The Nutritional and Health Benefits Of

REVIEW

The nutritional and health benefits ofmushroomsnbu_1859 292..299

P. C. K. CheungFood and Nutritional Sciences Programme, School of Life Sciences, the Chinese University of Hong Kong, University Science Centre, Shatin, New Territories,Hong Kong, China

Summary Both wild and cultivated mushrooms have been consumed by humans for theirnutritional and medicinal benefits. Nutritionally, mushrooms are low in energy andfat but high in protein, carbohydrate, and dietary fibre. Mushrooms contain avariety of minerals and trace elements such as potassium, and copper and vitaminssuch as riboflavin, niacin, and folates. They have been used as food for centuriesbecause of their unique taste. Apart from being recognised as a nutritious food,certain mushrooms are also an important source of biologically active compoundswith potential additional medicinal value in Chinese medicine. Bioactive secondarymetabolites found in mushrooms include phenolic compounds, sterols and triter-penes. In vitro and in vivo studies with mushrooms and isolated bioactive constitu-ents have purported many pharmacological effects such as anti-tumour,antioxidant, antiviral, hypocholesterolemic and hypoglycaemic effects. Consump-tion of mushrooms or mushroom products in our daily diet may provide healthbenefits.

Keywords: bioactive constituents, medicinal effects, mushrooms, nutritional values

Introduction

Mushrooms are fungi with distinctive fruiting bodies,which are large enough to be seen with the naked eyeand to be picked by hand (Chang & Miles 1992).Mushrooms can be broadly grouped into three catego-ries: (1) edible; (2) medicinal; and (3) poisonous.Edible mushrooms (mainly the fruiting body) can beconsumed either as flesh (e.g. Agaricus bisporus orbutton mushroom) or dried (e.g. Lentinus edodesor shiitake) or preserved in other ways. Medicinalmushrooms are fungi not for culinary purposes but

contain bioactive components (polysaccharides and orbioactive constituents) that have medicinal application(e.g. Ganoderma lucidum or lingzhi) (Wasser 2010).Poisonous mushrooms have been proved to be or sus-pected of being poisonous (e.g. Amanita phalloides ordeath cap). As far as human health is concerned,according to de Romn et al. (2006), both edible andmedicinal mushrooms may have beneficial effects forhumans. In some cases, high levels of heavy metalsoccur in wild edible mushrooms, and some poisonousspecies are being mistaken for edible ones. Certainmushroom species contain chemical groups (mycotox-ins) such as the cyclopeptide, phenylhydrazine andisooxazole that can be highly toxic to humans (Berger& Guss 2005). This overview focuses on the healthbenefits of the nutrients and non-nutrient compoundsin edible mushrooms, as well as the bioactive chemicalcomponents in medicinal mushrooms.

Correpondence: Professor Peter C. K. Cheung, Food andNutritional Sciences Programme, School of Life Sciences, theChinese University of Hong Kong, University Science Centre,Shatin, New Territories, Hong Kong, China.E-mail: [email protected]

292 2010 The AuthorJournal compilation 2010 British Nutrition Foundation Nutrition Bulletin, 35, 292299

Wild and cultivated mushrooms

Wild mushrooms have been part of the human diet forcenturies because of their nutritional and organolepticcharacteristics and purported medicinal properties (deRomn et al. 2006). The traditional and contemporaryuses of wild edible fungi/mushrooms as food and/or inmedicine have been reviewed recently (Hobbs 1986; Boa2004). Some of the wild mushrooms (of which severalalso are cultivated) that are used as food and/or for theirpotential medicinal properties are listed in Table 1.Among these species, A. bisporus and Pleurotus ostrea-tus are the two most cultivated edible mushroomsworldwide (Sanchez 2010). Other edible mushroomswith high economic value include black truffle (Tubermelanosporum), cep (Boletus edulis), and chanterelle(Cantharellus cibarius) from Europe and the matsutake(Tricholoma matsutake) and shiitake (L. edodes) vari-eties from China and Japan. Previously, only a smallnumber of edible mushroom species were cultivated suc-cessfully under controlled conditions in mushroomhouses and accepted as a food of economic importance(Smith 1972). Recently, the number of cultivated mush-rooms has risen to almost 30 and world production ofmushrooms has increased dramatically from 6.1 milliontons in 1997 to 12.2 million tons in 2002 (Chang 2006).The trend to increase mushroom production is expectedto continue into the future.

