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TOTAL PHENOLS AND ANTIOXIDANT ACTIVITY

OF COMMERCIAL AND WILD MUSHROOMS FROM
CHIHUAHUA, MEXICO FENOLES TOTALESY CAPACIDAD
ANTIOXIDANTE DE HONGOS COMERCIALESY
SILVESTRES DE CHIHUAHUA, MÉXICO
a a a b
E. Alvarez-Parrilla , L. A. de la Rosa , N. R. Martínez & G. A. Aguilar González
a
Departamento 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
b
Centro 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
Published online: 02 Oct 2009.

To cite this article: E. Alvarez-Parrilla , L. A. de la Rosa , N. R. Martínez & G. A. Aguilar González (2007) TOTAL PHENOLS
AND ANTIOXIDANT ACTIVITY OF COMMERCIAL AND WILD MUSHROOMS FROM CHIHUAHUA, MEXICO FENOLES TOTALESY
CAPACIDAD ANTIOXIDANTE DE HONGOS COMERCIALESY SILVESTRES DE CHIHUAHUA, MÉXICO, Ciencia y Tecnologia
Alimentaria, 5:5, 329-334, DOI: 10.1080/11358120709487708

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 SOMENTA Cienc. Tecnol. Aliment. 5(5) 329-334 (2007) CIENCIA Y
Sociedad Mexicana de Nutrición www.somenta.org/journal ISSN 1135-8122 TECNOLOGÍA
y Tecnología de los Alimentos ALIMENTARIA

TOTAL PHENOLS AND ANTIOXIDANT ACTIVITY OF COMMERCIAL AND WILD

MUSHROOMS FROM CHIHUAHUA, MEXICO
FENOLES TOTALES Y CAPACIDAD ANTIOXIDANTE DE HONGOS COMERCIALES Y SILVESTRES DE
CHIHUAHUA, MÉXICO

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

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

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: [email protected]
Abstract
Three wild edible mushrooms (Agaricus sp., Boletus sp., and Macrolepiota sp.) from the North of Mexico (Chihuahua
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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.

Resumen
Se 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
INTRODUCTION several diseases (Ferreira et al., 2007). For this reason,
during the last decade, an increase in the consumption of
Reactive oxygen species (ROS) are formed during antioxidants-rich foods such as fruits and vegetables has
the normal cellular metabolism, however, when the been observed.
concentration increase, they overcome the physiologic Among the antioxidant compounds, polyphenols
antioxidant mechanisms and become toxic. Epidemiological have gained importance due to their large array of
studies correlate high ROS values with DNA damage, heart biological actions that include free radical scavenging,
diseases, cancer and other chronic and degenerative metal chelation and enzyme modulation activities,
diseases (Tesoriere et al., 2004). There are several cellular inhibition of LDL oxidation, among others (Rodrigo and
defenses against elevated levels of free radicals, such as Bosco, 2006). The term polyphenol refers to a complex
the enzymes superoxide dismutase, catalase or glutathione group of compounds that includes in their structure an
peroxidase, which protect the organism against ROS. aromatic ring bearing one or more hydroxyl groups. They
Ingestion of exogenous antioxidants through fruit and include simple phenols such as phenolic acids and
vegetable rich diets can also help neutralize these free derivatives, as well as complex structures such as flavones,
radicals, and consequently decrease the prevalence of flavonoids, anthocyanins, among others.

