HEALTH AND NUTRITIONAL
PROPERTIES
OF MUSHROOMS
Report created by:
Irene Roncero Ramos
Doctor of Food Nutrition and Technology
[email protected]
January, 2015
Technological Centre for Research on
Mushroom (CTICH)
Ctra. de Calahorra, Km. 4
26560 Autol (La Rioja)
Spain
Tel. +34 941 39 09 60 / Fax +34 941 39 09 61
[email protected]
www.ctich.com
TO
European Group of Mushroom Growers
(GEPC)
44 rue d’Alésia
75014 Paris
FRANCE
GROUPEMENT EUROPEEN DES PRODUCTEURS
DE CHAMPIGNONS
[email protected]
EUROPEAN MUSHROOM GROWERS’ GROUP
www.infochampi.com
Tel. +33 153 91 45 23
Health and nutritional properties of mushrooms
CONTENTS
INTRODUCTION .......................................................................................................... 5
1. Production and consumption of mushrooms ...............................................................5
2. Mushrooms: a little known food ..................................................................................7
From an organoleptic perspective .........................................................................7
From a nutritional perspective ..............................................................................8
From a medicinal perspective................................................................................8
NUTRITIONAL PROPERTIES OF MUSHROOMS…………………………………………………………10
1. Energy and moisture content .....................................................................................12
2. Carbohydrates.............................................................................................................13
3. Fibre ............................................................................................................................14
4. Lipids ...........................................................................................................................15
5. Proteins .......................................................................................................................16
6. Minerals ......................................................................................................................17
7. Vitamins ......................................................................................................................21
BIOACTIVE COMPOUNDS OF MUSHROOMS………………………………………………………….26
1. Polysaccharides……………………………………………………………………………………………………..26
Beta-glucans.........................................................................................................26
Polysaccharide-protein complex .........................................................................28
2. Other bioactive compounds………………………………………………………………………………….29
Low molecular weight compounds........................................................................ 29
High molecular weight compounds ....................................................................... 29
3
Health and nutritional properties of mushrooms
HEALTH PROPERTIES OF MUSHROOMS ..................................................................... 31
1. Antioxidant.................................................................................................................... 31
2. Antitumoral ................................................................................................................... 33
3. Immunomodulatory ...................................................................................................... 34
4. Antiobesity and antihyperlipidaemia ........................................................................... 36
5. Cholesterol reducing property ..................................................................................... 37
6. Antidiabetic .................................................................................................................. 39
7. Antihypertensive........................................................................................................... 40
8. Hepatoprotective .......................................................................................................... 41
9. Antiallergenic ................................................................................................................ 42
10. Antimicrobial .............................................................................................................. 42
11. Antiviral ...................................................................................................................... 44
12. Role of mushrooms in neurodegenerative disease ................................................... 44
CONCLUSIONS .......................................................................................................... 46
BIBLIOGRAPHY .................................................................................................................. 47
4
Health and nutritional properties of mushrooms
INTRODUCTION
1. Production and consumption of mushrooms
Mushroom growing has been increasing worldwide in the past years and this
trend is expected to continue in the coming years. In Europe the production of fresh
mushroom is increasing, while the production of mushrooms for processing is almost
stable, but slightly decreasing. The consumption of fresh mushroom is growing in most
European countries, while the consumption of canned mushroom is decreasing, in
particular in the countries where the consumption is traditionally higher, such as
France and Germany. The overall increase in consumption is probably induced by the
better knowledge of the product and its health and nutritional virtues.
China is the biggest producing country worldwide, followed by the European
Union and by the United States. In Europe, the biggest producing country is Poland,
followed by the Netherlands, France and Spain.
The most commonly grown mushroom in Europe is of the specie Agaricus
bisporus (button mushroom), which represents 95% of the production. Other
commonly grown Mushrooms are Pleurotus ostreatus (Oyster mushroom) y Lentinula
edodes (shiitake). In Europe 65% of mushrooms are intended for the fresh market, and
35% are processed for the canned and the frozen industry.
The European Mushroom Growers Group (GEPC) was created in 1980 by France,
Germany, and the Netherlands. Nowadays the GEPC is composed of 10 delegations
representing the mushroom growers from Belgium, Denmark, France, Germany,
Hungary, Ireland, Italy, the Netherlands, Poland, and Spain. In 2015, those 10 countries
accounted for 90% of the overall European production of mushroom, which amounted
at 1,111,700 tons – feet cut.
The GEPC defends the interests of the fresh and processed cultivated
mushrooms production on a EU and international level.
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Health and nutritional properties of mushrooms
Evolution of the mushroom production in Europe
EU production of mushrooms (net tons)
2006 - 2015
1,400,000
1,200,000
1,000,000
800,000
600,000
400,000
200,000
0
2006
2007
2008
mushrooms for processing
2009
2010
2011
2012
fresh mushrooms
2013
2014
2015
Total production
Graph 1. Figures of the Agaricus bisporus mushroom production in the European Union from
2006 to 2015.
6
Health and nutritional properties of mushrooms
2. Mushrooms: a little known food
Traditionally, mushrooms have been used in the east both for eating and for
medicinal purposes. In Europe they began to be used only relatively recently. In some
countries, as is the case in Spain, their consumption is rare and they are not usually
used as the main product in the meal unless they are used sporadically. People are not
aware of the benefits that this food may have on health and the role they can play in
the prevention of some diseases. Hence, the aim of this report is to spread this
information among health and nutrition professionals, and as a consequence, to
society.
Scientific studies on the nutritional and medical properties of mushrooms are
becoming increasingly important. This report is a compilation of their health properties
and the recent studies that exist on the subject. Better knowledge of the benefits that
these products bring will help us achieve a healthier diet and improve our state of
health.
From an organoleptic perspective
The first thing about mushrooms that draws our attention is their flavour, aroma
and texture, i.e. their organoleptic characteristics. Mushrooms have a characteristic
taste, known as umami (delicious savoury in Japanese), making them flavourful and
versatile for using in various culinary dishes.
For decades we were told that there are only four basic sensations captured by
the sense of taste: sweet, salty, acidic and bitter. However, there is a fifth perception
of taste: the umami. This taste is found in foods rich in glutamate. Glutamate is a
natural aminoacid present in almost all foods, particularly in proteins, such as dairy
produce, meat and fish, and in vegetables and mushrooms. The shiitake mushroom is a
good example of this taste.
Benefits of the umami taste
The umami taste, and more precisely its main ingredient glutamate, is used to
reduce the intake of salt. When glutamate is added to meals, the quantity of salt can
be reduced by between 30 and 40%, without affecting the palatability. Excessive intake
of salt affects blood pressure, which may cause hypertension and coronary cardiac
disease and, as the intake of sodium in the Spanish population exceeds the
recommended limits, there are currently many scientific studies being carried out on
the acceptability of substituting part of the salty taste of meals by the umami taste.