Nutrient composition of edible mushroomsand their health effects

Introduction

The nutritional composition of some wild and ediblemushrooms can be found in previous publications(Crisan & Sands 1978; Chang &Miles 2004; de Romnet al. 2006; Kalac 2009). Several regional studies havebeen carried out on the nutritional quality of ediblemushrooms, including those produced in tropical areas(Aletor 1995; Sanmee et al. 2003), India (Longvah &Deosthale 1998), North America (Leichter & Bandoni1980) and Europe (Senatore 1992; Dez&Alvarez 2001;Manzi et al. 2001; Caglarirmak et al. 2002). In general,mushrooms are low in energy and fat but contain con-siderable amounts of protein, dietary fibre, vitamins, andminerals (Crisan & Sands 1978). Table 1 shows thenutrient composition of some selected mushrooms.

Proteins

In general, the crude protein content of edible mush-rooms varies greatly and ranges from 15% to 35% ofdry weight (DW), depending on the species, varieties,and stage of development of the fruiting body (Crisan &Sands 1978; Longvah & Deosthale 1998; Manzi et al.1999; Dez & Alvarez 2001; Mdachi et al. 2003). The

Table 1 Proximate composition of some common mushroom species that can be used as food and medicine*

Species Common names Crude protein Crude fat Carbohydrate Crude fibre Ash Reference

Agaricus bisporus Button mushroom 23.934.8 1.78.0 51.362.5 8.010.4 7.712.0 Crisan and Sands (1978)Agaricus blazei Murrills Agaricus 26.7 2.6 45.5 18.3 6.8 Tsai et al. (2008)Auricularia auricula-judae Black fungus or jelly ear 8.1 1.5 81.0 6.9 9.4 Crisan and Sands (1978)Boletus edulis Cep 29.7 3.1 51.7 8.0 5.3 Crisan and Sands (1978)Cantharellus cibarius Chanterelle 21.5 5.0 64.9 11.2 8.6 Crisan and Sands (1978)Cordyceps sinensis Caterpillar fungus 21.9 8.2 24.2 n.d.|| 2.9 Hsu et al. (2002)Ganoderma tsugae Ling chih or Reishi 8.8 5.7 10.4 73.4 1.7 Tseng et al. (2005)Grifola frondosa Maitake 21.1 3.1 58.8 10.1 7.0 Mau et al. (2001)Hericium erinaceus Monkeyhead or bearded tooth 22.3 3.5 57.0 7.8 9.4 Mau et al. (2001)Lentinus edodes Shiitake 13.417.5 4.98.0 67.578.0 7.38.0 3.77.0 Crisan and Sands (1978)Pleurotus ostreatus Oyster mushroom 10.530.4 1.62.2 57.681.8 7.58.7 6.19.8 Crisan and Sands (1978)Tremella fuciformis White jelly fungus or silver ear

mushroom4.6 0.2 94.8 1.4 0.4 Crisan and Sands (1978)

Tricholoma giganteum Matsutake 16.1 4.3 70.1 4.5 5.0 Mau et al. (2001)Tuber melanosporum Black truffle 23.3 2.2 66.2 27.9 8.3 Crisan and Sands (1978)Vovariella volvacea Straw mushroom 30.1 6.4 50.9 11.9 12.6 Crisan and Sands (1978)

*All data presented as percentage of dry weight (DW).The nitrogen factor used for crude protein calculation was 4.38.The carbohydrate content was calculated by subtracting difference.The crude fibre contains mainly the water-insoluble fibre fraction.||n.d. not determined.

