaction was

not totally completed. For this reason, FRAP values were

determined at 30 min, as suggested in the literature (Pulido

et al., 2000; Alvarez-Parrilla et al., 2005). When the FRAP

values determined at 4 and 30 min were compared, a 32-97

% increment was observed. However, the increment in the

FRAP values at 60 min was less than 20 % higher compared

to those observed at 30 min.

Figure 2b shows the FRAP values of the 80 %

methanolic mushroom extracts determined at 30 min and

expressed as mmol Fe2+/ 100 g FW. Figure 2b shows that

the antioxidant activity varied in a similar pattern than the

Figure 1. Total phenolic content (expressed as caffeic acid

equivalents, CAE/ 100 g FW) of 80% methanolic extracts from

wild and commercial mushrooms. Values are mean ± SD from four

determinations. Different letters in the bars indicate statistically

significant differences (LSD test, P < 0.05).

Figura 1. Concentración fenoles totales (expresado como

equivalentes de ácido caféico, CAE/ 100 g peso fresco) del extracto

metanol:agua 80:20 de los hongos comerciales y silvestres. Los

valores se reportan como media ± DS de cuatro repeticiones. Letras

diferentes en las barras indican diferencia significativa (prueba DMS,

P < 0,05).

Figure 2. Antioxidant activity, estimated by the FRAP assay

(expressed as mmol Fe2+/ 100 g FW) of (a) FRAP reaction kinetics

of 80 % methanolic extracts from wild and commercial mushrooms,

measure at 595 nm and (b) Ferric reducing ability of methanolic

extracts determined at 30 min. Values are mean ± SD from four

estimations. Different letters in the bars indicate statistically

significant differences (LSD test, P < 0.05).

Figura 2. Actividad antioxidante, determinada por el método FRAP

(expresado como mmol Fe2+/ 100 g peso fresco) de (a) cinética de

reacción FRAP de los extractos metanol:agua (80:20) de los hongos

comerciales y silvestres, determinado a 595 nm y (b) actividad

antioxidante de los extractos determinado a los 30 min. Los valores

se reportan como media ± DS de cuatro repeticiones. Letras diferentes

en las barras indican diferencia significativa (prueba DMS, P < 0,05).

Cienc. Tecnol. Aliment. 5(5) 329-334 (2007) ISSN 1135-8122 ©2007 SOMENTA

mg

CA

E/1

00 g

FW

0

100

200

300

400

a

b

c

a

d

Portabella Macrolepiota Champignon

(w)

Champignon

(c)

Boletus

3500

1000 2000 30000

3000

2500

2000

1500

1000

500

0

Abs

595 n

m

Portabella

Champignon (c)

Boletus

Macrolepiota

Champignon (w)

Time (s)

0

1

2

3

4

5

a,b

b

c

a

d

mm

ol

Fe2

+/1

00

g F

W

Portabella Macrolepiota Champignon

(w)

Champignon

(c)

Boletus

(A)

(B)

3500

1000 2000 30000

3000

2500

2000

1500

1000

500

0

Abs

595 n

m

PortabellaPortabella

Champignon (c)Champignon (c)

BoletusBoletus

MacrolepiotaMacrolepiota

Champignon (w)Champignon (w)

Time (s)

0

1

2

3

4

5

a,b

b

c

a

d

mm

ol

Fe2

+/1

00

g F

W

Portabella Macrolepiota Champignon

(w)

Champignon

(c)

Boletus

(A)

(B)

333

total phenolic concentration in the order: wild

champignon> Boletus > Macrolepiota >Portabela H =

commercial champignon. FRAP values ranged from 0.94

mmol Fe2+/ 100 g FW (10.01 mmol Fe2+/ 100 g DW) for

commercial champignon to 4.49 mmol Fe2+/ 100 g FW (20.03

mmol Fe2+/ 100 g DW) for wild champignon. Both

commercial mushrooms presented statistically lower FRAP

values, compared with wild mushrooms. Even though

Lakshmi et al. (2004) determined the antioxidant activity

of several Indian mushrooms with the FRAP method,

observing high FRAP values, however, our results can not

be compared with the former study, since they expressed

the antioxidant activity as TROLOX or ascorbic acid

equivalents. When the antioxidant activity values of the

wild and commercial mushrooms determined by the FRAP

method where compared with other fruits, it was observed

that mushrooms presented higher antioxidant activity than

those reported for peaches, which ranged from 0.84 to 1.2

mmol Fe2+/ 100 g FW (Rodrigo-García et al., 2006), but lower

than those for strawberries (19.3-24.4 mmol Fe2+/ 100 g DW)

(Böhm et al., 2006).

It has been reported that polyphenols are the main

contributors to the antioxidant activity of fruits and

vegetables (Mau et al., 2002), therefore a correlation study

between total phenols and antioxidant activity of wild and

commercial mushrooms was carried out. Figure 3 shows a

good correlation (R2 = 0.9721, significance level P < 0.002)

between these two parameters. This result indicates that

polyphenols may be the main antioxidant compounds

found in mushrooms, in agreement with several authors

(Lo and Cheung, 2005; Choi et al., 2006; Ferreira et al.,

2007). However it is important to evaluate the type of

phenol present in mushroom and its individual contribution

to the total antioxidant capacity. In this regards, studies

are in progress evaluating other phenols and antioxidants

present in mushrooms.

In conclusion, the results reveal that wild

mushrooms could be an important source for low caloric,

low fat functional foods, with high level of polyphenols

and antioxidant activity, especially for the ethnic groups

(Tarahumaras tribes) living in the North of Mexico. From

the wild mushrooms studied, «Boletus» may be an

interesting group due to their high nutritional value, total

phenol concentration and antioxidant activity, as well as

its high relative abundance in the region. As far as we

know, this is the first study of Mexican wild edible

mushrooms were in vitro antioxidant activity analysis was

evaluated and compared with commercial species.

ACKNOWLEDGEMENTS

Financial support from UACJ (internal projects) is

gratefully acknowledged. The authors would like to express

appreciation to Dr. Marcos Lizarraga for his helpful

assistance in collecting and identifying wild mushrooms

and to Héctor Osvaldo Sosa for technical assistance.

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