In a study done in Finland, the United States and Japan, in which glutamate was
added to foods low in salt, it was observed that the consumers’ acceptance of these
foods was increased. In fact, the United States Institute of Medicine found that the
combination of glutamic acid with sodium forms the monosodium glutamate
compound, responsible for the umami taste, and it has been proved that it is possible
to maintain the palatability of foods with a lowered level of sodium when monosodium
glutamate is substituted for part of the salt (Institute of Medicine, 2010; Roininen et
al., 1996).
7
Health and nutritional properties of mushrooms
Furthermore, the intake of glutamate increases the secretion of digestive juices
and insulin, which improves digestion. They also demonstrated that free glutamate
plays a beneficial role in the regulation of gastrointestinal functions which could be
used in the treatments of gastric illnesses such as dyspepsia and gastritis. (Nakamura
et al., 2008).
From a nutritional perspective
Mushrooms are foods with highly valued nutritional properties. In particular is
the low caloric value that they have due to their large water content (80%-90%), from
26-35 kcal for every 100 grams. In addition, they are a good source of proteins with an
aminoacid composition more similar to animal protein than to vegetable, making them
the ideal complement for vegetarian diets. Their high fibre content and low fat content
are desirable characteristics for a healthy food.
With regard to microelements, mushrooms are an important source of group B
vitamins, especially B2 and B3, and of vitamin D precursors like ergosterol that facilitate
the absorption of calcium and phosphorus (Barros et al., 2007a). They also contain
minerals essential for the correction functioning of our body, principally selenium,
phosphorus and potassium (Manzi et al., 2001). Their sodium content is very low,
which enables these products to be used for low salt content diets.
From a medicinal perspective
As mentioned previously, in the east these products have been known for
thousands of years for their curative and medicinal properties. However, in the west
they have only been used for a few decades. Mushrooms were used in popular Asian
medicine against various illnesses because they were considered natural remedies.
Chinese pharmacopeia documents the use of hundreds of species of mushrooms for a
wide range of diseases. Today it is known that the health properties of mushrooms are
due to the bioactive properties that they possess.
Some of the compounds and fractions isolated from medicinal fungi have shown
promising immunomodulatory, antitumoral, cardio-vascular, antiviral, antibacterial,
antiparasitic, hepatoprotector and antidiabetic properties. The polysaccharides
obtained from mushrooms are considered to be compounds capable of modulating the
immune response in animals and humans and inhibiting the growth of certain tumours
(Lindequist et al., 2005; Cheung, 2008).
Mushrooms are a valuable source of nutrients and bioactive compounds, and
their characteristic flavour and aroma have recently awoken a growing culinary
interest. Their potential beneficial effects on human health make them firm
candidates for what may be termed functional foods.
8
Health and nutritional properties of mushrooms
Scientific name
Common name
Agaricus
Agaricus bisporus
Common, button
Agaricus blazei
Brazil, sun
Agaricus brunnescens
Portobello
Pleurotus
P. ostreatus
P. eryngii
P. cornucopiae (var. citrinopileatus)
Oyster
King oyster
Yellow oyster
P. cornucopiae
Branched oyster
P. pulmonarius
Italian, Indian, Lung
P. sajor-caju (P. djamor)
Pink oyster
Lentinula Edodes
Shiitake
Agrocybe Aegerita
Poplar
Ganoderma lucidum
Pholiota Nameko
Hericium Erinaceus
Reishi, Lingzhi
Nameko
Lion’s mane
Hypsizygus Ulmarius
Elm
Hypsizygus Tessulatus
White beech (Shimeji)
Grifola frondosa
Maitake
Flammulina velutipes
Enoki
Cantharellus cibarius
Chanterelle
Trametes versicolor
Turkey tail
Auricularia auricula
Judas’ ear
Table 1. Summary of some mushrooms mentioned in this report
9
Health and nutritional properties of mushrooms
NUTRITIONAL PROPERTIES OF MUSHROOMS
The table below gathers data on the nutritional content of cultivated
mushrooms:
Common
(per 100g
edible
portion)
Shiitake
(per 100g
edible
portion)
RDI
men
RDI
women
Energy (kcal)
26
34
3000
2300
Proteins (g)
1.8
2.24
54
41
Total lipids (g)
0.3
0.49
<100
<77
Saturated FA(g)
0.07
-
<23
<18
Tr
Tr
>57
>43
Polyunsat. FA (g)
0.17
-
10-20
8-15
Ω-3 (g)
0.133
-
0.33-3.3
0.25-2.6
Ω-6 (g)
0.032
-
1.3-16.5
1.2-10.4
0
0
<300
<230
Monounsat. FA (g)
Cholesterol (mg)
Carbohydrates
4
6.79
375-450
288-345
Fibre (g)
2.5
2.5
38
29
Water (g)
91.4
89.74
1000-2000
1000-2000
Calcium (mg)
9
2
800
800
Iron (mg)
1
0.41
10
18
Iodine (μg)
3
140
110
Magnesium (mg)
14
20
350
330
Zinc (mg)
0.1
1.03
15
15
Sodium (mg)
5
9
<2400
<2400
Potassium (mg)
470
304
3500
3500
Phosphorus mg)
115
112
700
700
Selenium (μg)
9
5.7
70
55
Thiamine (mg)
0.1
0.015
1.2
0.9
Riboflavin (mg)
0.41
0.217
1.8
1.4
Niacin (mg)
4.6
3.877
20
15
Vitamin B6 (mg)
0.1
0.293
1.8
1.6
Folic acid (μg)
23
18
400
400
Vitamin B12 (μg)
0
0
2
2
Vitamin C (mg)
4
0
60
60
Vitamin A (μg)
1000
800
0
0
Vitamin D (μg)
0
0.5
5
5
Vitamin E (mg)
0.12
0
12
12
Table 2. Nutritional profiles from Food Comparison Tables, Moreiras et al., (2007)
(MUSHROOM). Recommendations: Recommended daily intake (RDI) for men and
women from 20 to 39 years with moderate physical activity
10
Health and nutritional properties of mushrooms
Agaricus
bisporus, raw
Agaricus bisporus,
canned
Agaricus bisporus,
sauteed
/100 g
/100 g
/100 g
Macronutrients
Energy
kcal
25
21.7
59
Protein
g
1.8
2.4
2.4
Fat
g
0.43
0.39
4.27
FA saturated
g
0.07
0.11
1.32
FA poli
g
0.14
0.26
1.55
Cholesterol
mg
0
0.14
4.7
Carbohydrate
g
2.73
0.98
0.33
Sugars
g
0.2
0.2
Traces
Fibres
g
1.33
2.31
4.8
Water
g
92.8
93.1
87
Vitamins
Vitamin B1 (Thiamin)
mg
0.09
0.05
0.07
Vitamin B2 (Riboflavin)
mg
0.31
0.12
0.34
Vitamin B3 (Niacin)
mg
3.2
0.5
2.9
Vitamin B5 (Phantotenic
mg
2
0.34
1.05
Vitamin B6
mg
0.18
0.02
0.18
Vitamin B9 (Folate)
µg
33.5
26.3
26.8
Vitamin C (Ascorbic acid)
mg
1
6.5
1.41
Minerals
Calcium
mg
28.5
24.6
16.9
Iron
mg
1.66
0.9
0.65
Magnesium
mg
8.61
6.48
12.7
Phosphorus
mg
56.4
47
79
Potassium
mg
326
88.6
341
Sodium
mg
16.9
310
107
Copper
mg
0.54
0.17
0.2
Selenium
µg
5.62
< 4.1
Original source: Ciqual French food composition table version (2013)
https://pro.anses.fr/TableCIQUAL/index.htm
14.4
Table 3. Differences in the nutritional composition of the mushroom depending on the
culinary process used.
