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International Journal of Food Sciences and Nutrition

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Effect of different cooking methods on nutritionalvalue and antioxidant activity of cultivatedmushrooms

Irene Roncero-Ramos, Mónica Mendiola-Lanao, Margarita Pérez-Clavijo &Cristina Delgado-Andrade

To cite this article: Irene Roncero-Ramos, Mónica Mendiola-Lanao, Margarita Pérez-Clavijo& Cristina Delgado-Andrade (2017) Effect of different cooking methods on nutritional value andantioxidant activity of cultivated mushrooms, International Journal of Food Sciences and Nutrition,68:3, 287-297, DOI: 10.1080/09637486.2016.1244662

To link to this article: https://doi.org/10.1080/09637486.2016.1244662

Published online: 20 Oct 2016.

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FOOD COMPOSITION AND ANALYSIS

Effect of different cooking methods on nutritional value and antioxidantactivity of cultivated mushrooms

Irene Roncero-Ramosa, M�onica Mendiola-Lanaoa, Margarita P�erez-Clavijoa and Cristina Delgado-Andradeb

aMushroom Technological Research Center of La Rioja (CTICH), Autol (La Rioja), Spain; bDepartment of Physiology and Biochemistry ofAnimal Nutrition, Estaci�on Experimental del Zaid�ın (CSIC), Armilla (Granada), Spain

ABSTRACTInfluence of culinary treatments (boiling, microwaving, grilling, and deep frying) on proximatecomposition and antioxidant capacity of cultivated mushrooms (Agaricus bisporus, Lentinula edo-des, Pleurotus ostreatus, and Pleurotus eryngii) was studied. Proximate composition was affectedby the cooking method and the mushrooms species. Frying induced more severe losses in pro-tein, ash, and carbohydrates content but increased the fat and energy. Boiling improved the totalglucans content by enhancing the b-glucans fraction. A significant decrease was detected in theantioxidant activity especially after boiling and frying, while grilled and microwaved mushroomsreached higher values of antioxidant activity. Maillard reaction products could be partially respon-sible, as supported by the absorbance values measured at 420nm. Since cooking techniquesclearly influence the nutritional attributes of mushrooms, the proper selection of treatments is akey factor to prevent/reduce nutritional losses. Microwaving and grilling were established as thebest processes to maintain the nutritional profile of mushrooms.

ARTICLE HISTORYReceived 8 July 2016Revised 6 September 2016Accepted 1 October 2016Published online 20 October2016

KEYWORDSMushrooms; b-glucans;cooking methods;antioxidant activity;proximal composition;Maillard reaction

Introduction

Mushrooms have been part of the human diet forthousands of years. The consumption of edible mush-rooms has risen greatly in recent times, involving alarge number of species (Reis et al. 2012a). The mostcultivated mushroom worldwide is Agaricus bisporus,followed by Lentinula edodes and Pleurotus spp.Mushrooms are considered valuable health foods,since they have a significant amount of dietary fiberand are poor in calories and fat (Reis et al. 2012a).Moreover, they have a good protein content (20–30%of dry matter) which includes most of the essentialamino acids (Ghorai et al. 2009); also provide a nutri-tionally significant content of vitamins (B1, B2, B12,C, D, and E) and trace minerals such as zinc or selen-ium (Manzi et al. 2004; Mattila et al. 2001,Ca�glar{rmak 2007; Ca�glar{rmak 2009)

Mushrooms are also an important source of bio-logically active compounds with potential medicinalvalue. The medicinal use of mushrooms has a verylong tradition in the Asian culture, whereas in theWestern countries, the study of fungal bioactive com-pounds and their health effects has only recently

emerged (Cheung 2010). The medicinal mushroomproperties have been reported by the scientific com-munity including antitumor, immunomodulating,antioxidant, radical scavenging, antihypercholesterole-mia, antiviral, antibacterial, hepatoprotective, andantidiabetic effects (Wasser 2011). The mushroomsbioactive compounds responsible for these propertiesare: polysaccharides, dietary fiber, and antioxidants(vitamins C, B12 and D; folate; ergothioneine andpolyphenols). Currently, authors are focused onb-glucans, a cell-wall non-starch polysaccharide withrepeating units of glucose. These glucose units maybranched in several ways depending on the sourcefrom which it is extracted, those synthetized by fungiand yeast have these side chains structure: b-1,3-D-glucans and b-1,6-D-glucans (Rop et al. 2009).Numerous positive effects have been associated withfungal b-glucans, for instance, in the treatment ofcancer disease; in the metabolism of fats and sugarsby reducing cholesterol and glucose level in blood;improving resistance against allergies by increasingthe numbers of lymphocytes, among others (Wasser2011).

CONTACT Irene Roncero Ramos irene_rr20@hotmail.com Centro Tecnol�ogico de Investigaci�on del Champi~n�on de La Rioja, Carretera de Calahorrakm. 4, 26560 Autol, La Rioja, Spain� 2016 Informa UK Limited, trading as Taylor & Francis Group

INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION, 2017VOL. 68, NO. 3, 287–297http://dx.doi.org/10.1080/09637486.2016.1244662

Processing of food products such as boiling, micro-waving, pressure-cooking, grilling, baking, steaming,and frying induces significant changes in the textureand chemical composition. During boiling losses ofvitamins, antioxidant compounds or leaching of sol-uble substances in the water may significantly influ-ence the nutritional value of the final product (Faller& Fiahlo 2009). On one hand, thermal treatments canalso reduce the food quality; it is well-known thatmost of the bioactive compounds are relativelyunstable to heating (Choi et al. 2006). However, onthe other hand, different chemical reactions betweenthe food components take place and new substancescan be formed, for instance, Maillard reaction prod-ucts (Delgado-Andrade et al. 2007). The developmentof the Maillard reaction in food matrix is oftenresponsible for the appearance of attractive aromas,colors, and flavors, and hence improved food palat-ability. Moreover, Maillard reaction products are asso-ciated to some positive biological actions such as anincrease in antioxidant activity (Somoza 2005).

The most mushrooms are commonly cooked beforebeing consumed, but scarce information is availableabout the changes in nutritional quality after culinarytreatments. Lower level of nutraceuticals and antioxi-dant activity was reported by Jaworska et al. (2015) inblanched mushrooms (Agaricus bisporus and Pleurotusostreatus) compared with raw ones. Accordingly,Manzi et al. (2004) also described a decrease in anti-oxidant activities in cooked mushrooms. However, thepolyphenol concentration seems to increase by cook-ing treatments as described by Choi et al. (2006) forLentinula edodes heated at 121 �C for 30min. In thesame line, Sun et al. (2014) also reported that theretention of total phenolic compounds after microwav-ing treatment was better than in others cooking meth-ods. Thus, microwaving seems to be one of the bestcooking processes to preserve the antioxidant proper-ties of mushroom as demonstrated by Tan et al.(2015), who established that microwaved Pleurotuseryngii showed 17% higher Trolox equivalent antioxi-dant capacity (TEAC) value compared with theuncooked sample.

All these data suggest that increasing the knowledgeof the nutritional consequences of culinary treatmentsis a good strategy to preserve the nutritional quality ofmushroom. Thus, this assay aimed to evaluate theinfluence of different cooking methods on proximatecomposition, b-glucans content and antioxidant activ-ity of four cultivated mushrooms species. Unspecificparameters as CIE Lab color and absorbance measure-ments at 420 nm were used as a tool to better under-stand emerging changes.