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

Mushrooms have been used as traditional foods specimens. We used this classification having in mind that
and medicines in different parts of the world, including when people from the region collect wild mushrooms, they
Asia, Africa and America. In Mexico, wild edible usually collect different non toxic species of the same
mushrooms have been part of the diet, especially among genus, assuming that they are the same mushroom.
ethnic groups. They have nutritional relevance due to their Commercial mushrooms (Champignon (champignon c):
high fiber, minerals and protein content, as well as low fat Agaricus bisporus white strain and Portabella: Agaricus
content (León-Guzmán et al., 1997). Moreover, in the last bisporus brown strain) were purchased at a local
few years, an increasing interest in the consumption of supermarket in Ciudad Juarez. Wild and commercial
mushrooms has arisen, due to their elevated polyphenol mushrooms were cut, weighted and frozen at -80 °C for 1
concentration, which correlates with an elevated day, lyophilized for 48 h (Labconco Freeze dry/shell freeze
antioxidant activity. Several studies analyzing the total system), milled and stored at -80 °C. In order to minimize
phenols and antioxidant activity of fresh and cooked wild variability between individuals from the same species, all
and commercial mushrooms have been published (Mau et mushrooms from the same specie were homogenized.
al., 2001; Hsu et al., 2002; Mau et al., 2002; Yang et al.,
2002; Lakshmi et al., 2004; Lo and Cheung, 2005; Choi et Proximate analysis
al., 2006; Ferreira et al., 2007). However, as far as we know, Moisture content was determined by lyophilization
characterization of species grown in different regions of (48 h) in order to prevent polyphenol and antioxidant
México has not been reported. activity losses. Protein, ash and fat were determined
The objective of this study was to evaluate the according to the AOAC (2000) procedures. For protein
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proximate composition, total phenols and antioxidant determination, a conversion factor of 4.38 was used, in
activity of wild and commercial edible mushrooms from the accordance with León-Guzmán et al., (1997). Total fat was
State of Chihuahua, in the north of Mexico. 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):
MATERIALS AND METHODS Energy (kcal) = 4(g protein + g carbohydrate) + 9(g fat) (1)

Samples Total phenols determination

Wild mushrooms (wild champignon: (Champignon Mushroom extracts were obtained according to the
w) Agaricus sp., Boletus sp, and Macrolepiota sp.) were methodology proposed by Kähkönen et al. (1999). Briefly,
collected at the end of the rain season at a Holm oak forest, 0.1 g of powdered dried mushrooms was weighted into a
near Namiquipa (29°15’ latitude, 107°25’ longitude, and 1828 test tube. 5 mL of 80 % methanolic solution was added,
m over sea level), Chihuahua, Mexico, during September stirred and sonicated for 15 min in the dark. Then extract
2004. Five to ten mushrooms of each species (100 g to 1 was centrifuged (3000 g) for 10 min at 4 °C, and the
kg, depending of the species) were collected and kept on supernatant was collected. Extraction was repeated and a
ice 4-6 h for transportation to the laboratory. Mushrooms total volume of 10 mL was obtained. This extract was used
were classified only to genus, using macroscopic for determination of total phenols and antioxidant activity.
characteristics. Especial care was taken not to collect toxic Total phenols were determined according to the method

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 Macrolepiota Boletus Wild

champignon champignon
Moisture 91.13 ± 0.20a 90.63 ±2.04a 86.08 ± 0.61b 84.2 ± 2.96b 77.57 ± 0.68c
Ash 0.13 ± 0.002a 0.96 ± 0.03b 0.50 ± 0.02c 0.22 ± 0.03d 1.17 ± 0.05e
Total fat 0.70 ± 0.09a 0.29 ± 0.04b 0.76 ± 0.11a 0.62 ± 0.04a 1.31 ± 0.06c
Protein 2.32 ± 0.16a 3.16 ± 0.10b 1.80 ± 0.20c 2.62 ± 0.15a 4.42 ± 0.16d
Total 5.72 4.96 10.86 12.34 15.52
carbohydrates
Energy 38.4 35.0 57.5 65.4 91.6
(Kcal/100g FW)