11
Health and nutritional properties of mushrooms
1. Energy and moisture content
The calorific or energy value of a food is related to the amount of calories (Kcal)
that it contains. To calculate the energy value of a food we need to know the quantity
of nutrients that it contains and the calories of each (carbohydrates 4 kcal/g, proteins 4
kcal/g and lipids 9 kcal/g).
Mushrooms have approximately 26-35 kcal/100 g depending on the variety. To
be precise, the common mushroom is one of the ones containing the fewest calories
(26 kcal/100g) and although the shiitake is the mushroom with the greatest energy
value, it only contains 35 kcal/100 g.
Figure 6. Energy content of some mushrooms in comparison to normal vegetable consumption
(U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Edible fungi have a very high percentage of moisture (81.8-94.8%). The
variability of this percentage depends on the specific species, the crop, and conditions
for growing and storage, etc. (Manzi et al., 1999).
Due to their high moisture content, mushrooms have a very short useful life. The
food industry attempts to conserve these foods for a greater length of time and to
preserve their nutritional qualities by various types of processing, such as drying,
sterilisation and freezing (Barros et al., 2007b), including in recent years selling them
freeze-dried (Hernando et al., 2008).
The content of dry material in fresh mushrooms is very low therefore, at around
10%, and mainly composed of carbohydrates, proteins, fibre and minerals.
Mushrooms are foods with a high satiating power and low energy density, i.e.
the relation between the calories and the volume of a food. The high degree of
moisture that they have is related to the sensation of satiety that they give and as they
also contain very few calories, they are a very useful product for low calorie diets.
12
Health and nutritional properties of mushrooms
2. Carbohydrates
The total content of carbohydrates in mushrooms, including digestible and nondigestible carbohydrates, varies according to the species from 35% to 70% of the dry
weight (Díez and Álvarez, 2001; Mau et al., 2001). The types of digestible
carbohydrates that are present in mushrooms are: manitol (0.3-5.5% in dry matter
(Vaz et al., 2011), glucose (0.5-3.6%) (Kim et al., 2009) and glycogen (1-1.6% in dry
matter) (Díez and Álvarez, 2001). Non-digestible carbohydrates include
oligosaccharides such as trehalose and non-starchy polysaccharides such as chitin, βglucans and mananos, which represent the greater part of mushroom carbohydrates.
According to the bibliography, the level of carbohydrates varies between the
different types of mushroom. Reis and collaborators (2012a) carried out a study on the
nutritional composition of the cultivated mushrooms most consumed on a global level.
The results show that the shiitake mushroom (17.62 g/100g) shows the greatest
quantity of total carbohydrates in comparison with the common mushroom (5.98
g/100g), the oyster mushroom (9.30 g/100g) and the king oyster (8.95 g/100g). In this
study they also analysed the sugar content, such as fructose, manitol and trehalose.
The shiitake again presented the highest levels in these sugars in comparison with the
other mushrooms. It is interesting to note that the common mushroom contains
polysaccharides typical of the animal kingdom, such as glycogen, and does not contain
either starch or cellulose, which are characteristic of plants.
Figure 7. Content in carbohydrates of some mushrooms in comparison with vegetables
normally consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods).
The glycaemic index of a food measures its immediate effect on the increase of
blood sugar and is a defined and constant number for each food. The content in
complex carbohydrates and fibre shows that mushrooms are a very low glycaemic
index food (IG=15), so their digestion is slower and the sugar is released gradually. The
foods with a low glycaemic index are recommended for people suffering from diabetes
since they involve a lower increase in postprandial glycaemia.
13
Health and nutritional properties of mushrooms
3. Fibre
Considered to be dietary fibre are those polymers originating from plants that
are formed by 10 or more monosaccharides that cannot be hydrolised endogenously
by the digestive enzymes and that exercise a physiological effect that is potentially
beneficial for the health. Dietary fibre includes polysaccharides, oligosaccharides and
lignin. The consumption of dietary fibre and its compounds promotes the maintenance
of health and the prevention of certain diseases such as diabetes, cancer,
cardiovascular disease, hypercholesterolemia and obesity (Theuwissen and Mensink,
2008; Charles, 2005; Bordonaro and Sartorelli, 2008). Fibre regulates the absorption of
sugar, absorbs certain organic compounds such as bile acids and can delay the
intestinal absorption of sugar, which is very beneficial in the treatment of diabetes.
Mushrooms are a good source of dietary fibre. According to bibliographical data,
mushrooms contain a greater quantity of insoluble fibre (2.28–8.99 g/100 g edible
portion) than soluble (0.32–2.20 g/100 g edible portion) (Manzi et al., 2004). The
polysaccharides that are found in greater proportions in the common mushroom fibre
are β-glucans (4-13% of the total dietary fibre) followed by chitin (Guillamon et al.,
2010). As with other nutrients, the fibre content will vary depending on the species,
morphology and growth conditions of the mushrooms, as well as their conservation
and the culinary processes that these products undergo. According to Manzi et al.,
(2001 and 2004), the mushrooms presenting the higher percentage of total fibre are
Agrocybe aegerita, Agaricus bisporus, Pleurotus eryngii and Pleurotus ostreatus.
A study carried out in the United Kingdom shows that 100 g of fresh mushrooms
contains between 5% and 25% of the recommended daily intake of fibre (18 g
fibre/day in UK) (Manzi et al., 2001).
Figure 8. Amount of fibre of some mushrooms in comparison to vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
14
Health and nutritional properties of mushrooms
As has already been described above, fibre has many beneficial effects for
health. In recent years numerous studies have been carried out on the effect that
mushroom fibre has on health. Firstly, eating more fibre helps to regulate intestinal
transit. In addition, fibre’s bioactive compounds, type β-glucans, are considered
bioactive compounds that have the effect, among others, of stimulating the immune
response, and are anticancer, hypoglycaemic and antioxidant.
It has been observed that a β-glucan isolated from the fruiting body of Lentinula
edodes, i.e. lentinan, stimulates the immune system in animals, inhibiting the
proliferation of cancer cells. β-glucans are being used as immunomodulatories in
anticancer therapies with some success (Reshetnikov et al., 2001).
Currently, much attention is being given, particularly commercially, to the
functional properties that certain compounds of mushroom fibre possess. Particularly
worthy of note are the β-glucans of the Pleurotus type for their immunomodulatory
properties. In addition, it has been demonstrated that Pleuran, a β-glucan of this type,
has a suppressive effect on tumours (Karácsonyi & Kuniak, 1994).