Materials and methods

Mushrooms samples and cooking methods

Fresh fruiting bodies of four mushrooms: Agaricus bis-porus (common name: white button mushroom),Lentinula edodes (common name: shiitake) and twospecies of oyster mushrooms (Pleurotus spp.),Pleurotus ostreatus, and Pleurotus eryngii, commonlyknown as oyster mushroom and king oyster, respect-ively, were harvested from the cultivation rooms atCTICH facilities. Fresh mushrooms fruiting werecleaned from soil and substrate. Mushrooms werethen cut along their vertical axes into slices 4–5mmthick and submitted to one of these methods.

The experiments were carried out using 15 kg ofeach mushroom; this amount was randomly dividedinto five groups (3 kg each). One of them remainedraw and the rest were cooking in four different meth-ods (boiling, microwaving, griddling, and frying).Culinary conditions were as follows:

1. Boiling: Mushroom slices (300 g/batch) were boil-ing on a pot containing 3 L of bottled water for10min.

2. Deep frying: Mushroom slices (150 g/batch) werefrying in a pan with 500mL olive oil (160 �C) for3min.

3. Microwaving: Mushroom slices (100 g/batch) wereplaced in a dish and cooked in a domestic micro-wave at 1000 W for 1.5min.

4. Grilling: Mushroom slices (180 g/batch) werecooked in an electric grill at 100 �C for 6min(3min on each side).

All these processes were repeated until the 3 kg ofslices of each mushroom were cooked. After cooking,all samples were placed on a filter paper to drainwater or oil excess. Raw and processed mushroomswere then freeze-dried, powdered, and homogenizedin a commercial grinder to use in subsequentexperiments.

Chemical composition

The chemical composition of the edible mushrooms,including moisture, ash, crude fat, and protein, weredetermined in triplicate according to AOAC methods(1995). The protein content (N� 4.38) of the sampleswas estimated by Kjeldahl method using Kjeltec diges-tion apparatus (2100 Digestion Unit, Tecator,Sweden). The conversion factor nitrogen-to-proteinused was 4.38, since mushrooms proteins are part ofchitin which is not digestible so that digestible

288 I. RONCERO-RAMOS ET AL.

proteins were calculated using the adjustment factor4.38 (Shashirekha et al. 2002). The crude fat wasdetermined by extracting a known weight of powderedsample with petroleum ether using a Soxhlet appar-atus. The ash content was measured by incineration at500 �C. Total carbohydrates were calculated by differ-ence. Energy was estimated according to the followingequation: energy (kcal)¼ 4� (g proteinþ gcarbohydrate)þ 9� (g fat).

The content of glucans was determined spectro-photometrically using a Mushroom and Yeastb-Glucan Assay kit (Megazyme, Bray, Ireland) accord-ing to the protocol of the manufacturer.

Antioxidant assays

Reagents

All chemicals were of analytical reagent grade orhigher purity. Bidistilled deionized water was obtainedfrom a Milli-Q purification system (Millipore,Bedford, MA). Methanol, Folin–Ciocalteau reagent, 6-hydroxy-2,5,7,8-tetramethyl-chroman-2-carboxylic acid(Trolox), 2,2-azinobis-(3-ethylbensothiazoline)-6-sul-fonic acid (ABTS), and 2,2-diphenyl-1-picrylhydrazyl(DPPH) were provided by Sigma (St. Louis, MO).2,4,6-Tri(2-pyridyl)-s-triazine (TPTZ) for the ferricreducing power (FRAP) method was obtained fromFluka Chemicals (Fluka Chemicals, Madrid, Spain).Sodium bicarbonate, sodium carbonate and hydro-chloric acid (37%) were provided by Merck(Darmstadt, Germany).

Chemical extraction

The chemical extraction of antioxidants was per-formed following the procedure described by P�erez-Jim�enez and Saura-Calixto (2005). Briefly, 0.250 g ofsample was placed in a tube and 2.5mL of acidicmethanol/water (50:50 v/v, pH 2) were added. Thetube was thoroughly shaken at room temperature for1 h and centrifuged at 2500 g for 10min, and thesupernatant was recovered. 2.5mL of acetone/water(70:30, v/v) were added to the residue, and the shak-ing and centrifugation steps were repeated. The meth-anolic and aqueous-acetone extracts were thencombined and the volume made up to 5mL.

Antioxidant activity

Three procedures were applied to test the antioxidantactivity of the samples: the ABTS and DPPH assays, tomeasure the free radical scavenger ability, and the FRAPmethod, to study the ferric reducing antioxidant power.

Aqueous solutions of Trolox were used for calibration(0.01–0.1mg/mL). Results were expressed as lmolequivalents of Trolox per 100mg of raw or cookedmushrooms (lg TE/100mg).

ABTS method The ABTS assay was conducted asdescribed by Rufi�an-Henares and Delgado-Andrade(2009) with slight modifications. ABTSþ. was prepared12–16 h before use by dissolving ABTS 7mM with2.45mM potassium persulfate, and then diluted inethanol:water 50:50 to an absorbance of 0.7 ± 0.02.20 lL of the samples and 280lL of ABTS solutionwere incubated for 20min in the dark and the absorb-ance was read at 730 nm in a Victor X3 multilabelplate reader (Perkin-Elmer, Norwalk, CT).

DPPH method The antiradical activity was estimatedfollowing the procedure reported by Rufi�an-Henaresand Morales (2007). Briefly, 50lL of the sample weremixed with 250lL of DPPH solution (74mg/L inmethanol freshly prepared). After incubation for60min, the absorbance was measured at 520 nm in thesame plate reader, maintaining the temperature in themeasurement chamber at 30 �C.

FRAP method The ferric reducing ability of the extractof each sample was estimated following the proceduredescribed by Rufi�an-Henares and Delgado-Andrade(2009). About 280lL of FRAP reagent freshly pre-pared and warmed at 37 �C was mixed with 20 lL ofthe sample. The FRAP reagent contained 2.5mL of a10mM TPTZ solution in 40mM HCl plus 2.5mL of20mM FeCl3 and 25mL of 0.3 M acetate buffer, pH3.6. The samples were incubated at 37 �C for 30minin the dark and the absorbance was read at 595 nm inthe plate reader indicated.

Total polyphenols

Total polyphenol content was determined followingthe Folin–Ciocalteau colorimetric method as describedby Saura-Calixto and Go~ni (2006) with modifications.About 10 lL of sample and 10 lL of Folin–Ciocalteaureagent were mixed in 96-well multi-well plates andlet stand for 3min. Sodium carbonate solution(75 g/L) of 200lL were added, the volume was madeup to 250 lL with Milli-Q water, mixed and allowedto stand in the dark for 60min. The absorbance wasmeasured at 750 nm using a Victor X3 multilabel platereader (Waltham, MA) against a standard curve ofgallic acid (0–200mg/L). The total polyphenolscontent was expressed as lg gallic acid equivalent

INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 289

per 100mg of raw or cooked mushroom (lg GAE/100mg).