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

reported by Georgé et al. (2005), with the Folin-Ciocalteu champignon, which showed clear signs of dehydration,
reagent, using caffeic acid in methanol (80 %) as standard. had moisture values in the 85-92 % range. These results
Absorbance at 760 nm was determined by using a BioRad are similar to those reported by other authors for fresh
Benchmark Plus microplate reader, and results were mushrooms (León-Guzmán et al., 1997; Choi et al., 2006).
expressed as mg of caffeic Acid (CAE)/ 100 g fresh weight. As expected, fat levels were low (0.29 to 1.13 % fresh
weight, FW; 3.05-7.85 % dried weight, DW), and similar to
Antioxidant capacity those reported for several species of commercial and wild
Antioxidant capacity was determined by the ferric mushrooms studied elsewhere (León-Guzmán et al., 1997;
reducing/antioxidant power assay (FRAP) according to Manzi et al., 2001; Manzi et al., 2004). Commercial and wild
Benzie and Strain (1996) and modified by Alvarez-Parrilla champignon presented the lowest and highest fat levels,
et al. (2005), with slight modifications. FRAP reagent was respectively. Commercial champignon showed fat content
daily prepared and kept at 37 °C, by mixing 0.3 M acetate similar to those reported by Manzi et al. (2001) for raw and
buffer, pH 3.6 with 10 mM 2,4,6-tripyridyl-s-triazine (TPTZ, canned champignon.
Acrôs Organics, USA) solution in 40 mM HCl plus 20 mM Protein content in the analyzed mushrooms ranged
FeCl3·6H2O, at a 10:1:1 ratio. Assay solutions were prepared from 1.8 to 4.42 % FW (12.95-33.73 % DW). These values
by mixing 180 µL of FRAP reagent with 24 µL of 3: 1 water: are higher to those reported by León-Guzman et al. (1997)
sample mixture, standard or 80% methanol (blank). for wild mushrooms collected in Queretaro, Mexico (13.2-
Methanolic solutions of Fe2+ (80%) in the range of 100- 17.5 % DW), but in the range of the commercial Italian fresh
3000 µM were prepared from a 3000 µM FeSO4·7H2O stock mushrooms reported by Manzi et al. (2001, 2004).
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solution to obtain the calibration curves. All measurements Portabella (26.2 % DW) and commercial champignon
were carried out at 37 °C. Absorbance was measured at (33.73% DW) showed lower protein content than those
595 nm, every 30 s, during 60 min, using a BioRad reported by Dikeman et al. (2005) for the same mushrooms
Benchmark Plus microplate reader. Results are reported as (42.4 and 37.5 %, respectively). However, the mushrooms
mM Fe2+/100 g fresh mushroom. studied by Dikeman et al. (2005) presented lower moisture
content which affects directly protein content.
Statistical analysis Total carbohydrate content, calculated by
Values are presented as the mean ± SD of four difference, varied from 15.52 to 4.96 % FW (52.9-78.1 %
replicates. ANOVA and LSD analyses were performed in DW). These values are in the range of the commercial
order to determine differences between mushrooms, using Italian fresh mushrooms reported by Manzi et al. (2001;
the commercial software SPSS 13.0 (SPSS Inc. 2004). From the proximate composition, the energy
Headquarters Chicago, Illinois, USA). 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
RESULTS AND DISCUSSION reported by Manzi, et al. (2001, 2004) for Italian commercial
mushrooms. As already discussed, the higher energy value
Proximate composition of the champignon samples is due to the low water content
Moisture was determined by lyophilization to of this mushroom. From the low fat content and energy
prevent polyphenol degradation and minimize antioxidant value, it can be concluded that wild and commercial
activity loss. Table 1 shows the proximate composition of mushrooms can be considered good alternatives for low
wild and commercial mushrooms. Moisture values ranged fat/energy diets.
from 77.57 to 91.13 %. Commercial samples presented
statistically higher moisture values than wild samples. The Antioxidant activity
moisture values varied in the order Portabela > commercial It is well known that polyphenols are one of the
champignon > Macrolepiota > Boletus > wild champignon. major contributors to the antioxidant activity of fruits,
This may be explained by considering that wild mushrooms vegetables and mushrooms (Ferreira et al., 2007). For this
were collected at the end of the raining season, when some reason, in this study, total phenols concentration, and
dehydration may have occurred. Exposure to different antioxidant activity of commercial and wild mushrooms
ambient conditions of wild mushrooms affected were determined, from methanol:water (80:20) extracts. In
considerably moisture content. Meanwhile the growth of the literature, total phenolics of different plant tissues have
commercial mushrooms is carried out at controlled been reported either as Gallic Acid Equivalent (GAE) or as
atmospheres and humidity. The higher moisture of pyrochatecol equivalent. In the present study, caffeic acid
Portabella as compared to commercial champignon may be was used as standard, since it has been reported as one of
explained considering that the former mushrooms are sold the major phenolic compounds present in some wild and
in plastic packages, with moisture controlled atmosphere, commercial mushrooms (Valentão et al., 2005).
meanwhile, the later is sold in bulk, and consequently some Figure 1 shows the total phenol concentration of
dehydration occurs. All mushrooms, except wild mushrooms, expressed as mg of caffeic acid equivalents