4. Lipids
Generally, mushrooms are low in fat (less than 5% in dry weight). The
environmental factors that affect the lipid content in mushrooms, their concentration
depending on the growing conditions, can be nutritional factors, oxygen, temperature
and nature of the substrate (Pedneault et al., 2007). Unsaturated fatty acid content is
predominant in mushrooms and therefore is in greater quantities that saturated.
Linoleic acid is that present in a greater proportion in mushrooms (Díez and Álvarez,
2001).
Linolenic and linoleic acids are essential fatty acids for the human being and,
since our body does not synthesise them, we must ingest them with food. Linoliec acid
is an omega 6 fatty acid and linolenic is omega 3, both polyunsaturates, from which
can be synthesised the rest of the omega 6 and omega 3 fatty acids. In addition to the
nutritional importance of linoliec acid, its precursor function in mushrooms of volatile
compounds should also be highlighted, such as 1-octen-3-ol, 3-octanol, 1-octen-3-ona
and 3-octanone (Combet et al., 2006), which are the main aromatic compounds in the
majority of the species (Maga, 1981). These compounds also contribute to the flavour
of the majority of the mushroom species analysed (Guedes de Pinho et al., 2008).
According to the work of Reis et al., (2012a), in which a comparative study of
different cultivated mushrooms was carried out, it was concluded that the shiitake is
the one with the highest levels of polyunsaturates and a lower amount of saturates
than the rest of the mushrooms studied. The species of the genus Pleurotus has a very
similar fatty acid profile and is notable as the one presenting the most
monounsaturated fatty acids.
15
Health and nutritional properties of mushrooms
5. Proteins
The protein content of mushrooms varies between 15 and 35% of dry weight,
depending on the species, varieties and stage of development of the fruiting body
(Manzi et al., 2004; Díez and Álvarez, 2001). The protein digestibility of mushrooms in
general is quite good, for P. ostreatus and L. edodes it is 73.4% and 76.3%, respectively
(Adewusi et al., 1993; Dabbour and Takruri, 2002). These values are comparable with
those for legumes (70-80%) (Wong and Cheung, 1998) but are lower than those of
animal protein that has a digestibility of more than 90% (McDonough et al., 1990).
The common mushroom, unlike the rest of vegetables, contains all the essential
aminoacids (lle, Leu, Lys, Met, Phe, Thr, Trp, Val), which are those that the human
body cannot generate on its own and that have to be ingested in the diet. According to
the World Health Organisation (WHO), common mushrooms are particularly rich in
glutamic acid, aspartic acid and arginine. The aminoacids that present in greatest
quantities in the common mushroom are methionine and cysteine (Manzi et al., 1999).
The genus Pleurotus seems to be the one presenting the greatest protein quality; some
of the varieties of this genus have a good distribution of both essential and nonessential aminoacids (Dundar et al., 2008; Patil et al., 2010).
Figure 9. Protein content of some mushrooms in comparison to vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
The presence of aminoacids in free form is rare. Some of them that can be found
are glutamic acid, ornithine and alanine (Kim et al., 2009). Their basic importance is
that they contribute to the particular aroma and flavour of the mushrooms, for
example glutamic acid is principally responsible for the umami taste.
According to the Food and Agriculture Organisation (FAO), the protein quality of
mushrooms is better than that of most vegetables (FAO, 1981). The composition in
aminoacids of the proteins of the mushrooms is comparable to animal protein, which
16
Health and nutritional properties of mushrooms
is important today in countering a high consumption of protein foods of animal origin,
particularly in developed countries (Guillamon et al., 2010).
American scientists carried out a study on healthy and obese individuals in which
they substituted beef in lunch by common mushrooms for 4 consecutive days. The
result was that the amount of energy and fat ingested on the day reduced when the
mushroom was introduced into the diet compared with the diet that includes meat.
With regard to the subjects’ assessment of the meals’ palatability and sensation of
appetite and satiety, no significant differences were observed when they were eating
the various culinary preparations. The authors suggest including more low density
calories, such as the common mushroom, into foods in the daily diet in place of foods
with higher energy density, as a strategy to reduce the prevalence of obesity and
overweight in the population (Cheskin et al., 2008).
6. Minerals
Minerals are chemical elements that are fundamental for the normal metabolic
functioning of our body. The mineral nutrients play essential structural and metabolic
roles. The diet must contain them in sufficient but not excessive quantities, in order to
cover the body’s requirements, as well as accessibly, so that needs can be satisfied.
Some are required in quantities greater than 100 milligrams per day (calcium,
phosphorus, sodium and potassium) and others, called oligoelements (iron, fluoride,
iodine, copper, zinc, selenium, etc.), are needed in lesser amounts.
The mineral content in mushrooms varies between 6 and 11% in dry matter,
according to the species. For example, Pleurotus ostreatus has 6.90%, Pleurotus eryngii
8.60%, Lentinula edodes 5.85% and Hericium erinaceus 9.35%.
Compared with other vegetables, mushrooms contain a reasonable quantity of
minerals (Manzi et al., 1999). The macroelements that abound in cultivated
mushrooms are calcium, phosphorus, potassium and magnesium and the
microelements that dominate are copper, selenium, iron and zinc (Cheung, 2008).
Some of the more common cultivated mushrooms, A. bisporus, P. ostreatus and
L. edodes, among others, are rich in potassium (2670-4730 mg/100g in dry matter) and
are considered a good source of phosphorus (493-1390 mg/100g in dry matter),
magnesium (20-200 mg/100g in dry matter), zinc (4,70-9,20 mg/100g in dry matter)
and copper (0.52-3,50 mg/100g in dry matter) (Cheung, 2008).
With regard to the mineral content of mushrooms, it should be pointed out that
the majority of cultivated mushrooms and also some species of the genus Boletus are
rich in selenium in natural form (Cocchi et al., 2006).
Sodium
Sodium requirements in humans are about 3 g/day. Usually, the population
consumes much more sodium than the recommended amount, which is due mainly to
the greater consumption of pre-cooked meals. Excessive consumption of salt causes a
greater risk of high blood pressure.
17
Health and nutritional properties of mushrooms
Figure 10. Sodium content of some mushrooms in comparison to vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Mushrooms contain a very low amount of sodium, which means they are the
ideal food for a low-salt diet. In addition, they have the advantage that they contain
glutamate in natural form. This aminoacid is responsible principally for the umami
taste. The umami taste enables reduction of the amount of salt in meals without losing
the perception of salt.
Potassium
The common mushroom contains relatively high concentrations of potassium
with levels equivalent to 7-9% of the recommended daily intake in an 85 g portion.
Phosphorus
Phosphorus is an essential compound in living organisms since it participates in
numerous vital functions. Phosphorus and potassium are the major elements in the
common mushroom. Mushrooms contain a greater quantity of phosphorus than other
vegetables.
18
Health and nutritional properties of mushrooms
Figure 11. Phosphorus content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Selenium
Compared with other trace minerals such as copper, magnesium and zinc,
selenium is an element that is required in a smaller dose. The recommended daily
intake of selenium for humans is 57 µg (although the values vary between 30 and 80
µg depending on the bibliography). The maximum recommended intake varies
between 100 and 200 µg per day (Jarzynska and Falandysz, 2011). Although only a
small amount is required to cover requirements of selenium, it is not always easy to
obtain the recommended amount through the normal diet.