Measurement of color

The color of different samples was determined using aChroma Meter CR-400 optical sensor (Konica MinoltaSensing, Inc., Osaka, Japan) according to the CIE Labscale (CIE Colorimetric Committee 1974). The systemprovides the values of three color components: L�(black–white component, luminosity) and the chroma-ticity coordinates, a� (þred to� green component)and b� (þyellow to� blue component). The sampleswere placed in a 34mm optical glass cell and illumi-nated with D65-artificial daylight (10� standard angle)in accordance with the instructions of the manufac-turer. The E index is calculated from the equation:E¼ (L�2þ a�2þ b�2)1/2 and the yellowing index (YI)was estimated from the equation YI¼ 142.86 � b�/L�.Each color value reported was the mean of threedeterminations at 22–24 �C.

Measurement of absorbance at 420 nm

The browning associated with Maillard reaction devel-opment was determined at 420 nm. The progress ofthe reaction involves the production of final and highmolecular weight compounds, termed melanoidins,with chromophore groups with a characteristicabsorbance maximum at 420 nm (Morales &Jim�enez-P�erez 2004). Briefly, the measurement of

browning was performed using the extracts preparedfor antioxidant assays, they were measured at 420 nmin an UV/Vis spectrophotometer (UV-1700Pharmaspec, Shimazu Corporation, Japan). Analyseswere performed in triplicate.

Statistical analysis

Statistical significance of the data was tested by one-way analysis of the variance (ANOVA), followed bythe Duncan test to compare the means that showedsignificant variation (p< .05). Analyses were per-formed using Statgraphics Centurion XVI software(StatPoint Technologies, Inc., Warrenton, VA).Relationship between the different variables was car-ried out by computing the relevant correlation coeffi-cient (Pearson’s linear correlation) at the p< .05confidence level.

Results and discussion

Proximate composition

Data from the proximate composition of raw andcooked mushrooms are presented in Table 1. On anaverage, 60 g of A. bisporus was obtained from 100 gof fresh mushrooms, regardless the culinary treatment.However, in Pleurotus mushrooms, after boiling andmicrowaving methods, the culinary yield was greater(80%) comparing with the treatments that involvedhigher temperatures, grilling, and deep frying.Regarding L. edodes, in general, the culinary yields

Table 1. Cooking yield (%) and proximate composition (g/100 g dry weight) of raw and cooked mushroomsa.%

Samples Cooking methods Cooking yield % Moisture Ash Proteinb Fat Carbohydratesc Energyc

Agaricus bisporus Raw 89.71 ± 0.25a 9.40 ± 0.06a 24.64 ± 0.17a 2.34 ± 0.03a 63.66 ± 0.24a 374.2 ± 0.5a

Boiling 57.3 85.87 ± 0.24b 5.46 ± 0.09b 26.56 ± 0.37b 1.19 ± 0.02b 66.55 ± 0.37b 384.4 ± 0.2b

Microwaving 60.9 82.14 ± 0.72c 8.21 ± 0.04c 23.87 ± 0.14c 1.42 ± 0.01b 66.62 ± 0.09b 374.4 ± 0.2a

Grilling 60.6 79.62 ± 1.09d 8.81 ± 0.10d 23.67 ± 0.18c 3.27 ± 0.08c 64.06 ± 0.04a 381.0 ± 1.0c

Deep frying 61.5 56.24 ± 1.01e 5.01 ± 0.05e 15.27 ± 0.14d 45.08 ± 0.19d 34.81 ± 0.10c 605.3 ± 0.6d

Lentinula edodes Raw 87.83 ± 1.08a 7.36 ± 0.01a 16.82 ± 0.36a 2.06 ± 0.01ab 73.43 ± 0.21a 380.9 ± 0.1a

Boiling 109.1 89.14 ± 0.24a 4.49 ± 0.10b 16.88 ± 0.08a 1.57 ± 0.03a 77.02 ± 0.14b 389.5 ± 0.3c

Microwaving 84.8 81.11 ± 0.75b 6.73 ± 0.07c 16.75 ± 0.10a 1.98 ± 0.03ab 74.40 ± 0.14a 382.9 ± 0.2ab

Grilling 73.9 78.31 ± 0.54c 6.89 ± 0.07c 16.50 ± 0.04a 3.00 ± 0.04b 73.62 ± 0.01a 387.5 ± 0.7bc

Deep frying 86.3 39.44 ± 0.26d 2.66 ± 0.02d 5.90 ± 0.08b 62.27 ± 0.75c 29.20 ± 0.88c 700.6 ± 3.7d

Pleurotus ostreatus Raw 89.41 ± 0.27a 6.73 ± 0.05a 12.55 ± 0.24a 2.46 ± 0.01a 78.35 ± 0.36a 382.5 ± 0.1a

Boiling 88.0 88.05 ± 0.47ab 3.50 ± 0.09b 12.85 ± 0.11a 2.14 ± 0.08ab 81.33 ± 0.01b 396.3 ± 0.3b

Microwaving 80.8 83.87 ± 1.12bc 6.02 ± 0.15c 12.82 ± 0.08a 1.52 ± 0.01b 79.70 ± 0.24c 383.4 ± 1.1a

Grilling 71.2 81.81 ± 1.05c 6.05 ± 0.09c 12.69 ± 0.06a 2.03 ± 0.02ab 79.19 ± 0.03ac 385.6 ± 0.1a

Deep frying 61.7 54.01 ± 2.21d 3.14 ± 0.01d 5.96 ± 0.10b 50.38 ± 0.48c 40.47 ± 0.33d 639.4 ± 2.4c

Pleurotus eryngii Raw 88.16 ± 0.17a 5.39 ± 0.04a 12.30 ± 0.04a 1.60 ± 0.02ab 80.74 ± 0.02a 386.5 ± 0.2a

Boiling 84.8 88.09 ± 0.18a 3.22 ± 0.04b 13.01 ± 0.05b 1.67 ± 0.01a 82.15 ± 0.06b 395.4 ± 0.3b

Microwaving 81.0 80.58 ± 0.54b 5.08 ± 0.05c 12.05 ± 0.31a 1.57 ± 0.01b 81.03 ± 0.06a 387.6 ± 0.2c

Grilling 67.7 77.80 ± 0.56c 5.24 ± 0.02d 13.97 ± 0.04c 2.02 ± 0.05c 78.79 ± 0.12c 389.2 ± 0.2d

Deep frying 59.6 45.95 ± 1.40d 2.93 ± 0.04e 7.38 ± 0.21d 51.03 ± 0.02d 38.50 ± 0.16d 643.5 ± 0.4e

aValues are means ± SE, n¼ 3. Different letters within a column indicate significant differences between raw and cooked samples of each mushroom(p< .05).bN� 4.38.cCalculated by difference.

290 I. RONCERO-RAMOS ET AL.

were higher than in the others mushrooms assayed,especially after boiling where the value exceededthe 100%. Probably, because of its own structure, L.edodes could absorb more water during the boilingprocess than the others; in fact, this mushroom pre-sented the highest values of moisture and less ash con-tent. Similar values to the average yield data of thisassay were found in the study of Manzi et al. (2004)after cooking mushrooms for 10min in the grill.