Nutritional and health benefits of mushrooms 293

2010 The AuthorJournal compilation 2010 British Nutrition Foundation Nutrition Bulletin, 35, 292299

difference in the crude protein content between wild andcultivated mushrooms is not significant (Oyetayo et al.2007). With reference to the Food and AgricultureOrganization (FAO) standard, the protein quality ofmushrooms is better than most plant proteins (FAO1991). The in vivo true protein digestibility values for P.ostreatus and L. edodes are 73.4% and 76.3%, respec-tively (Adewusi et al. 1993; Dabbour & Takruri 2002).These values are comparable with those of legumes,which are around 7080% (Wong & Cheung 1998), butare lower than those of animal protein, which are morethan 90% (McDonough et al. 1990).With a few excep-tions, the amount of essential amino acids in mushroomproteins ranges from 30 to 50 g/100 g protein DW(Manzi et al. 1999). Mushroom proteins are relativelyrich in the amino acids threonine (4195 mg/g proteinDW), valine (3689 mg/g protein DW), glutamic acid(130240 mg/g protein DW), aspartic acid (91120 mg/g protein DW %), and arginine (37140 mg/gprotein DW) but are poor in methionine (1.222 mg/gprotein DW) and cysteine (1619 mg/g protein). It hasalso been reported that lysine, leucine, isoleucine andtryptophan are the limiting amino acids in some ediblemushrooms (Cheung 1997; Manzi et al. 1999; Dez &Alvarez 2001). Levels of free amino acids in mushroomsare rather low, ranging from 7.0 to 12 mg/g DW, withglutamic acid (220240 mg/g protein DW) and alanine(app.180 mg/g protein DW) as the major ones (Manziet al. 1999). Together with 5-nucleotides such as5-adenosine monophosphate, 5-cytosine monophos-phate, and 5-guanosine monophosphate, free aminoacids such as aspartic acid and glutamic acid are similarto monosodium glutamate (MSG) in that they contrib-ute to the unique taste of mushrooms (Mau et al. 2001).

Lipids

Edible mushrooms are generally low in lipids (usuallyless than 5% DW). Their fatty acid profile favoursunsaturated fatty acids, especially linoleic acids (688840 mg/g lipid DW) (Cheung 1997; Longvah & Deost-hale 1998; Dez & Alvarez 2001; Yang et al. 2002).Although the level of linolenic acid is generally low inmushrooms (Yilmaz et al. 2006), it contributes greatlyto the flavour of mushrooms because of its role as theprecursor to 1-octen-3-ol, which is the principal aro-matic compound known as fungal alcohol in mostmushrooms (Maga 1981).

Carbohydrates

The total carbohydrate content of mushrooms, includ-ing digestible and non-digestible carbohydrate, varies

with species and ranges from 35% to 70% DW(Longvah & Deosthale 1998; Dez & Alvarez 2001;Mau et al. 2001). Digestible carbohydrates found inmushrooms include mannitol and glucose, usuallypresent in very small amounts (less than 1% DW) andglycogen (510% DW). Mushroom carbohydrates,therefore, are not a major source of energy for humans.Non-digestible carbohydrates include oligosaccharidessuch as trehalose and non-starch polysaccharides (NSPs)such as chitin, b-glucans and mannans, which are themajor portion of mushroom carbohydrates. MushroomNSPs can be regarded as dietary fibre, which may havephysiological benefits for humans. These are discussedfurther in the section on cell wall polysaccharides. Thereis large variation in the dietary fibre content of mush-rooms, depending on their morphological form andspecies. The fruiting bodies of some mushroom specieshave low levels of dietary fibre (e.g. 4.5% DW in Tri-coloma giganteum), whereas others are high in fibre(e.g. 49.7% DW in Auricularia auricular-judea)(Cheung 1997; Dez & Alvarez 2001). In general, mush-rooms provide dietary fibre, with 100 g of fresh mush-rooms providing between 5% and 25% of therecommended dietary intake (18 g of NSP fibre/day inthe UK) (Manzi et al. 2001). Mushroom dietary fibrepredominantly comprises water-insoluble fibre, mainlychitin and b-glucans with low levels of water-solubledietary fibre (less than 10%).

Ash and minerals

The ash content of wild edible mushrooms ranges from6% to 11% DW and contains a wide variety of minerals(Zakhary et al. 1983). The ash content (% DW) of somecommon edible mushrooms is as follows: P. ostreatus(6.9), Leccinum edodes (5.9) and Hericium erinaceus(9.4) (Manzi et al. 1999; Mau et al. 2001).

Edible mushrooms contain the spectrum of mineralsand trace elements. Common edible mushrooms such asP. ostreatus, L. edodes and A. bisporus have beenreported to contain various levels of potassium (27004700 mg/100 g DW), phosphorus (5001400 mg/100 gDW), magnesium (20200 mg/100 g DW), zinc (4.79.2 mg/100 g DW), and copper (0.503.5 mg/100 gDW) (Zakhary et al. 1983; Verma et al. 1987; Vetter1990). The Boletus genus, in particular, contains thehighest level of selenium (3090 mg/100 g fresh weight)among other mushrooms (Cocchi et al. 2006; Falandysz2008). Several recent reports have been published on themetal content of wild edible mushrooms with an empha-sis on metals such as lead, cadmium and mercury thatmay have toxicological effects on humans (Ouzouni

294 P. C. K. Cheung


et al. 2007; Kalac 2010). Mushrooms are known toaccumulate heavy metals, the levels of which are deter-mined by species, substrate composition and environ-mental factors (Svoboda et al. 2006; Garcia et al. 2009).However, detailed evaluation on the toxicological riskand nutritional assessment of such substances in mush-rooms is limited.