The foods considered to be good sources of selenium are, among others: crab,
liver, seafood and fish (Rayman, 2000). Currently, mushrooms are also considered to
be rich in selenium. In general, fruit and vegetables are very low in this mineral that is
normally plentiful in fish and meat.
The selenium content in the common mushroom varies from 0.46 to 5.63 ppm in
dry matter depending on the species (Clement, 1998), the average being between 1
and 2 ppm of selenium in dry matter. This quantity represents 15% of the
recommended daily intake in the EEUU. Mushrooms accumulate selenium as a
function of the element’s availability in the medium in which they are growing.
Among selenium’s roles in our body, its antioxidant capacity is foremost, and it
also helps to neutralise free radicals, induces apoptosis, stimulates the immune system
and intervenes in the function of the thyroid gland. Selenium is a compound of various
selenoproteins with a preventive role for some forms of cancer (Lu and Holmgren,
2009). Supplementing with selenium in low doses seems to be beneficial not only in
preventing cancer, but it can also have a positive influence on many other functions in
the body through the reduction of inflammation, heart disease and the regulation of
blood pressure (Brozmanova et al., 2009). The efficacy of selenium compounds as
chemopreventive agents in vivo correlates with its capacity to produce cellular cycle
19
Health and nutritional properties of mushrooms
regulation, stimulate apoptosis and inhibit the migration of tumour cells and invasion
in vitro (Zeng and Combs, 2008).
Figure 12. Selenium content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Selenium and zinc are trace minerals with a known antioxidant potential.
Selenium performs an antioxidant activity through selenoproteins like glutathione
peroxidase and thioredoxine reductase. Zinc is an important co-factor of the
antioxidant enzyme superoxide dismutase. A deficiency in selenium or in zinc entails a
reduction in the antioxidant capacity and the reverse has been demonstrated, that
when there is a supplement of one or both of these, the oxidative condition is
improved (Hu et al., 2010; Sahin and Kucuc, 2003).
In a recent study (Yan and Chang, 2012), Pleurotus ostreatus is enriched with
selenium and zinc and this food is introduced into the diet of experimental animals to
test whether the antioxidant and antitumoral activity were increasing. Pleurotus
ostreatus is capable of accumulating large quantities of trace elements and
incorporating them as organic compounds. This mushroom in itself has a high
antioxidant capacity and if we further enrich it with selenium and zinc it can be seen to
increase this capacity. The results of the study showed that Pleurotus ostreatus
enriched with selenium and zinc improved the antioxidant activity and was preventing
the development of lung cancer in mice. According to the authors, supplementing
mushrooms with these minerals is cheap and safe and can help increase their
antioxidant capacity, thus boosting their antitumoral property.
20
Health and nutritional properties of mushrooms
Figure 13. Zinc content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Earlier investigations carried out at CTICH, that consist in enriching the common
mushroom with selenium in the growing cycle, succeeded in adding value to this
product, through increasing its content. Fortifying substrates is also a potential route
for increasing the level of trace elements in cultivated mushrooms.
7. Vitamins
Vitamins are organic compounds fundamental to life that, when ingested in a
balanced way and in essential doses, promote correct physiological function. The
majority of essential vitamins cannot be synthesised by the body, which means that
they can only be obtained through the intake of food. Each vitamin plays a particular
role in the body. Some, known as co-enzymes, form part of enzymatic systems and
catalyse certain chemical reactions in food metabolism. Mushrooms are considered a
good source of vitamins, especially riboflavin (B2), niacin (B3) and folates (B9) that are
those contained in the greatest amounts.
Mattila et al., (2001) published some data on the content of various vitamins in
cultivated mushrooms, the concentration varying from 1.8 to 5.1 mg/100 g dry matter
for riboflavin, from 31 to 65 mg/100 g dry matter for niacin and from 0.30 to 0.64
mg/100 g dry matter for folates. It is notable that mushrooms contain folates in
quantities that are relatively high and very similar to the concentration that vegetables
present (Beelman and Edwards, 1989). The riboflavin content in mushrooms is also
higher than the concentration present in vegetables and, in addition, some varieties of
Agaricus bisporus present riboflavin concentrations as high as those that can be
found in eggs and cheese (Mattila et al., 2001).
21
Health and nutritional properties of mushrooms
Figure 14. Riboflavin content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
In cultivated mushrooms, the vitamin content can vary from one species to
another. In the case of niacin, it is observed that P. ostreatus presents quantities that
vary between 34 and 109 mg/100 g in dry matter, L. edodes between 12 and 99
mg/100 g in dry matter and A. bisporus between 36 and 57mg/100 g in dry matter
(Crisan and Sands, 1978; Bano and Rajarathnam, 1986).
Figure 15. Niacin content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods)
Vitamins B1, B12 and C are also present in mushrooms although in smaller
quantities (Mattila et al., 2002). The vitamin B1 or thiamine content in mushrooms
varies between approximately 0.60 and 0.90 mg/100 g in dry matter. In the case of
vitamin B12, the amount present is much smaller, between 0.60 and 0.80 µg/100 g in
22
Health and nutritional properties of mushrooms
dry weight. Even so, mushrooms contain more B12 than vegetable since these contain
hardly any of this vitamin. Vegetarian diets are therefore lacking in B12.
Vitamin D
Vitamin D plays an important part in maintaining the organs and systems
through multiple functions, such as the regulation of calcium and phosphorus levels in
the blood, promoting their intestinal absorption from foods and their re-absorption at
renal level. With this, they contribute to bone formation and mineralisation, essential
for skeletal development. In addition, vitamin D has been the subject of much
attention in recent years for its role in muscular function, immunology, the heart,
cardiovascular disease and cancer, etc. (Phillips et al., 2012).
With regard to vitamin D, mushrooms are the only non-animal food that
contains this vitamin (in precursor form) and because of this are the natural source of
vitamin D for vegetarians. The content of D2 (ergocalciferol), one of the forms of
vitamin D, is present in a greater quantity in species of wild mushrooms than in
cultivated species. More specifically, in common mushrooms it has been shown that in
fact the presence of vitamin D2 is greater in wild mushrooms than in cultivated ones.
Furthermore, this vitamin’s distribution has been studied in the fruiting body of
different species, the cap of the mushroom being the part with the greatest
concentration (Mattila et al., 2002).
Figure 16. Vitamin D content of some mushrooms in comparison with vegetables normally
consumed (U.S.D.A., http://ndb.nal.usda.gov/ndb/foods).
As already described, vitamin D is not present as such in mushrooms but it is its
precursor, ergosterol, which is present. The levels of ergosterol, the provitamin of
ergocalciferol (vitamin D2), are relatively high (400 to 600 mg/100 g in dry matter)
(Mattila et al., 2002). The presence of vitamin D in mushrooms is attributed to
exposure to sunlight, which catalyses the conversion of ergosterol in mushrooms into
vitamin D2 through a series of photochemical reactions.