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

400
3500
c Portabella
(A)
Champignon (c)
3000 Boletus
300 Macrolepiota
mg CAE/100 g FW

2500 Champignon (w)

Abs 595 nm
d
200 2000

1500
b
100
a 1000
a

500
0
Portabella Macrolepiota Champignon Champignon Boletus
(w) (c) 0
0 1000 2000 3000
Time (s)
5 c
Figure 1. Total phenolic content (expressed as caffeic acid (B)

mmol Fe2+/100 g FW
equivalents, CAE/ 100 g FW) of 80% methanolic extracts from 4
d
wild and commercial mushrooms. Values are mean ± SD from four
determinations. Different letters in the bars indicate statistically 3
significant differences (LSD test, P < 0.05).
2 b
a,b
Figura 1. Concentración fenoles totales (expresado como a
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equivalentes de ácido caféico, CAE/ 100 g peso fresco) del extracto 1

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

0
valores se reportan como media ± DS de cuatro repeticiones. Letras Portabella Macrolepiota Champignon Champignon Boletus
diferentes en las barras indican diferencia significativa (prueba DMS, (w) (c)
P < 0,05).

Figure 2. Antioxidant activity, estimated by the FRAP assay

(CAE)/ 100 g of fresh weight. Phenolic concentration (expressed as mmol Fe2+/ 100 g FW) of (a) FRAP reaction kinetics
of 80 % methanolic extracts from wild and commercial mushrooms,
ranged from 45.6 mg CAE/ 100 g FW for commercial measure at 595 nm and (b) Ferric reducing ability of methanolic
champignon to 308.3 mg CAE/ 100 g FW for wild extracts determined at 30 min. Values are mean ± SD from four
champignon. Figure 1 shows that both commercial species estimations. Different letters in the bars indicate statistically
presented statistically the same phenolic concentration, significant differences (LSD test, P < 0.05).
and slightly lower than that for Macrolepiota. Boletus Figura 2. Actividad antioxidante, determinada por el método FRAP
presented a total phenol concentration of 169.6 ± 26.7 mg (expresado como mmol Fe2+/ 100 g peso fresco) de (a) cinética de
CAE/100 g FW. The higher phenolic concentration reacción FRAP de los extractos metanol:agua (80:20) de los hongos
observed for wild champignon can be partially explained comerciales y silvestres, determinado a 595 nm y (b) actividad
antioxidante de los extractos determinado a los 30 min. Los valores
considering its low water content due to dehydration. Wild se reportan como media ± DS de cuatro repeticiones. Letras diferentes
mushrooms presented, in general, statistically higher en las barras indican diferencia significativa (prueba DMS, P < 0,05).
phenolic concentration than commercial ones. The total
phenolic concentration of the samples analyzed in the to Fe2+-TPTZ. In this way, a higher Fe3+-TPTZ reduction
present study (4.87 to 13.74 mg CAE/ g DW) were higher means a higher antioxidant activity.
than those reported by Mau et al. (2002), and Choi et al. The original FRAP methodology proposed by
(2006), but in the range of those reported by Lo and Cheung Benzie and Strain (1996) established a 4 min interval before
(2005), Cheung et al. (2003), Yang et al. (2002), and Ferreira the determination of the FRAP value. However, as shown
et al. (2007) for different commercial and wild mushrooms in Figure 2a, and in agreement with Pulido et al. (2000) and
found world widespread. Alvarez-Parrilla et al. (2005), the reduction of Fe3+ to Fe2+
The antioxidant activity of wild and commercial in the presence of the mushroom extract follows a slow
mushrooms has been determined by several methods, such kinetic mechanism, and even after 30 min the reaction was
as 2,2-diphenyl-1-pycrilhydracyl radical, DPPH (Mau et al., not totally completed. For this reason, FRAP values were
2001; Mau et al., 2002; Cheung et al., 2003; Lakshmi et al., determined at 30 min, as suggested in the literature (Pulido
2004; Ribeiro et al., 2006; Turkoglu et al., 2007), TEAC et al., 2000; Alvarez-Parrilla et al., 2005). When the FRAP
(Lakshmi et al., 2004), conjugated diene method (Mau et values determined at 4 and 30 min were compared, a 32-97
al., 2001; Mau et al., 2002), Ferricyanide reducing power % increment was observed. However, the increment in the
(Mau et al., 2001; Mau et al., 2002), and ferric reducing/ FRAP values at 60 min was less than 20 % higher compared
antioxidant power assay, FRAP (Lakshmi et al., 2004), to those observed at 30 min.
among others. Figure 2b shows the FRAP values of the 80 %
In the present work, antioxidant activity was methanolic mushroom extracts determined at 30 min and
measured by the FRAP method, which measures the expressed as mmol Fe2+/ 100 g FW. Figure 2b shows that
capacity of an antioxidant to reduce a Fe3+-TPTZ complex the antioxidant activity varied in a similar pattern than the