Vitamins

While little information on the vitamin contents of wildmushrooms is available, data on cultivated mushroomsshow that they contain several vitamins including ribo-flavin (vitamin B2), niacin, and folates in concentrationsthat are species dependent and vary within the range of1.85.1, 3165, and 0.300.64 mg/100 g DW, respec-tively (Mattila et al. 2001). The riboflavin content inmushrooms is higher than that generally found in veg-etables, and some varieties of A. bisporus have beenreported to have concentrations as high as those foundin eggs and cheese (Mattila et al. 2001). Cultivatedmushrooms contain niacin, but again, the content variesfrom 34109 mg/100 g DW for P. ostreatus, 1299 mg/100 g DW for L. edodes and 3657 mg/100 g DW forA. bisporus (Crisan & Sands 1978; Bano & Rajarath-nam 1986). Mushrooms contain moderately highamounts of folates at concentrations that are generallysimilar to those found in vegetables (Beelman &Edwards 1989). Vitamin D is almost entirely absent incultivated mushrooms, but levels of ergosterol, the pro-vitamin of ergocalciferol, are relatively high (400600 mg/100 g DW). Ergocalciferol (provitamin D) canbe converted into vitamin D in the presence of sunlight(Mattila et al. 2002). With the exception of folate,studies on the bioavailability of vitamins from mush-rooms are rare (Clifford et al. 1991).

Bioactive components of medicinalmushrooms and their potentialhealth effects

Introduction

The medicinal use of mushrooms has a long historyin Asian countries (especially in China, Korea andJapan), whereas their use as medicine in theWest is morerecent (Wasser 2010). Medicinal mushrooms are char-acterised by having more fungal cell wall materials andsecondary metabolites that have a wider range of phar-macological activities compared with edible mushrooms(Lindequist et al. 2005). The fungal cell wall containsmainly b-glucan-chitin complexes and mannoproteins

(Bartnicki-Garcia 1970), which are not digested enzymesin the human gastrointestinal tract, and for this reasonthey are therefore classified as dietary fibre (Cheung1996). Large variations in the structure and content ofthese mushroom cell wall polymers exist, which aredependant on the developmental stage of the mush-rooms (Zhang et al. 2007). Other than cell wall polysac-charides and proteins, medicinal mushrooms containhigh molecular weight substances such as lignins andlow molecular weight substances such as triterpenes andphenolics (Lindequist et al. 2005).

Cell wall polysaccharides

Bioactive properties have been reported for mushroomcell wall polysaccharides, namely immunostimulating,anti-tumour, hypoglycaemic, and antioxidant effects,mainly through various in vivo and in vitro studies, themechanisms of which are not, however, fully understood(Reshetnikov et al. 2001; Wasser 2002; Zhang et al.2007; Cheung 2008; Ooi 2008). Polysaccharides(mainly b-glucans) and polysaccharide-protein com-plexes isolated from a number of mushrooms such aslentinan from L. edodes, b-glucan fraction D fromGrifola frondosa, and Krestin (PSK) andpolysaccharide-peptide from Trametes versicolor canstimulate the non-specific immune system and exertanti-tumour activity through the stimulation of thehosts defence system in animal studies (Reshetnikovet al. 2001). These compounds are considered to beimmunomodulators and have been used clinically inadjuvant tumour therapy with differing degrees ofsuccess in prolonging the survival time of cancerpatients (Taguchi et al. 1982; Mitomi et al. 1992;Kodama et al. 2002). It has also recently been shownthat a low molecular weight polysaccharide (48 kilodal-tons) isolated from Agaricus blazei can suppress angio-genesis in vivo, thus shedding new insight into themechanisms behind the purported anti-tumour effects ofmushroom polysaccharides (Niu et al. 2009). Ganopoly,a polysaccharide isolated from G. lucidum, which is themost well-known medicinal mushroom, has beenstudied for its clinical efficacy in alleviating cancer-related symptoms and is widely sold as an over-the-counter product in Asian countries (Gao et al. 2003).Ganopoly has also been shown to lower post-prandialglucose levels in patients with type 2 diabetes mellitusduring a Phase I/II clinical trial (Gao et al. 2004).Other than the b-glucan-type polysaccharides, furthermushroom heteropolysaccharides such as glucuronoxy-lomannan (Tremellastin) obtained from Tremella fuci-formis and Tremella mesenterica have been shown to



demonstrate multiple pharmacological activities includ-ing immunomodulatory and hypoglycaemic effects inexperimental studies (Wasser et al. 2002; Lo et al.2006). It has also been demonstrated that mushroomcell wall polysaccharides have in vitro free radical scav-enging activity (hydroxyl and superoxide) and may havethe potential to be developed as antioxidants (Liu et al.1997).