23
Health and nutritional properties of mushrooms
Mushroom growers have incorporated UV light treatments into their growing,
and in this way the mushrooms contain a quantity of vitamin D similar to wild ones
(Simon et al., 2013). Recent analyses in the EEUU carried out on 10 different species of
cultivated mushrooms show that the concentration of vitamin D2 varied between 0.03
and 63.2 mg/100 g (1.2 to 2528 IU/100 g) in fresh weight, it being found that the
highest levels corresponded to the mushrooms that had been exposed to UV rays
during their production (Phillips et al., 2011). Many articles (Ko et al., 2008;
Koyyalamudi et al., 2009; Simon et al., 2011) confirm that exposure to UV light
considerably raises the bio-available content of vitamin D2. It seems that the treatment
is more effective if the packets are arranged in a single layer and uniformly distributed.
The vitamin D2 content can reach a level of 100 mg/kg in dry matter in optimum
conditions (Kalăc, 2013).
24
Health and nutritional properties of mushrooms
Figure 17. Comparison of the content in some micronutrients between mushrooms and other
vegetables (USDA Nutrient Data Laboratory, 2010). Based on the standard portion of
mushrooms (84 g) and vegetables (85 g) of the FDA. (www.ars.usda.gov/nutrientdata)
25
Health and nutritional properties of mushrooms
BIOACTIVE COMPOUNDS OF MUSHROOMS
Traditionally, scientific investigations have been centred on the nutritional
properties of mushrooms. In the last decade, as well as the study of the nutritional
composition of mushrooms, the study of the biologically active compounds that they
contain has become more important, as well as those they have tested with significant
beneficial properties for health.
Numerous bioactive compounds have been identified in mushrooms. The
concentration of these will depend on the variety, substrate, crop, storage and
processing conditions, etc. (Barros et al., 2007b). Among the bioactive compounds are
polysaccharides, proteins, phenolic compounds (flavonoids, lignans and phenolic acids)
lignins, triterpenes, etc. These compounds are responsible for the medicinal properties
that mushrooms have, such as their antioxidant capacity, immunomodulatory property
and anticarcinogenic and hepatoprotector capacities, among others.
1. Polysaccharides
Among the bioactive compounds in mushrooms, polysaccharides are those that
show most antitumoral, antiviral and immunomodulatory activity (Mizuno and
Nishitani, 2013). In particular the polysaccharides that are found on the cellular wall
are those that show most bioactivity.
These polysaccharides are: chitin, cellulose and β-glucans polysaccharideprotein complexes (Zhang et al., 2007). These biologically active polysaccharides can
be found in fruiting bodies and cultivated mycelium and can also be extracted from the
environment in which they are grown. There are numerous studies, both in vivo and in
vitro, in which β-glucans and polysaccharide-protein complexes have been isolated
from different mushrooms and it has been shown that they have important biological
properties as immunomodulatory, antitumoral, hypoglycaemic and antioxidant agents
(Cheung, 2010). Recent investigations have observed that the polysaccharides of
mushrooms can help avoid ontogenesis, through their direct antitumoral activity
against various tumours and also prevent metastasis of the tumour. The effects are
better when they are used together with chemotherapy (Wasser, 2002).
Below are highlighted some of the better known polysaccharides present in
mushrooms, to which are attributed numerous medicinal properties.
β-glucans
- Pleuran. Is a type β-glucan polysaccharide that is found in species of mushrooms
that belong to the genus Pleurotus. This polysaccharide has significant
anticarcinogenic activity and stimulates immunity (Khan and Tania, 2012). In the
study of Jesenak et al., (2013), it is shown that Pleuran reduces morbidity caused
by recurrent infections of the respiratory passages through changes in the
humoral and cellular immunity.
26
Health and nutritional properties of mushrooms
Positive effects have been associated to this compound in the reduction of
cholesterol levels in the blood of rats (Bobek et al., 2001) and hamsters (Cheung,
1998). In humans the β-glucans derived from mushrooms also seem to reduce
cholesterol (Braaten et al., 1994) and LDL in the blood (Behall et al., 1997).
Among the activities of β-glucan, Pleuran stands out as having the best
antioxidant status (it increases the activities of superoxide dismutase,
glutathione peroxidase and glutathione reductase in the liver), as is
demonstrated in a trial carried out on rats (Bobek and Galbavy, 2001).
- Lentinan. Polysaccharide of the mushroom Lentinula edodes (shiitake). According
to the bibliography consulted, Lentinan and Pleuran are the two β-glucans most
used by the pharmaceutical industry since they seem to be those with the best
biological activity. Lentinan stands out mainly for its antitumoral and
immunomodulatory activity. Various studies have demonstrated that this
polysaccharide stimulates the immune function, for example, in the work of
Gordon et al., (1995) with patients with HIV, the treatment of this disease was
combined with 2 mg de Lentinan and the disease’s evolution was improved
thanks to its immunomodulatory effect.
Along the same lines as the polysaccharide from Pleurotus, Lentinan also has
antitumoral activity (Rathee et al., 2011). It was observed that the
administration of Lentinan together with the cancer treatment (chemotherapy)
prolonged patients’ survival time, improved the immunological parameters and
increased the quality of life of patients with cancer of the stomach, cancer of the
colon and other carcinomas, in comparison with patients who were only treated
with chemotherapy (Hazama et al., 1995).
Other effects that have been related to this β-glucan are that it increases
resistance to intestinal mucus inflammation (Zeman et al., 2001) and inhibits the
development of intestinal ulcers (Nosalova et al., 2001). In addition, it shows a
positive effect in peristalsis (Van Nevel et al., 2003). Finally, its capacity to
promote antioxidant enzymatic activity is also significant.
Figure 18. Structure of the polysaccharide lentinan (http://www.biospectrum.com).
- Ganopoly. This polysaccharide has been isolated from Ganoderma lucidum, one
of the mushrooms with the most medicinal properties known. The bioactive
properties of Ganopoly align with that written above for Pleuran and Lentinan. It
27
Health and nutritional properties of mushrooms
has high antitumoral activity; its clinical effectiveness has been demonstrated in
anticancer therapies because it improves the symptoms arising from this disease
(Gao et al., 2003).
The antidiabetic activity that is associated with it is determined by its ability to
lower the postprandial glucose level in patients with type II diabetes (Gao et al.,
2004). It has also been shown that this polysaccharide can act as a powerful
immunostimulant (El Enshasy and Hatti-Kaul, 2013).
- Grifolan. β-glucan extracted from the mushroom Grifola frondosa. This
compound possesses important medicinal properties, including promoting
microphage activity and increasing the production of interleukin IL-1 improving
the immune response.
It has been shown that the polysaccharide Grifolan is capable of increasing the
production of insulin, which means that this compound could be used for the
treatment of diabetes (Manohar et al., 2002). Antifungal activity is also
attributed to this compound. According to Uchiyama et al., (2002), it is able to
suppress the pathogenic fungus Candida albicans that can cause infections in the
oral cavity membranes and systemically, including infections of the lungs, lymph
nodes, liver and spleen.