The moisture content of cooked samples was sig-nificantly lower than the uncooked ones in all themushrooms species (Table 1). The values of moisturein frying samples were found to be the lowest ones,with a reduction of up to 50% in L. edodes and P.eryngii. A decrease in moisture content after cookingof mushroom has been previously reported (Jaworskaet al. 2015). Similar results were observed in theRam�ırez-Anaya et al. (2015) assay comparing raw andcooked vegetables: a strong reduction in moisture wasdetected in fried vegetables, while in samples cookedby other method as boiling or saut�eed, only a slightdecrease was noted. In the same line, a reduction inash content was shown in all cooked samples com-pared with the raw ones in the present assay. In thiscase, boiled and fried mushrooms exhibited the lowestvalues, probably due to the leaching of soluble sub-stances in the water or in the oil. Comparing the typeof mushroom, A. bisporus had the major ash contentvalues follows by L. edodes, P. ostreatus, and P. eryngii.The ash values of the four uncooked mushroom are inthe same range that those reported by Crisan andSands (1978).

Regarding the protein content, on one hand, friedmushrooms shown a significant reduction comparedwith the raw and cooked samples. This decrease couldbe explained by the high temperatures during deepfrying since the oil can reach up to 175 �C. It is wellknown that heat treatment can reduce the amount ofprotein and destroy some amino acids, changing thequality of protein composition in food (Henry 1998).On the other hand, the frying process implies thepenetration of fat in the food matrix and exerts a"dilution effect" in the rest of the nutrients present inthe food. Mushrooms processed by other cookingmethods had similar protein content to uncookedones. Once again, A. bisporus was the mushroom withmajor values compared with others species, even two-fold the protein content of Pleurotus spp.

The fat content significantly increased in friedmushrooms in the four species compared with raw,boiled, microwaved, and grilled samples which hadvalues of 1–3%. Fried mushrooms contained between45 and 60% of fat depending on the specie, this

increase during the frying process is due to the oilpenetration into the mushroom after water is partiallylost by evaporation (Saguy & Dana 2003), greatly con-tributing to the composition of the final product. As aresult of this fat penetration during frying, the caloricvalue of fried mushrooms was two-fold higher thanthat of raw and cooked mushrooms. The data are inagreement with the study published by Pogo�n et al.(2013) who observed a pronounced increase of fat andenergy values when a mushroom called Lactarius deli-cioius was fried.

Carbohydrates, calculated by difference, followedthe same trend as protein content; similar values werefound between raw and cooked samples, except infried ones which presented an important reduction ofcarbohydrates content. As it mentioned above, thehigh amount of oil absorbed by these samples led tochanges in their nutritional composition. In the rest ofcooking methods, some significant increases have beendetected in carbohydrates, protein, and energy valueswith respect to raw ones, this fact could be due to aloss of moisture during the mushrooms processingand a subsequent concentration of nutrients (Manziet al. 2001, 2004). Dikeman et al. (2005) also reportedcooking losses and, therefore, a concentration of drymatter constituents in Agaricus bisporus and Lentinulaedodes, especially for carbohydrates (starch and totaldietary fiber).

The composition of the cooked mushrooms wascomparable with the data available in the literature(Barros et al. 2007; Pogo�n et al. 2013) and the valuesof uncooked samples are in agreement with those pre-viously described for each species of mushroomstudied (Diez & Alvarez 2001; Manzi et al. 2004).

Glucans content

Results of total glucans, a-glucans, and b-glucans aredepicted in Table 2. Glucan concentration varieddepending on the cooking method to which mush-rooms have been submitted. In A. bisporus and L. edo-des, boiling treatment significantly increased the totalglucans content, followed by microwaving and grillingmethod. Mushrooms processed by these three meth-ods presented similar or even more total glucans con-tent than the raw ones. The same trend can beobserved in a-glucans content; however, in this case,boiled samples presented lower amount of these com-pounds than microwaved and grilled ones. Therefore,the percentage of b-glucans, calculated by difference,only increased significantly after boiling process.Results from L. edodes showed that despite some sig-nificant differences in a-glucans between raw and

INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 291

cooked samples were observed, the boiled mushroomshad the highest values of b-glucans compared withraw ones but, in this case, a slight increase was alsodetected in grilled mushrooms. b-Glucans are consid-ered as bioactive compounds with medicinal proper-ties, so it is important to know which culinary methodbetter preserves or even increases the b-glucans con-tent. The increase of these compounds in boiledmushrooms could be due to the leaching of solublesubstances during boiling, which could result in a con-centration effect of the fraction of insoluble carbohy-drates (Pogo�n et al. 2013).

In Pleurotus ostreatus, despite some differencesbetween cooked and raw samples observed in totaland a-glucans, the b-glucan content were unchangedin all the samples except in the fried one. The sameoccurred in P. eryngii although, in this case, theamount of b-glucan in grilled mushroom alsodecreased respect to the uncooked one.

Mushrooms from frying treatment had the lowestvalues of total and a-glucans, and subsequently ofb-glucans in the four mushrooms species. Althoughfew studies have described the effect of processing onmushrooms-derived biologically active polysacchar-ides, it is logical to think that the high temperaturescould affect the content and concentration of bio-logical compounds. Radzki et al. (2016) investigatedthe impact of some processing methods in P. ostrea-tus, confirming that the content and the activity ofpolysaccharides decreased due to the culinary proc-essing, and that temperature and heating time arekey factors.

Taking into account the values of b-glucans withinthe different species of mushrooms, P. eryngi hadhigher content of b-glucans than the other three spe-cies. It is well known that Pleuran, a specific b-glucanisolated from P. ostreatus, and Lentinan, from L. edo-des, are currently the most frequently glucans used fortheir pharmacological properties. However, there arescant studies about the bioactive properties of P.eryngii and the most of the researchers have publishedlower values of b-glucans for this mushroom (Manziet al. 2001, 2004) than those reported in the presentstudy. Only the paper published by Synytsya et al.(2008) is in agreement with our data for P. eryngiiand P. ostreatus. In view of these results, P. eryngiiseems to be a promising candidate as medicinal mush-room and further studies are needed to explore itspotential.

Antioxidant activity and polyphenols content

Total polyphenols content and antioxidant activity ofraw and cooked mushrooms are shown in Table 3.Total polyphenol content was expressed as lg GAE/100mg in dry weight and the antioxidant activity aslmol TE/100mg in dry weight.

The amount of polyphenols present in the mush-rooms is not as important as those found in fruits orvegetables (Kettawan et al. 2011). Therefore, our pur-pose was not to identify the phenolic compoundsfound in mushrooms by HPLC but we wanted toknow the total polyphenol quantity to correlate them

Table 2 Contents of total glucans, a-glucans and b-glucans (g/100 g dry weight) in raw andcooked mushroomsa.

