Effect of Different Cooking Methods on the True Retention of Vitamins, Minerals, and Bioactive Compounds in Shiitake Mushrooms (Lentinula edodes)

Kyeongmin Lee; Hana Lee; Youngmin Choi; Younghwa Kim; Heon Sang Jeong; Junsoo Lee

doi:10.3136/fstr.25.115

Abstract

This study investigated the effect of cooking methods including steaming, blanching, microwaving, boiling, and roasting on the true retention of minerals, vitamins, and bioactive compounds in shiitake mushrooms (Lentinus edodes). The proximate composition significantly decreased after cooking. In general, the true retentions of minerals were lowest in the boiled samples. Microwaved and roasted samples showed higher true retentions of minerals than other cooking methods. Boiling resulted in the lowest true retention levels of vitamins and bioactive compounds, while roasting resulted in the higher true retention values. The 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radical scavenging activities of blanched, boiled, and steamed samples decreased compared with the activities of the raw samples. However, the antioxidant activities of microwaved and roasted samples were maintained or increased. These results suggest that cooking causes changes in nutritional content that are dependent on the type of cooking method. In addition, when estimating the dietary intake of nutrients in the future, nutrient retention should be taken into consideration.

Introduction

The consumption of various mushroom species has increased in recent years (Mattila et al., 2001). Besides their unique flavor and sensory properties, mushrooms provide excellent health benefits (Guillamon et al., 2010). The shiitake mushroom (Lentinula edodes), also known as the black oak mushroom, is the second most cultivated edible mushroom in the world, comprising about 25 % of world mushroom production (de Roman et al., 2006). Shiitake mushrooms contain various bioactive compounds such as polysaccharides, fiber, ergosterol, thiamin, riboflavin, ascorbic acid, folate, niacin, minerals and several polyphenolic compounds known to be excellent antioxidants (Jiang et al., 2010). Previous studies of shiitake mushrooms showed anti-tumor activity, antimicrobial properties, the improvement of liver function, and the reduction of viremia in patients with chronic hepatitis B (Hirasawa et al., 1999).

In general, cooking methods induce significant changes in the chemical composition, texture, and enzymes of foods (Medoua and Oldewage-Theron, 2014). Mushrooms may be cooked in different ways before consumption according to the recipes and culinary traditions of various countries. Therefore, mushrooms prepared by different cooking methods can have an impact on the nutrients and other compounds in the meal (Falandysz and Borovicka, 2013). The retention of vitamins and bioactive compounds after cooking has been studied in food science. For example, thermal processing of blueberries results in the loss of polyphenolic compounds and decreased antioxidant capacities (Brownmiller et al., 2008). In addition, lower nutrient amounts and reduced antioxidant activity have been reported in cooked mushrooms (Manzi et al., 2004), while polyphenol concentrations and antioxidant properties are increased by heat treatment in shiitake mushrooms (Choi et al., 2006). However, it is still unclear as to the effect of cooking methods on nutrient retention. Therefore, it is necessary to establish how different cooking methods affect the nutritional and health benefits of natural food materials, such as the retention of vitamins and functional compounds. Information on the changes in individual nutrients of shiitake mushrooms due to different cooking methods has been scarce. The objective of this study was to compare the effect of cooking methods (steaming, boiling, blanching, microwaving, and roasting) on the nutritional composition and true retention values of shiitake mushrooms.

Materials and Methods

Materials and chemicals Shiitake mushrooms (Lentinula edodes) were obtained from a market (Chengju, Republic of Korea). Thiamin, niacin, cobalamin, ascorbic acid, ergosterol, folate, γ-aminobutyric acid (GABA) and ergothioneine were purchased from Sigma-Aldrich (St. Louis, MO, USA). α-Ketoglutaric acid, sodium cyanide, α-amylase, pepsin, metaphosphoric acid, phosphate, and ferrous chloride were also obtained from Sigma-Aldrich.