In addition to the properties already described for this β-glucan, in a study on
mice it was observed that Grifolan can suppress the inflammation of the mucus
membranes of the respiratory tract (Korpi et al., 2003). This polysaccharide also
has anticancer activity because it is capable of restoring the cellular immunity
that is destroyed as a result of the radio- and chemotherapy treatments (Ooi and
Liu, 2000).
Polysaccharide-protein complex
The polysaccharide-protein complexes of mushrooms increase the immune
response, both innate and cellular, and also show antitumoral activity in animals and
humans (Mizuno, 1999; Reshetnikov et al., 2001). The stimulation of the host’s
immune defence by bioactive polysaccharides derived from medicinal mushrooms has
a significant effect on the maturation, differentiation and proliferation of many types
of immune cells in the host (Wasser, 2011).
Together with the polysaccharide-protein complexes, glycoproteins and
polysaccharide-peptide complexes also pursue important antitumoral and
immunomodulatory activity. For example, the study of the mushroom Trametes
versicolor enabled the discovery of two very interesting compounds, a water-soluble
polysaccharide-protein complex, polysaccharide-K (PSK), commercial name Krestino,
and a polysaccharide-peptide (PSP), both obtained from the mycelium, and with an
extraordinary immunopotentiating and anticancer activity (Rowan et al., 2002). In
other mushrooms, polysaccharides with immunomodulatory properties have also been
identified, such as the polysaccharide-protein complex known as LEM, in the mycelium
of Lentinula edodes, glycoproteins with immunostimulating activity (FIPs) and a
polysaccharide-peptide complex (GPP) in Ganoderma lucidum (Rop et al., 2009).
28
Health and nutritional properties of mushrooms
2. Other bioactive compounds
Besides polysaccharides and proteins, mushrooms contain other bioactive
compounds that are classified according to their molecular weight. The compounds
with the greatest molecular weight are the lignins and lectins, among others, and
those with lowest weight are notably the triterpenes and phenolic compounds
(Lindequist et al., 2005).
Compounds with low molecular weight
Triterpenes represent one of the largest groups of bioactive compounds that are
found in medicinal mushrooms. Ganoderma lucidum is a good example since it has
more than 120 different triterpenes (Kim and Kim, 1999). It has been shown that
various triterpenes from G. lucidum are antiviral agents active against type I HIV and
against the herpes type I virus (El-Mekkawy et al., 1998; Mothana et al., 2003). Others
can inhibit cholesterol synthesis (Komoda et al., 1989) and, in addition, some are
capable of inhibiting the enzymes that participate in the conversion of angiotensin
(Morigiwa et al., 1986) or platelet aggregation (Su et al., 1999), thus being able to
reduce the risk of atherosclerosis.
Phenolic compounds, also bioactive compounds of mushrooms, are
characterised by their high antioxidant capacity. Numerous works conducted on
various species of mushroom, including G. frondosa, H. erinaceus, L. edodes and P.
ostreatus, among others, have shown that their aqueous and metanolic extracts are
rich in phenolic compounds and that they have a high antioxidant capacity in vitro
(Mau et al., 2002; Elmastas et al., 2007). Phenolic compounds have also been found
with antioxidant power in other species of mushrooms as well as those named above.
Flavoglaucin, a phenolic compound isolated from the mycelium of the mushroom
Eurotium chevalieri, is an excellent antioxidant in vegetable oils in a concentration of
0.05% (Elmastas et al., 2007). In most of these studies, a positive correlation is found
between the total phenolic content in extracts from mushrooms and its antioxidant
properties, which confirms that edible mushrooms have an important role as natural
antioxidants due to the ability of their phenolic compounds to inhibit the oxidation of
lipids.
Besides phenolic compounds, mushrooms also have other compounds with
antioxidant activity, like β-tocopherol and β-carotene.
Compounds with high molecular weight
Lectins are proteins that attach to sugars with a high specificity. Lectins derived
from mushrooms are characterised by their activities: immunomodulatory,
antiproliferative and antitumoral (El Enshasy and Hatti-Kaul, 2013). These compounds
modulate the human immune system because they stimulate the maturation of the
immune cells in vitro (Wang et al., 1996; Lin et al., 2009).
29
Health and nutritional properties of mushrooms
It has been shown that lectins also have a hypoglycaemic activity. In the study of
Ahmad et al., (1984) lectins were isolated from the Agaricus campestris and Agaricus
bisporus mushrooms and it was observed that they were able to increase the release
of insulin in islets of Langerhans extracted from rats.
http://www.mushrooms.ca
In some species of Pleurotus, lectins have been isolated that contain aminoacids
like glucose, arabinose, galactose, manose and xilose with anti-inflammatory
properties, among which species are P. japonicus (Lindequist et al., 2005), P. ostreatus
and P. cornucopiae (Yoshida et al., 1994).
Lignins are polymers present in the cellular walls of mushrooms. It has been
shown that lignins soluble in water, isolated from Lentinula edodes, have antiviral
activity since they are able to inhibit to some extent the development of HIV
(Lindequist et al., 2005).
30
Health and nutritional properties of mushrooms
HEALTH PROPERTIES OF MUSHROOMS
For thousands of years, mushrooms have been used in traditional eastern
medicine, although it has not been until the last two or three decades that studies
have begun to evolve to demonstrate the properties of their extracts in the prevention
and treatment of various diseases, including cancer, Alzheimer’s, diabetes and obesity,
etc. (Cheung, 2008). Thanks to these studies, it has been shown that the consumption
of mushrooms or their isolated bioactive compounds entails a benefit for health
(Lakhanpal and Rana, 2005).
Some of the health properties that mushrooms present and their bioactive
compounds are explained below:
1. Antioxidant
Currently, the antioxidant capacity of foods is
gaining increasing importance as a means for combating
oxidative stress. Cellular metabolism naturally produces
species that are reactive to oxygen, known as “free
radicals”. When the antioxidant mechanism is not able
to detoxify an excess of these species, the result is
oxidative stress.
Antioxidants can be endogenous, generated by
the body itself, or exogenous, which are those coming
from the diet. Increasing the intake of antioxidants helps to protect the body from free
radicals and slow down the progress of many chronic illnesses (Liu et al., 2013). There
are various types of antioxidants depending on their action mechanism: preventive,
those that inhibit the formation of free radicals; free radical sequestrant, and repair
enzymes that are responsible for repairing the damage once it has occurred.
There is a wide variety of foods rich in compounds with recognised antioxidant
activity, including mushrooms. The antioxidant potential of mushrooms, both
cultivated and wild, is today the motive for many scientific studies and publications.
The antioxidant value of mushrooms is comparable with that of foods of vegetable
origin, the compounds responsible for the antioxidant power in mushrooms being
various: selenium, phenolic compounds, ergothioneine, tocopherols, carotenoids, etc.
It has been shown that a good number of edible mushrooms could be used as natural
antioxidants for their high potential against oxidative stress (Kim et al., 2008; Liu et al.,
2012; Palacios et al., 2011; Reis et al., 2012b).