%

Samples Cooking methods Total glucans a-Glucans b-Glucans

Agaricus bisporus Raw 15.97 ± 0.69a 3.03 ± 0.11a 12.94 ± 0.81a

Boiling 20.71 ± 0.44b 3.71 ± 0.16b 17.00 ± 0.33b

Microwaving 18.51 ± 0.31c 4.17 ± 0.13c 13.44 ± 0.42a

Grilling 17.58 ± 0.39c 4.14 ± 0.03c 14.35 ± 0.39a

Deep frying 12.91 ± 0.38d 2.35 ± 0.11d 10.56 ± 0.44c

Lentinula edodes Raw 34.81 ± 1.23a 2.26 ± 0.01a 32.55 ± 1.13a

Boiling 43.48 ± 0.61b 3.39 ± 0.04b 40.09 ± 0.63b

Microwaving 36.94 ± 0.30c 3.09 ± 0.06c 33.85 ± 0.29ac

Grilling 36.67 ± 0.24ac 2.13 ± 0.03d 34.55 ± 0.23c

Deep frying 14.66 ± 0.11d 1.04 ± 0.04e 13.62 ± 0.08d

Pleurotus ostreatus Raw 49.15 ± 0.52ab 8.29 ± 0.06a 40.86 ± 0.57a

Boiling 51.23 ± 0.29a 7.90 ± 0.09b 43.33 ± 0.32a

Microwaving 49.48 ± 0.78ab 7.88 ± 0.10b 41.60 ± 0.86a

Grilling 48.36 ± 0.91b 5.18 ± 0.05c 43.18 ± 0.95a

Deep frying 26.89 ± 1.29c 2.80 ± 0.12d 24.09 ± 1.37b

Pleurotus eryngii Raw 54.25 ± 0.43a 9.79 ± 0.14a 44.47 ± 0.30a

Boiling 56.06 ± 0.88a 12.60 ± 0.55b 43.46 ± 0.77ab

Microwaving 55.32 ± 0.30a 12.40 ± 0.18b 42.92 ± 0.22ab

Grilling 48.60 ± 0.65b 6.44 ± 0.04c 42.16 ± 0.62b

Deep frying 25.04 ± 0.30c 2.01 ± 0.07d 23.03 ± 0.27c

aValues are means ± SE, n¼ 3. Different letters within a column indicate significant differences between raw andcooked samples of each mushroom (p< .05).

292 I. RONCERO-RAMOS ET AL.

with the antioxidant activity measured as DPPH,ABTS, and FRAP.

After submitting L. edodes to different cookingtreatments, an appreciable decrease in polyphenol con-tent and antioxidant activity measured by ABTS,DPPH, and FRAP methods was observed in boiledand fried samples with respect to the raw ones andthe other cooking procedures. In contrast, in grilledand microwaved L. edodes, the polyphenol contentand the antioxidant activity increased significantlycompared with the uncooked ones. Previous studiesalso reported an increase of the antioxidant activityautoclaved L. edodes at 121 �C during 30min (Choiet al. 2006). The authors explained this fact with tworeasons: (I) the heat treatment might disrupt the cellwall and liberate antioxidant compounds from insol-uble portion of mushroom increasing the pool of bio-accessible antioxidant compounds, it has beendescribed that many antioxidant compounds in plantmaterials are mainly present as a covalently boundform with insoluble polymers (Peleg et al. 1991); and(II) the formation of novel compounds having antioxi-dant activity during heat treatment or thermal proc-essing, such as Maillard reaction products.

Results from P. ostreatus and P. eryngii shown asimilar trend in polyphenols content and antioxidantactivity as L. edodes. A decrease in antioxidant cap-acity in boiled and fried mushrooms was also detected,although in this case, the decline in fried samples wasnot as pronounced as the boiled ones. Previously, sev-eral authors have demonstrated that the boiling pro-cess significantly decreased antioxidant activity andpolyphenol content in different mushrooms varieties,

P. eryngii, L. edodes, and P. ostreatus among them(Kettawan et al. 2011; Lam & Okello 2015)

When P. ostreatus and P. eryngii were cooked bymicrowave or grill, the content of polyphenol andantioxidant activity increased significantly (Table 3).As it stated above, the increase could be explained bythe release of antioxidant compounds which were pre-viously linked to other molecules increasing the poly-phenol content and then the antioxidant activity and/or for the development of the Maillard reaction duringthermal treatment, leading to the formation of highmolecular weight compounds with a strong antioxi-dant capacity. Grilling is the best treatment to cook P.eryngii, since this treatment induced the major valuesfor antioxidant activity and polyphenols content,which is consistent with data published by Manziet al. (2004) who reported an increase in total phenolswhen P. eryngii was grilled for 10min. In the case ofP. ostreatus, according with the literature (Sun et al.2014) and with our own data, the microwave treat-ment was better in the retention of total phenols.Regarding the antioxidant capacity, values from DPPHand FRAP methods also increased in the microwavesamples but not in ABTS method where the antioxi-dant activity decreased respect to the raw one. Itshould be taken into account that each antioxidanttest is based on different principles and mechanisms(Barros et al. 2007), so it is possible that a food sam-ple shows high antioxidant activity with a single meas-uring method but not with another antioxidant test(Kettawan et al. 2011). This is the reason for what dif-ferent antioxidant assays, at least three methods,should be used to measure antioxidant activity.

Table 3. Antioxidant activities (lmol TE/100mg) and total polyphenols content (lg GAE/100mg) in raw and cookedmushroomsa.

Total polyphenols ABTS DPPH FRAPSamples Cooking methods lg GAE/100mg lmol TE/100mg lmol TE/100mg lmol TE/100mg

Agaricus bisporus Raw 181.99 ± 2.29a 2.333 ± 0.018a 0.752 ± 0.005a 2.358 ± 0.030a

Boiling 96.31 ± 1.21b 1.120 ± 0.025b 1.268 ± 0.015b 1.243 ± 0.008b

Microwaving 170.79 ± 1.97c 1.388 ± 0.033c 1.880 ± 0.020c 1.927 ± 0.017c

Grilling 166.87 ± 2.68c 1.581 ± 0.021d 1.808 ± 0.039d 2.198 ± 0.032d

Deep frying 130.87 ± 2.35d 1.372 ± 0.012c 1.426 ± 0.018e 1.811 ± 0.013e

Lentinula edodes Raw 104.35 ± 1.13a 0.413 ± 0.007a 1.012 ± 0.024a 1.376 ± 0.017a

Boiling 54.64 ± 0.66b 0.383 ± 0.004b 0.350 ± 0.006b 0.439 ± 0.006b

Microwaving 147.03 ± 1.91c 0.405 ± 0.003a 2.310 ± 0.015c 2.100 ± 0.014c

Grilling 151.67 ± 1.62d 0.480 ± 0.004c 2.221 ± 0.027d 1.985 ± 0.014d

Deep frying 44.01 ± 0.49e 0.329 ± 0.004d 0.334 ± 0.009b 0.393 ± 0.006e

Pleurotus ostreatus Raw 82.30 ± 1.23a 0.770 ± 0.013a 0.467 ± 0.010a 0.480 ± 0.005a

Boiling 30.08 ± 0.31b 0.100 ± 0.006b 0.150 ± 0.014b 0.163 ± 0.002b

Microwaving 91.21 ± 1.23c 0.456 ± 0.004c 0.517 ± 0.007c 0.519 ± 0.004c

Grilling 86.75 ± 1.62d 0.432 ± 0.007d 0.463 ± 0.006a 0.588 ± 0.007d

Deep frying 47.86 ± 0.80e 0.431 ± 0.005d 0.308 ± 0.005d 0.524 ± 0.007c

Pleurotus eryngii Raw 76.55 ± 0.89a 0.396 ± 0.007a 0.412 ± 0.003a 0.539 ± 0.006a

Boiling 40.67 ± 0.43b 0.172 ± 0.005b 0.259 ± 0.004b 0.318 ± 0.005b

Microwaving 82.79 ± 1.00c 0.196 ± 0.009c 0.427 ± 0.004a 0.524 ± 0.005a

Grilling 96.58 ± 1.54d 0.462 ± 0.009d 0.589 ± 0.005c 0.604 ± 0.007c

Deep frying 70.68 ± 0.79e 0.455 ± 0.005d 0.382 ± 0.007d 0.500 ± 0.004d

aDifferent letters within a column indicate significant differences between raw and cooked samples of each mushroom (p< .05).