Cooking methods Fresh shiitake mushrooms (Lentinula edodes) were washed to clean out all the silt and mud, then were cut into 5 mm thick slices. For each cooking method, 200 g of mushroom slices were used. For blanching, the mushroom slices were placed in boiling water (1 : 5, sample/water) for 1 min. The same sample/water ratio was used for boiling, but the mushroom slices were cooked for 15 min. The microwave process used a microwave oven without water. Samples were put on a glass plate and cooked at 2,450 MHz with 700 W for 3 min. Mushrooms were steamed for 10 min. Samples were roasted in a pan without oil for 5 min. The raw and cooked samples were freeze-dried.

Determination of proximate compositions and mineral contents Proximate compositions including moisture, fat, and ash were measured using AOAC procedures. Mineral elements in the shiitake mushrooms were determined by inductively coupled plasma optical emission spectroscopy (ICP-OES, Optima 5300 DV, Perkin Elmer, USA). One gram of sample was transferred to a digestion tube. Then, nitric acid (20 mL) and hydrogen peroxide (5 mL) were added, and the mixture was put on a hot plate until the liquid became clear. After digestion, solvent was added to increase the volume to 50 mL, and the resulting solution was used for the analysis of individual metal contents by ICP-OES.

Analysis of vitamins Thiamin and niacin were analyzed according to Kim et al. (2014). The folate content was assessed using the previous method (Chen and Eitenmiller, 2007). Vitamin B₁₂ contents were determined according to the method of a previous study (Marley et al., 2009). The amount of ascorbic acid was measured according to the method of Lee et al. (2018). The determination of ergosterol (vitamin D₂) content was followed by the method of Shao et al. (2010).

Determination of functional compounds Ergothioneine content was determined using the previous method by Yang et al. (2004). The content of GABA was determined according to the method of Zhang and Bown (1997). Glucan contents was measured using a commercial mushroom and yeast β-glucan assay kit K-YBGL (Megazyme Int., Bray, Ireland) with manufacturer's protocol.

Determination of total polyphenol and flavonoid contents Polyphenolic contents in shiitake mushrooms were determined using the Folin-Ciocalteu method (Dewanto et al., 2002) and flavonoid contents in the shiitake mushrooms were determined according to the procedure described in a previous study (Zou et al., 2004).

Determination of antioxidant activities The 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radical cation scavenging activity of shiitake mushrooms was estimated according to the method of Re et al. (1999). The 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity of shiitake mushrooms was measured according to the method of a previous study (Kim et al., 2002).

Calculation of true retention To measure the true retention of compounds, the change in weight during cooking had to be taken into account. This information was calculated using the nutritional compound contents in the raw samples and the nutritional compound contents in the cooked samples. The true retention was calculated by the equation proposed in a previous study (Murphy et al., 1975).

Statistical analysis One-way analysis of variance (ANOVA) was performed using SAS version 9.4 (SAS Institute, Cary, USA). Results were expressed as the mean and standard deviation (SD). Significant differences were determined by Duncan's test (p < 0.05).

Results and Discussion

Proximate composition The proximate compositions and true retentions in raw and cooked shiitake mushrooms are shown in Table 1. The moisture content of raw shiitake mushrooms was 83.34 g/100 g. The moisture values of cooked shiitake mushrooms, conversely, range from 78.27 to 82.86 g/100 g, indicating a decrease in moisture after cooking. The true retention values of water in cooked shiitake mushrooms range from 67.53 to 87.57 %. The protein content of the raw sample was 4.59 g/100 g, while the values of the cooked samples range from 3.89 to 5.57 g/100 g. The true retention value of protein in the blanched (74.65 %) and boiled (75.17 %) samples were markedly lower than that of the other cooked mushrooms. The fat content ranges from 0.13 to 0.25 g/100 g, and the ash content ranges from 0.45 to 1.05 g/100 g. The true retention value of fat in microwaved shiitake mushrooms was the lowest (46.14 %) of all the samples. The true retention value for ash of cooked mushrooms ranged from 45.50 to 86.24 %. The decrease in protein and ash contents after blanching and boiling are likely a result of the diffusion of certain minerals into the cooking water (Wang et al., 2010). The protein and ash contents were higher in roasted mushrooms compared with raw, however, the true retention value for roasted mushrooms was not higher than that of the raw mushrooms due to water loss. Similar results have been reported for sea bass flesh (Badiani et al., 2013). After cooking, all true retention values of water, protein, fat and ash had decreased compared with the raw material.