332
 SOMENTA ©2007 Alvarez-Parrilla et al.: Total phenols and antioxidant activity of …

5 found in mushrooms, in agreement with several authors

(Lo and Cheung, 2005; Choi et al., 2006; Ferreira et al.,
4
2007). However it is important to evaluate the type of
phenol present in mushroom and its individual contribution
Mmol Fe2+/100 g FW

to the total antioxidant capacity. In this regards, studies

3
are in progress evaluating other phenols and antioxidants
present in mushrooms.
2 In conclusion, the results reveal that wild
mushrooms could be an important source for low caloric,
1 low fat functional foods, with high level of polyphenols
and antioxidant activity, especially for the ethnic groups
0
(Tarahumaras tribes) living in the North of Mexico. From
0 50 100 150 200 250 300 350 the wild mushrooms studied, «Boletus» may be an
mg CAE / 100 g FW
interesting group due to their high nutritional value, total
phenol concentration and antioxidant activity, as well as
Figure 3. Linear correlation between total polyphenols (expressed
as caffeic acid equivalents, CAE/ 100 g FW) and antioxidant activity its high relative abundance in the region. As far as we
(expressed as mmol Fe2+/ 100 g FW) of 80% methanol extract from know, this is the first study of Mexican wild edible
wild and commercial mushrooms. Values are mean ± SD from four mushrooms were in vitro antioxidant activity analysis was
estimations. Correlation coefficient = 0.9721, significance level P evaluated and compared with commercial species.
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< 0.002.

Figura 3. Correlación linear entre los fenoles totales (expresado

como equivalentes de ácido caféico, CAE/ 100 g peso fresco) y ACKNOWLEDGEMENTS
actividad antioxidante (expresado como mmol Fe 2+/ 100 g peso
fresco) de de los extractos metanol:agua 80:20 de los hongos
comerciales y silvestres. Los valores se reportan como media ± DS Financial support from UACJ (internal projects) is
de cuatro repeticiones. Coeficiente de correlación = 0,9721, nivel gratefully acknowledged. The authors would like to express
de significancia P < 0,002. appreciation to Dr. Marcos Lizarraga for his helpful
assistance in collecting and identifying wild mushrooms
total phenolic concentration in the order: wild and to Héctor Osvaldo Sosa for technical assistance.
champignon> Boletus > Macrolepiota >Portabela H =
commercial champignon. FRAP values ranged from 0.94
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