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Interestingly, results from Agaricus bisporus showna different tendency than the rest of the speciesstudied. A decrease in total polyphenols and in ABTSand FRAP procedures was detected in all cooked sam-ples with respect to the uncooked one, more pro-nounced in boiled and fried mushroom. However, theDPPH radical scavenging ability increased in allthe culinary methods compared with the raw one. Thelack of concordance between the results from differentantioxidant techniques again underlines the import-ance of applying several antioxidant tests for a betterconsideration of the antioxidant response of a foodmatrix.

As mentioned, when A. bisporus is cooked by dif-ferent methods, the antioxidant activity decreased,contrary to that occurred in the other assayed mush-rooms. Probably, this fact could be due to the particu-lar structure and shape of each mushroom variety,which could affect the cooking process as well as theyielding extraction of antioxidants during the chemicalextraction, thus leading to different release of finalantioxidant material from the mushroom matrix(Kettawan et al. 2011). Thermal treatment influencesthe tissue of the mushrooms, the membranes denatur-ize, and their permeability increases, which leads to aloss of water and softening of the cells and causes achange in their structure (Pogo�n et al. 2013). It can behypothesized that A. bisporus could be more affectedby high temperatures than others species.

Comparing the data of polyphenols and antioxidantactivity between the different species, A. bisporus

showed the highest values of both parameters. Severalauthors have reported higher antioxidant activities inAgaricus bisporus compared with others mushrooms.Reis et al. (2012b) analyzed the antioxidant propertiesof the most cultivated worldwide species and con-cluded that A. bisporus had the highest antioxidantactivity compared with the others mushrooms studied.Dubost et al. (2007) also demonstrated that A. bispo-rus had significantly higher antioxidant potential withrespect to Lentinula edodes, Pleurotus ostreatus, andPleurotus eryngii.

Strong positive correlations were observed betweenpolyphenol content and antioxidant activity measuredby the ABTS (r¼ 0.7423, p¼ .0000), DPPH(r¼ 0.7622, p¼ .0000), and FRAP (r¼ 0.9346,p¼ .0000) methods, indicating the important contribu-tion of polyphenols to the antioxidant profile of thesemushrooms.

Unspecific indicators of Maillard reactiondevelopment in cooked mushrooms

Color analysis

The color of foods is the result of colored naturalproducts associated with the raw material and/or thecolored compounds generated as a result of processing(Giangiaconmo & Messina 1988). The L� parametermeasures the luminosity, reflecting the black–whitecomponent, so that a decrease on L� values indicatesdarkening. As can be observed in Table 4, the L� datain the present assay decreased in all cooked samples

Table 4. Unspecific indicators of Maillard reaction development in cooked mushrooms. Colorimetric parametersa.CIE Lab color

Samples Cooking methods L* a� b� YI indexb E indexc

Agaricus bisporus Raw 80.01 ± 0.61a 0.31 ± 0.09a 13.11 ± 0.11a 23.40 ± 0.37a 81.07 ± 0.58a

Boiling 76.86 ± 0.02b �0.33 ± 0.04b 11.87 ± 0.06b 22.06 ± 0.11b 77.77 ± 0.02b

Microwaving 73.47 ± 0.17c 1.03 ± 0.06c 11.23 ± 0.07c 21.84 ± 0.19b 74.33 ± 0.15c

Grilling 74.51 ± 0.37c 0.69 ± 0.01d 11.93 ± 0.13b 22.86 ± 0.13a 75.46 ± 0.39c

Deep frying 61.38 ± 0.37d 0.86 ± 0.04cd 17.65 ± 0.14d 41.08 ± 0.08c 63.87 ± 0.39d

Lentinula edodes Raw 73.92 ± 0.37a 1.80 ± 0.02a 10.14 ± 0.01a 19.59 ± 0.11a 74.63 ± 0.36a

Boiling 65.07 ± 0.01b 1.99 ± 0.01b 8.26 ± 0.12b 18.14 ± 0.26b 65.62 ± 0.02b

Microwaving 67.70 ± 0.06c 1.93 ± 0.03b 9.32 ± 0.10c 19.67 ± 0.23a 68.37 ± 0.05c

Grilling 67.01 ± 0.10d 1.99 ± 0.01b 10.12 ± 0.07a 21.58 ± 0.12c 67.80 ± 0.11c

Deep frying 35.24 ± 0.09e 2.54 ± 0.08c 7.23 ± 0.10d 29.32 ± 0.48d 36.06 ± 0.06d

Pleurotus ostreatus Raw 81.66 ± 0.66a �1.47 ± 0.24a 12.17 ± 0.34a 21.29 ± 0.76a 82.57 ± 0.59a

Boiling 71.68 ± 0.19b 0.84 ± 0.01b 8.16 ± 0.13b 16.27 ± 0.31b 72.15 ± 0.17b

Microwaving 72.84 ± 0.25b �1.34 ± 0.02a 13.31 ± 0.01c 26.11 ± 0.07c 74.05 ± 0.24c

Grilling 71.43 ± 0.30b �0.94 ± 0.03c 14.03 ± 0.14d 28.05 ± 0.15d 72.80 ± 0.32bc

Deep frying 43.42 ± 0.35c 2.23 ± 0.01d 11.09 ± 0.15e 36.49 ± 0.20e 44.87 ± 0.37d

Pleurotus eryngii Raw 82.26 ± 0.09a �1.00 ± 0.06a 11.67 ± 0.06a 19.56 ± 0.12a 86.06 ± 0.08a

Boiling 80.77 ± 0.01b 0.58 ± 0.01b 7.95 ± 0.08b 14.05 ± 0.14b 81.16 ± 0.01b

Microwaving 80.68 ± 0.07b �0.14 ± 0.05c 10.41 ± 0.25c 18.43 ± 0.43c 81.35 ± 0.10b

Grilling 79.59 ± 0.19c 0.05 ± 0.02d 11.60 ± 0.01a 20.82 ± 0.05d 70.43 ± 0.18c

Deep frying 51.76 ± 0.31d 2.91 ± 0.04e 13.94 ± 0.16d 38.47 ± 0.21e 56.83 ± 0.34d

aValues are means ± SE, n¼ 3. Different letters within a column indicate significant differences between raw and cooked samples of each mushroom(p< .05).bYI¼ 142.86 � b�/L�.cE¼ (L�2þ a�2þ b�2)1/2.

294 I. RONCERO-RAMOS ET AL.

respect to raw ones, the most pronounced reductionwas found in fried mushrooms. This could be relatedwith the heating load applied in each culinary process,higher temperatures could reach the activation energyof the Maillard reaction and more colored compoundscan be formed (Jim�enez-Zamora et al. 2016).