Table 1. Proximate composition of raw and cooked shiitake mushrooms (Lentinula edodes)

Sample	Cooking yield (%)	Water		Protein		Fat		Ash
Sample	Cooking yield (%)	g/100g CW¹	TR (%)²	g/100g CW	TR (%)	g/100g CW	TR (%)	g/100g CW	TR (%)
Raw	100.00	83.34^a	100.00^a	4.59^c	100.00^a	0.24^a	100.00^a	0.88^b	100.00^a
Blanching	83.72	82.86^a	83.24^bc	4.09^d	74.65^d	0.22^a	75.95^ab	0.63^c	60.41^c
Boiling	88.79	82.15^a	87.57^b	3.89^e	75.17^d	0.22^a	80.83^ab	0.45^d	45.50^d
Microwaving	82.69	79.46^bc	78.84^cd	4.91^b	88.38^b	0.13^b	46.14^b	0.88^b	83.41^b
Steaming	79.72	80.39^b	76.89^d	4.63^c	80.35^c	0.25^a	82.86^ab	0.88^b	79.83^b
Roasting	71.90	78.27^c	67.53^e	5.57^a	87.26^b	0.22^a	66.06^ab	1.05^a	86.24^b

1 CW = cooked weight.

2 TR (true retention, %) = (Nc × Gc)/(Nr × Gr) × 100, Nc = nutrient content per gram of mushrooms after cooking, Gc = grams of mushrooms after cooking, Nr = nutrient content per gram of mushrooms before cooking, Gr = grams of mushrooms before cooking.

Mineral contents The contents and true retention values of minerals in raw and cooked mushrooms are presented in Table 2. It is evident that K, P, and Mg are the main constituents in the ash. The K contents were especially high in comparison to those of Na, which is considered to be nutritionally advantageous (Mattila et al., 2001). The K, Mg and P contents in boiled mushrooms were lower than the same values in other cooked mushrooms. In contrast, the mineral contents in microwaved mushrooms were the highest values among the cooked mushrooms. The highest reduction in mineral content was observed in boiled mushrooms, followed by blanching and steaming. However, microwaving and roasting treatments resulted in greater retention of all minerals over boiling, blanching, and steaming treatments. These results show that cooking loss was dependent on the type of cooking method irrespective of the type of mineral. Cooking loss of minerals is suspected to be caused by the outflow of minerals from food (Kimura and Itokawa, 1990). Puupponen-Pimiä et al. (2003) also reported that losses of minerals during cooking were not caused by destruction but only by leaching into the cooking water. Taken together, microwaving or roasting can prevent the cooking loss of minerals in shiitake mushrooms.

Table 2. Essential element contents in raw and cooked shiitake mushrooms (Lentinula edodes)