Low molecular weight compounds

Triterpenes represent one of the most diverse and yetimportant group of bioactive compounds found inmedicinal mushrooms. G. lucidum is a classic example,having more than 120 different triterpenes (Kim & Kim1999). A number of triterpenes from G. lucidum havebeen shown to be active antiviral agents against HIVtype 1 as well as herpes simplex virus type 1 (El-Mekkawy et al. 1998; Mothana et al. 2003). Some trit-erpenes from G. lucidum can inhibit the biosynthesis ofcholesterol (Komoda et al. 1989) as well as have theability to inhibit angiotension converting enzymes(Morigiwa et al. 1986) or platelet aggregation (Su et al.1999), thus having the potential to lower the risk ofatherosclerosis.

Investigations into mushrooms as a source ofnatural antioxidants, particularly the correlationbetween mushroom phenolic compounds and their invitro antioxidant properties, have increased (Cheunget al. 2003; Cheung & Cheung 2005; Elmastas et al.2007; Ferreira et al. 2009; Vidovic et al. 2010). Studieson some edible mushrooms, including Dictyophoraindusiata, Flammulina velutipes, G. frondosa, H. eri-naceus, L. edodes, Tricholoma giganteum andP. ostreatus, have shown that their extracts (methan-olic and aqueous) are rich in phenolic compounds thathave strong in vitro antioxidant properties includinginhibition of lipid peroxidation, scavenging of freeradicals, as well as ferric reducing power (Mau et al.2002; Cheung et al. 2003; Elmastas et al. 2007). Fla-voglaucin was the first mushroom phenolic antioxidantisolated from the mycelium of Eurotium chevalieri(Ishikawa et al. 1984). Subsequently, two novel preny-lated phenolic substances known as asiaticusin A andasiaticusin B have been isolated from the fruiting bodyof Boletus asiaticus (Wada et al. 1996). Recently, phe-nolic acids, including trans-cinnamic acid, hydroxy-benzoic acid, protocatechuic acid and caffeic acid,have also been isolated from A. bisporus and L.edodes (Mattila et al. 2001). Studies on certain phe-nolic compounds in Inonotus hispidus and ergosterolperoxide present in several mushrooms also show in

vitro antiviral activity against influenza viruses type Aand B (Awadh et al. 2003).

High molecular weight compounds

Proteins from G. lucidum and sugar-binding proteins(lectins) from mushrooms have been reported to modu-late the human immune system by stimulating the func-tional maturation of human immune cells in vitro(Wang et al. 1996; Lin et al. 2009). Other fungal mac-romolecules such as protein-degrading enzymes fromHandkea utriformis, ribosome-inactivating proteinsfrom Hypsizygus marmoreus and lectins (sugar-boundproteins) from P. ostreatus have demonstrated in vitroanti-tumour activities (Wang et al. 2000; Lam et al.2001; Lam & Ng 2001). Lectins isolated from Agaricuscampestris and A. bisporus have also been shown toenhance insulin release in isolated Langerhans rat islets(Ahmad et al. 1984). Finally, water-soluble lignin iso-lated from Fuscoporia oblique and L. edodes has beenreported to have in vitro antiviral activities by inhibitingHIV proteases (Tochikura et al. 1988; Ichimura et al.1998).

Conclusion

Mushrooms are valuable resources for food, medicineand nutraceuticals (Lakhanpal & Rana 2005). Theycontain a large array of nutrients and other naturalphytochemicals that have a wide range of nutritionaland health benefits. These benefits will have potentialimplications such as boosting the immune system, pro-viding an anti-cancer function as well as controllingblood lipids and glucose levels in humans. Given themany mushroom species that have not yet been studied,it is anticipated that new discoveries of the health ben-efits in mushrooms will continue and promising mush-room treatments and products for human diseases maybe found in the future (Wasser 2010).

Conflict of interest

The author has no conflict of interest to disclose.

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