Redness (a�) is a parameter that describes the colorof samples in the red-green axis. All cooked samplesshow an increase in this parameter compared with theuncooked ones, except in boiled A. bisporus in whichthe value tended to the green color. Mushrooms sub-mitted to deep frying had the major values in a� par-ameter probably due to the reddish compoundsdeveloped during the thermal process.

Yellowness (b�) is a parameter that measures colorchanges in the yellow-blue range, becoming moreyellowish as the values increase. Depending on themushroom species the b� value had shown a differenttrend in this assay. After boiling, b� values decreasedin all the mushrooms compared with the other treat-ments. Deep frying method produced the highest b�values in A. bisporus and P. eryngii and the lowestones in L. edodes. In the case of P. ostreatus, the majorvalues were achieved after grilling process.

Yellowing index (YI) is a color measurement relatedto browning intensity, calculated as follows: YI¼142.86 � b�/L�. This parameter is used for the firsttime to evaluate milk color changes after 60min ofheat treatment between 90 and 130 �C (Pagliarini et al.1990) and then many authors have used it to evaluatecolor associated to Maillard reaction development. TheYI index in the present assay varied depend on thecooking treatment: boiled mushrooms show the lowestYI values; microwaved samples presented practicallythe same YI levels as uncooked samples; grilled mush-rooms show a slight significant increased comparedwith raw ones, and frying samples had the major YIvalues. The highest YI values in grilled and deep fryingmushrooms could be due to the higher temperaturesapplied in these methods which are related to Maillardreaction development; however, this parameter was notcorrelated with the antioxidant activity in this assay.

The parameter E, named as color, is calculatedfrom the equation E¼ (L

�2þ a�2þ b

�2)1/2 and it issuitable to understand the final color of a food asdetermined by its three color coordinates L�, a�, andb�. Observing data from Table 4, all the E values fromcooked mushrooms were lower than the raw ones,especially in deep frying mushrooms where the valuesdecreased up to 50% in the case of L. edodes.Therefore, it can be summarized that darkening ofmushrooms during cooking was mainly linked to thechanges induced by the thermal treatment on their

nutritional profile as well as by the possible formationof Maillard reaction products (MRP) during the moresevere processing conditions.

Absorbance at 420 nm

The development of the browning during the cookingprocess involves the appearance of high molecularweight compounds came from the Maillard reaction(Jim�enez-Zamora et al. 2016). Since these compoundsare associated with antioxidant properties, the higherantioxidant activity measured in microwaved andgrilled mushrooms could be due to the formation ofMRP. In order to establish unspecifically the Maillardreaction development in cooked mushrooms, theabsorbance at 420 nm (the typical wavelength for mel-anoidins absorption) was measured (Figure 1).

Comparing the values of absorbance between thedifferent cooking methods, it was noted that extracts ofmicrowaved and grilled samples showed significantlyhigher absorbance than those obtained from boilingand frying methods in all the mushrooms species,which would indicate a greater abundance ofadvanced-final MRP in these samples. Indeed, it seemslogical that boiled and fried samples had the lowest val-ues of absorbance meaning a lessened Maillard reactionrate, since important amounts of protein and carbohy-drates were lost while cooking, as depicted in Table 1.

The major values of absorbance presented byAgaricus bisporus compared with the other mush-rooms of this assay are probably due to the majorlevel of protein presented by Agaricus bisporus(Table 1). If this food matrix has more amino groupsavailable, then it is more prone to react via Maillardpathway, thus a major abundance of MRP increasesthe absorbance values in these mushrooms.

Figure 1. Determination of absorbance at 420 nm in metha-nolic and aqueous-acetone extracts of cooked mushrooms asunspecific index of Maillard reaction development during cook-ing (mean± SE, n¼ 3). For each mushroom, different lettersindicate significant differences between culinary techniques(p< .05).

INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 295

A noteworthy and significant relationship wasdepicted between absorbance values at 420 nm and theantioxidant activity with any of the method used(DPPH, r¼ 0.7734; FRAP, r¼ 0.8430; and ABTS,r¼ 0.9049, all p values ¼ .0000), a fact pointing to cer-tain implication of MRP formed during culinary treat-ments in the antioxidant capacity detected.

Conclusion

This study evaluates the effects of four cooking meth-ods (boiling, microwaving, grilling, and deep frying)on the proximate composition, b-glucans content, andantioxidant activity in four of most consumed mush-room worldwide. The results show a decrease in pro-tein and ash content in cooked mushrooms withrespect to raw ones. Frying treatment produced moresevere losses in protein, ash, and carbohydrates con-tent but increased the fat and energy. Boilingimproved the total glucans content by enhancing theamount of b-glucans; this increase could be due to theleaching of soluble substances during boiling, whichcould result in a concentration effect of the fraction ofinsoluble carbohydrates. Regarding the antioxidantactivity, a significant decrease was detected speciallyafter boiling but also after frying, while grilled andmicrowaved mushrooms had higher values of antioxi-dant activity. This increase could be due to Maillardreaction development as supported by the highestabsorbance values measured at 420 nm. Microwavingand grilling were the more adequate culinary treat-ments to preserve the nutritional profile of mush-rooms. Therefore, the cooking technique clearlyinfluences the nutritional value and the antioxidantactivity of mushrooms so that the adequate selectionof the culinary method is a key factor to preserve thenutritional profile of this highly consumed food.

Disclosure statement

The authors report no conflicts of interest. The authorsalone are responsible for the content and writing of thisarticle.

Funding

This research was financed by the Department of Industry,Innovation and Employment of La Rioja and the EconomicDevelopment Agency of La Rioja (ADER).

References

AOAC, 1995. Official Methods of Analysis, 16th ed.Association of Official Analytical Chemistry, Arlington,USA.

Barros L, Baptista P, Correia DM, Morais JS, Ferreira ICFR.2007. Effects of conservation treatment and cooking onthe chemical composition and antioxidant activity ofPortuguese wild edible mushrooms. J Agric Food Chem.55:4781–4788.

Ca�glar{rmak N. 2007. The nutrients of exotic mushrooms(Lentinula edodes and Pleurotus species) and an estimatedapproach to the volatile compounds. Food Chem.105:1188–1194.

Ca�glar{rmak N. 2009. Determination of nutrients and vola-tile constituents of Agaricus bisporus (brown) at differentstages. J Sci Food Agric. 89:634–638.

Cheung PCK. 2010. The nutritional and health benefits ofmushrooms. Nutr Bull. 35:292–299.

Choi Y, Lee SM, Chun J, Lee HB, Lee J. 2006. Influence ofheat treatment on the antioxidant activities and poly-phenolic compounds of Shiitake (Lentinus edodes) mush-room. Food Chem. 99:381–387.

CIE Colorimetric Committee. 1974. Technical notes: work-ing program on color differences. J Opt Soc Am.64:896–897.

Crisan EV, Sands A. 1978. Nutritional values. In: Chang ST,Hayes WA, editors. The biology and cultivation of ediblemushrooms. New York: Academic Press. p. 137–168.

Delgado-Andrade C, Rufi�an-Henares JA, Morales FJ. 2007.Lysine availability is diminished in commercial fiber-enriched breakfast cereals. Food Chem. 100:725–731.

Diez VA, Alvarez A. 2001. Compositional and nutritionalstudies on two wild edible mushrooms from northwestSpain. Food Chem. 75:417–422.