Sample	Ca		K		Mg		P		Mn		Na		Fe		Cu		Zn
Sample	mg/kg CW¹	TR (%)²	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)	mg/kg CW	TR (%)
Raw	18.13^d	100.00^ab	3917.35^c	100.00^a	216.49^c	100.00^a	1385.93^c	100.00^a	2.14^bc	100.00^a	20.67^c	100.00^a	4.82^a	100.00^a	1.57^b	100.00^a	12.69^c	100.00^a
Blanched	25.62^ab	118.38^a	2517.22^e	53.79^d	173.68^d	67.16^d	1126.79^d	68.06^d	1.60^d	62.80^c	21.28^c	86.26^ab	3.21^b	55.79^b	1.18^d	62.88^d	13.05^c	86.11^c
Boiled	22.57^c	110.42^ab	1380.95^f	31.31^e	123.19^e	50.50^e	854.26^e	54.71^e	1.25^e	52.08^c	17.47^d	74.98^b	3.23^b	59.58^b	0.81^e	45.94^e	13.08^c	91.55^abc
Microwaved	23.57^bc	107.51^ab	4178.42^b	88.20^b	240.84^b	91.99^b	1522.63^b	90.84^b	2.32^bc	89.60^ab	23.75^b	95.01^a	4.32^a	74.20^a	1.61^b	84.67^b	14.74^b	96.08^ab
Steamed	22.18^c	97.58^b	3434.29^d	69.89^c	213.59^c	78.65^c	1367.40^c	78.65^c	2.10^c	78.24^b	24.43^b	94.21^a	4.37^a	72.28^b	1.47^c	74.55^c	14.21^b	89.29^bc
Roasted	27.65^a	109.68^ab	4449.53^a	81.67^b	267.25^a	88.76^b	1703.76^a	88.38^b	2.65^a	89.08^ab	27.44^a	95.42^a	4.68^a	69.75^b	1.76^a	80.23^bc	16.27^a	92.22^abc

1 CW = cooked weight.

Vitamin contents Vitamin contents and true retention values in raw and cooked shiitake mushrooms are shown in Table 3. The thiamin content of raw shiitake mushrooms was 0.43 mg/100 g, and the thiamin content of cooked shiitake mushrooms ranged from 0.03 (boiled) to 0.28 mg/100 g (roasted). The true retention of thiamin in cooked shiitake mushrooms ranged from 5.2 % (boiled) to 47.2 % (roasted). The results show that thiamin content was significantly decreased in cooked shiitake mushrooms compared with the raw shiitake mushrooms. The highest level of niacin in cooked mushrooms was present after roasting. The highest loss of vitamins was caused by the boiling process. The vitamin B₁₂ content in roasted shiitake mushroom was considerably higher than that after other cooking processes. The vitamin C content in shiitake mushroom was also significantly higher after roasting and microwaving than it was after boiling. The lowest level of ergosterol was present in after the boiling treatment. The folate content in shiitake mushroom was noticeably higher after the microwaving and roasting process than after other processes. The results show that vitamin contents significantly decreased in shiitake mushrooms after cooking treatments, especially boiling. In general, thermal cooking treatments are known to cause a decrease in the amount of vitamins. The loss of water-soluble vitamins can probably be ascribed to water leaching and thermal degradation as reported in a previous study (Lee and Kader, 2000). Moreover, boiling leads to high losses in ascorbic acid content while steaming and microwaving cause only small losses. For better vitamin retention, Erdman and Klein (1982) have suggested using minimal cooking water and cooking for short time periods. The true retention of ergosterol was not greatly altered after cooking as compared with water-soluble vitamins. Fat-soluble vitamins are said to be more heat-stable than water-soluble vitamins (Ersoy and Özeren, 2009). In general, the carotenoid content is not changed by common household cooking methods such as microwaving, steaming, and boiling, but extreme heat can result in oxidative destruction of carotenoids (Thane and Reddy, 1997). Therefore, these results suggest that the loss of water-soluble vitamins was more common than the loss of fat-soluble vitamins for shiitake mushrooms after general cooking methods.

Table 3. Vitamin contents in raw and cooked shiitake mushrooms (Lentinula edodes)

Sample	Vitamin B₁ (Thiamin)		Vitamin B₃ (Niacin)		Vitamin B₁₂ (Cobalamin)		Vitamin C (Ascorbic acid)		Vitamin D₂ (Ergosterol)		Vitamin B₉ (Folate)
Sample	mg/100 g CW¹	TR (%)²	mg/100 g CW	TR (%)	µg/100 g CW	TR (%)	mg/100 g CW	TR (%)	mg/100 g CW	TR (%)	µg/100 g CW	TR (%)
Raw	0.43^a	100.00^a	53.78^a	100.00^a	0.53^c	100.00^bc	7.00^c	100.00^b	60.19^d	100.00^a	54.75^a	100.00^a
Blanched	0.18^bc	36.23^b	4.01^c	6.24^c	0.46^c	73.11^cd	4.63^d	55.35^c	63.20^cd	87.93^bc	13.02^d	19.92^e
Boiled	0.03^d	5.21^b	1.12^c	1.85^a	0.43^c	71.40^d	3.01^e	38.18^d	55.23^e	81.52^c	10.92^e	17.71^e
Microwaved	0.13^cd	25.05^b	4.78^c	7.35^c	0.59^bc	92.04^bcd	8.74^b	103.30^b	64.88^c	89.15^bc	36.61^b	55.29^b
Steamed	0.18^bc	33.73^b	2.23^c	3.31^c	0.73^b	111.28^ab	8.51^b	96.87^b	70.66^b	93.59^ab	28.44^c	41.42^d
Roasted	0.28^b	47.15^b	32.16^b	42.78^b	0.93^a	127.29^a	11.69^a	120.30^a	73.99^a	88.39^bc	36.96^b	48.54^c

1 CW = cooked weight.

Bioactive compound contents The functional compound contents and true retention in raw shiitake mushrooms and the changes after cooking treatments are presented in Table 4. The GABA content of cooked shiitake mushrooms ranged from 0.41 (boiled) to 6.62 mg/100 g (roasted). The retention of GABA in mushrooms varies significantly depending on the cooking treatment. The true retention of GABA of the cooked mushrooms ranged from 7.4 (boiled) to 100.00 % (roasted). All cooking methods significantly reduced ergothioneine content in the shiitake mushrooms. Among the cooking treatments, boiling caused the highest loss of ergothioneine in the shiitake mushrooms. Cooking processes using less water and/or with a shorter cooking time can maintain ergothioneine and phenolic compound contents in the cooked mushrooms (Nguyen et al., 2012). The polyphenol and flavonoid contents in raw shiitake mushrooms were 28.56 mg gallic acid equivalent/100 g and 4.13 mg catechin equivalent/100 g, respectively. Significant losses in polyphenolic and flavonoid contents of shiitake mushrooms were shown for all cooking methods. The tendency for the reduction of polyphenols and flavonoids could be due to from disruption of the plant tissue and their release from the food matrix after heating (Faller and Fialho, 2009). As shown in Table 4, glucan retentions in the mushrooms were not influenced by the heat treatments. The true retention of glucan was not changed after any of the cooking methods. It is reported that beta glucan has thermostable activity (Jensen et al., 1996) which would explain why glucan content was not reduced by the various cooking treatments. Therefore, microwaving and roasting were better than other cooking methods for the retention of functional compounds including GABA, ergothioneine, polyphenols and flavonoids, while boiling showed the highest decrease in the functional compound content of the mushrooms.

Table 4. Functional compound contents in raw and cooked shiitake mushrooms (Lentinula edodes)

Samples	GABA		Ergothioneine		Polyphenol		Flavonoid		Glucan
	GABA		Ergothioneine		Polyphenol		Flavonoid		Total		Alpha		Beta
	mg/100g CW¹	TR (%)	mg/100g CW	TR (%)	gallic acid mg/100g CW	TR (%)	catechin mg/100g CW	TR (%)	g/100g CW	TR (%)	g/100g CW	TR (%)	g/100g CW	TR (%)
Raw	4.72^b	100.00^a	15.68^b	100.00^a	28.56^c	100.00^a	4.13^c	100.00^c	11.23^c	100.00^b	0.70^c	100.00^b	10.54^c	100.00^b
Blanched	1.71^d	30.40^cd	9.14^d	48.76^d	18.56^d	54.39^c	3.21^d	65.00^d	14.79^ab	111.69^a	0.86^bc	101.70^b	13.93^ab	112.37^a
Boiled	0.41^e	7.41^d	4.64^e	26.25^e	10.53^e	32.71^d	2.11^e	45.41^e	13.69^b	112.24^a	1.01^ab	136.43^ab	12.68^b	110.61^a
Microwaved	4.19^bc	73.31^ab	15.86^b	83.63^b	31.70^b	91.77^a	7.27^a	145.59^a	14.02^b	104.39^ab	0.98^ab	120.87^ab	13.04^b	103.28^ab
Steamed	3.27^c	55.30^bc	12.34^c	62.73^c	25.70^c	71.73^b	4.83^b	92.54^c	15.47^ab	112.77^a	1.22^a	138.43^ab	14.24^ab	111.04^a
Roasted	6.62^a	100.00^a	16.69^a	76.52^b	36.67^a	92.25^a	7.43^a	129.34^b	16.45^a	99.02^b	1.03^ab	104.05^b	15.42^a	98.68^b