Dikeman CL, Bauer LL, Flickinger EA, Fahey GC. 2005.Effects of stage of maturity and cooking on the chemicalcomposition of select mushroom varieties. J Agric FoodChem. 53:1130–1138.

Dubost NJ, Ou B, Beelman RB. 2007. Quantification of pol-yphenols and ergothioneine in cultivated mushrooms andcorrelation to total antioxidant capacity. Food Chem.105:727–735.

Faller ALK, Fiahlo E. 2009. The antioxidant capacity andpolyphenol content of organic and conventional retailvegetables after domestic cooking. Food Res Int.42:210–215.

Ghorai S, Banik SP, Verma D, Chowdhury S, Mukherjee S,Khowala S. 2009. Fungal biotechnology in food and feedprocessing. Food Res Int. 42:577–587.

Giangiaconmo R, Messina G. 1988. Determinazione oggetivadel colore del latte alimentare mediante colorimetria tris-timolo. Sci Tec Latt.– Casearia. 39:20–39.

Henry CJK. 1998. Impact of fried foods on macronutrientintake, with special reference to fat and protein. Grasas YAceites. 49:336–339.

Jaworska G, Pogo�n K, Berna�s E, Duda-Chodak A. 2015.Nutraceuticals and antioxidant activity of prepared forconsumption commercial mushrooms Agaricus bisporusand Pleurotus ostreatus. J Food Qual. 38:111–122.

Jim�enez-Zamora A, Delgado-Andrade C, Rufi�an-HenaresJA. 2016. Antioxidant capacity, total phenols and colorprofile during the storage of selected plants used for infu-sion. Food Chem. 199:339–346.

Kettawan A, Chanlekha K, Kongkachuichai R, CharoensiriR. 2011. Effects of cooking on antioxidant activities and

296 I. RONCERO-RAMOS ET AL.

polyphenol content of edible mushrooms commonly con-sumed in Thailand. Pak J Nutr. 10:1094–1103.

Lam YS, Okello EJ. 2015. Determination of lovastatin,b-glucan, total polyphenols, and antioxidant activity inraw and processed oyster culinary-medicinal mushroom,Pleurotus ostreatus (higher basidiomycetes). Int J MedMushrooms. 17:117–128.

Manzi P, Aguzzi A, Pizzoferrato L. 2001. Nutritional valueof mushrooms widely consumed in Italy. Food Chem.73:321–325.

Manzi P, Marconi S, Guzzi A, Pizzoferrato L. 2004.Commercial mushrooms: nutritional quality and effect ofcooking. Food Chem. 84:201–206.

Mattila P, K€onk€o K, Eurola M, Pihlava JM, Astola J,Vahteristo L, Hietaniemi V, Kumpulainen J, Valtonen M,Piironen V. 2001. Contents of vitamins, mineral elements,and some phenolic compounds in cultivated mushrooms.J Agric Food Chem. 49:2343–2348.

Morales F, Jim�enez-P�erez S. 2004. Peroxyl radical scaveng-ing activity of melanoidins in aqueous systems. Eur FoodRes Technol. 218:515–520.

Pagliarini E, Vernile M, Peri C. 1990. Kinetic study on colorchanges in milk due to heat. J Food Sci. 55:1766–1767.

Peleg H, Naim M, Rouseff RL, Zehavi U. 1991. Distributionof bound and free polyphenolic acids in oranges (Citrussinensis) and grapefruit (Citrus paradise). J Sci FoodAgric. 57:417–426.

P�erez-Jim�enez J, Saura-Calixto F. 2005. Literature data mayunderestimate the actual antioxidant capacity of cereals. JAgric Food Chem. 53:5036–5040.

Pogo�n K, Jaworska G, Duda-Chodak A, Maciejaszek I. 2013.Influence of the culinary treatment on the quality ofLactarius deliciosus. Foods 2:238–253.

Radzki W, Ziaja-Sołtys M, Nowak J, Rzymowska J, TopolskaJ, Sławi�nska A, Michalak-Majewska M, Zalewska-KoronaM, Kuczumow A. 2016. Effect of processing on the con-tent and biological activity of polysaccharides fromPleurotus ostreatus mushroom. Food Sci Technol.66:27–33.

Ram�ırez-Anaya JP, Samaniego-S�anchez C, Casta~neda-Saucedo MC, Villal�on-Mir M, L�opez-Garc�ıa de la SerranaH. 2015. Phenols and the antioxidant capacity ofMediterranean vegetables prepared with extra virgin oliveoil using different domestic cooking techniques. FoodChem. 188:430–438.

Reis FS, Barros L, Martins A, Ferreira ICFR. 2012a.Chemical composition and nutritional value of the most

widely appreciated cultivated mushrooms: an inter-speciescomparative study. Food Chem Toxicol. 50:191–197.

Reis FS, Martins A, Barros L, Ferreira ICFR. 2012b.Antioxidant properties and phenolic profile of the mostwidely appreciated cultivated mushrooms: a comparativestudy between in vivo and in vitro samples. Food ChemToxicol. 50:1201–1207.

Rop O, Mlcek J, Jurikova T. 2009. Beta-glucans in higherfungi and their health effects. Nutr Rev. 67:624–631.

Rufi�an-Henares JA, Morales FJ. 2007. Effect of in vitroenzymatic digestion on antioxidant activity of coffee mel-anoidins and fractions. J Agric Food Chem.55:10016–10021.

Rufi�an-Henares JA, Delgado-Andrade C. 2009. Effect ofdigestive process on Maillard reaction indexes and anti-oxidant properties of breakfast cereals. Food Res Int.42:394–400.

Saguy IS, Dana D. 2003. Integrated approach to deep fatfrying: engineering, nutrition, health and consumeraspects. J Food Eng. 56:143–152.

Saura-Calixto F, Go~ni I. 2006. Antioxidant capacity of theSpanish Mediterranean diet. Food Chem. 94:442–447.

Shashirekha MN, Rajarathnam S, Bano Z. 2002.Enhancement of bioconversion efficiency and chemistryof mushroom, Pleurotus sajor-caju (Berk and Br.) Sacc.produced on spent rice straw substrate, supplementedwith oil seed cakes. Food Chem. 76:27–31.

Somoza V. 2005. Five years of research on health risks andbenefits of Maillard reaction products: An update. MolNutr Food Res. 49:663–672.

Sun L, Bai X, Zhuang Y. 2014. Effect of different cookingmethods on total phenolic contents and antioxidant activ-ities of four Boletus mushrooms. J Food Sci Technol.51:3362–3368.

Synytsya A, Mickova K, Jablonsky I, Slukoya M, Copikova J.2008. Mushrooms of genus Pleurotus as a source of diet-ary fibers and glucans for food supplements. Czech JFood Sci. 26:441–446.

Tan YS, Baskaran A, Nallathamby N, Chua KH,Kuppusamy UR, Sabaratnam V. 2015. Influence of cus-tomized cooking methods on the phenolic contents andantioxidant activities of selected species of oyster mush-rooms (Pleurotus spp.). J Food Sci Technol. 52:3058–3064.

Wasser SP. 2011. Current findings, future trends, andunsolved problems in studies of medicinal mushrooms.Appl Microbiol Biotechnol. 89:1323–1332.

INTERNATIONAL JOURNAL OF FOOD SCIENCES AND NUTRITION 297