1 CW = cooked weight.

Antioxidant activities The antioxidant activity of raw shiitake mushrooms and the changes in activity after cooking treatments are present in Fig. 1 and 2. The ABTS and DPPH radical scavenging activities of raw shiitake mushroom were 174.1 and 116. 9 mg TEAC mg/100 g, respectively. The ABTS and DPPH radical scavenging activities were significantly reduced after blanching and boiling compared with the values of the raw mushrooms. However, antioxidant activities after microwaving and steaming were maintained compared to those of fresh mushrooms. Roasted mushrooms showed increased antioxidant activities compared with those of raw mushrooms. A similar trend was observed in the true retention values of polyphenols and flavonoids. In particular, boiling caused the lowest true retention of polyphenols and flavonoids, as well as the lowest radical scavenging activities. Kenny and O'Beirne (2009) indicated that the loss of antioxidant activity was relative to the contact area between the vegetables and water as well as the processing time. It was clear that the contact area in microwaving and roasting processes was much smaller than that in boiling. For this reason, it was thought that the vegetables' antioxidant capacities did not decrease during microwaving. In a previous study, the antioxidant activity of barley was increased by roasting and microwave cooking treatments (Sharma and Gujral, 2011). Microwave heating retains the active components in cooked tissue (Yamaguchi et al., 2001). The antioxidant activity of vegetables cooked by microwaving was generally higher than that of vegetables cooked in boiling water, because microwaving, roasting, and baking do not stimulate the release of ascorbic acid or other antioxidants from cooked tissue (Jimenez-Monreal et al., 2009). Also, various antioxidant substances are leached into the water during boiling, which results in a decrease of the food's antioxidant capacities (Francisco et al., 2010). Therefore, microwaving and roasting were better methods for retaining antioxidant activity than other cooking methods.

Fig. 1.

ABTS radical scavenging effects of shiitake mushroom (Lentinula edodes) extracts (50 mg/mL). Values with different letters above the bar graphs are significantly different at the 5 % level as determined by the one-way ANOVA and Duncan's test.

Fig. 2.

DPPH radical scavenging effects of shiitake mushroom (Lentinula edodes) extracts (50 mg/mL). Values with different letters above the bar graphs are significantly different at the 5 % level as determined by the one-way ANOVA and Duncan's test.

In conclusion, the stability of proximate composition, minerals, vitamins, and functional compounds in shiitake mushrooms varies depending on the cooking method. Accordingly, to increase the dietary intake of proximate composition, minerals, vitamins, and functional compounds, and to enhance their bioavailability, a recommended general strategy would be to optimize cooking processes such that any appreciable decline of materials is prevented while the bioavailability is increased. We also provided important information regarding the impact of different cooking treatments on the true retention of nutrients and bioactive compounds in shiitake mushrooms. Higher true retention of all nutrients and bioactive compounds were observed in the roasted and microwaved mushrooms. Boiled mushrooms showed the lowest retention value of water soluble vitamins, bioactive compounds, and antioxidant capacities. Despite the reduction in vitamins and other bioactive compounds, consumption of boiled mushrooms is still one of the more common cooking methods. Therefore, using minimal cooking water could be recommended for better retention values of nutrients and bioactive compounds as well as antioxidant activity.

Acknowledgement This study was supported by the Rural Development Administration (project number PJ01339807).

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