Among the phenols identified in the common mushroom are tyrosine, catechol,
phenolic acids, ρ-hydroxybenzoic acid, tr-cinnamic acid, ρ-coumaric acid and vanillic
acid (Dubost, 2007). In animals, it has been shown that the extract from Pleurotus
protects the organs of older rats against oxidative stress and the bases have been laid
to be able to prove the activity of these extracts in humans (Jayakumar et al., 2007;
Jayakumar et al., 2006). In addition, this author suggested incorporating the extract in
the diet as a nutritional supplement to increase the body’s defences against oxidative
31
Health and nutritional properties of mushrooms
stress (Jayakumar et al., 2007). In another study by the same author also with rats of
an advanced age, it was observed that an extract from P. ostreatus was increasing
gene expression for the antioxidant catalase enzyme and reducing the incidence of
protein oxidation induced by free radicals, which means that this extract seems to
protect against the appearance of disorders associated with age in those where free
radicals are implicated (Jayakumar et al., 2010).
With regard to polyphenols, the common mushroom is the one that contains the
highest level of these antioxidants. A portion of common mushrooms (85 g) contains
between 43 and 75 mg of total phenols. A positive relation has been found between
this high phenol content and the free radical sequestering ability, as these phenols are
the compounds that contribute most to the antioxidant capacity (Dubost, 2007).
In addition, the mushroom polysaccharides can boost the defence systems in
vivo against oxidative damage. The fruiting bodies of Pleurotus abalonus produce a
polysaccharide-peptide complex (F22) capable of increasing the activity and gene
expression of antioxidant enzymes and of reducing lipid peroxidation in mice with
accelerated senescence (Li et al., 2007). Pleuran, another β-1,3-D-glucan that is
extracted from Pleurotus ostreatus, improves the antioxidant status of rats, increases
the activity of the superoxide dismutase enzyme (SOD), glutathione peroxidase (GSHPX) and glutathione reductase (GRD) (Bobek and Galbavy, 2001).
Ergothioneine is a compound found in mushrooms that is an excellent
antioxidant in vivo (Dubost et al., 2007) and furthermore protects the cells against
oxidative damage (Aruoma et al., 1999). Boletus edulis is the mushroom that presents
the highest concentration of all foods (528.1 mg/kg of moist matter) (Ey et al., 2007).
Other less common mushrooms like A. bisporus show concentrations that hover
around 0.21-0.47 mg/g in dry matter (Dubost et al., 2006; Dubost et al., 2007),
although P. ostreatus (2-2.59 mg/g in dry matter) and L. edodes (1.98-2.09 mg/g in dry
matter) show higher levels. Thus, edible mushrooms contain a quantity of
ergothioneine suited to improving the antioxidant capacity of meals.
Selenium plays a very important role in the antioxidant systems of the human
body, acting as a co-factor in glutathione peroxidase, boosting the activities of αtocopherol and helping the DNA repair mechanisms. As mentioned previously,
mushrooms of the genus Boletus possess high concentrations of this compound, from
1 to 5 mg/kg in dry matter (B. edulis, B. pinicola and B. aestivalis) (Kalac, 2009). The
cultivation substrates of other mushroom species that present lower concentrations of
this mineral, like Agaricus bisporus, can be supplemented by adding sodium selenite to
increase the concentration (Spolar et al., 1999).
At CTICH, studies have been carried out on the antioxidant capacity of
mushrooms. Specifically, the antioxidant activity was determined of 10 mushroom
species that had been cultivated on La Rioja’s own substrate. The results obtained
suggested that mushrooms like Agaricus bisporus, Hypsizygus ulmarius, Agrocybe
aegerita and Pleurotus ostreatus have a high antioxidant capacity and a high
concentration of phenols (Grifoll et al., 2014).
32
Health and nutritional properties of mushrooms
Figure 19. Content of total phenols in different mushrooms cultivated in La Rioja (HU =
Hypsizygus ulmarius, AB = Agaricus bisporus, PO = Pleurotus ostreatus, AA = Agrocybe aegerita,
HE = Hericium erinaceus, PE = Pleurotus eryngii, LE = Lentinula edodes, HTg = Hypsizygus
tessulatus grey, HTb = Hypsizygus tessulatus white, PN = Pholiota nameko). Different letters
indicate significant differences between the various mushrooms (p < 0.05) (Grifoll et al., 2014).
2. Antitumoral
In most countries, cancer is the second cause of mortality in the population and
is considered as a global epidemic. It is possible to prevent almost 30% of cases of
cancer by modifying the main risk factors, such as food, tobacco, alcohol and lack of
physical exercise. According to many studies, a diet rich in fruit, vegetables, whole
grain, dietary fibre and certain micronutrients (vitamins and minerals), helps to protect
the body against certain types of tumour (Menendez and Lupu, 2006).
Mushrooms contain a series of compounds, already mentioned above, that
display anticancer activity. The consumption of mushrooms can reduce the risk of
suffering from certain tumours or prevent them. For example, in a study carried out
among Korean postmenopausal women, it was observed that the regular consumption
of mushrooms reduced the risk of breast cancer (Hong, 2008).
Epidemiological studies have shown that the habitual intake, as part of a normal
diet, of mushrooms that display anticancer activity reduces the risk of tumour
formation. The mortality levels for cancer in population groups that were eating
Agaricus blazei and Flammulina velutipes as part of their regular diet were significantly
lower than those for the rest of the world’s population (Gi-Young et al., 2005).
Consumption of the Maitake mushroom increases the activity of the auxiliary T cells
that attack cancer cells (Israilides et al., 2008) and has a positive effect on breast (Chan
et al., 2011), colon (Masuda, 2009) and prostate cancer (Fullerton, 2000). The works of
Tanaka et al., (2011) and Sliva (2003) also show that shiitake and reishi mushrooms
also have antitumoral activity in studies in vivo with animals. Some mushrooms of the
33
Health and nutritional properties of mushrooms
genus Cordyceps are capable of inhibiting the division and proliferation of cancer cells
(Das et al., 2010). The common white mushroom can also modulate the aromatase
enzyme activity and reduce the production of oestrogen in situ in postmenopausal
women, which makes it an excellent chemopreventive agent in breast cancer (Chen et
al., 2006).
Among the compounds with antitumoral activity in mushrooms, polysaccharides
seem to be the most powerful. Scientific studies show that the polysaccharides of the
common mushroom can avoid oncogenesis, through their direct antitumoral activity
against various tumours and furthermore prevent metastasis of the tumour. Its
activity is increased when it is used in conjunction with chemotherapy (Wasser, 2011).
Another example is the administration of lentinan during chemotherapy treatment,
which has been observed to increase the quality of life of patients with stomach and
colon cancer and other carcinomas, in comparison with patients who have only been
treated with chemotherapy (Hazama et al., 1995).
More polysaccharides have been studied in detail, such as schizophyllan from
Schizophyllum commune. Clinical trials on humans with this compound have
demonstrated its beneficial activity in patients with an inoperable and recurrent gastric
cancer. Other studies indicate its activity as an inhibitor in second stage cervical cancer
and advanced grades of cervical carcinoma (Hobbs, 1995; Borchers et al., 1999). Also
noteworthy are the clinical studies carried out with Ganopoly, the polysaccharide
extracted from Ganoderma lucidum, in which it was detected that symptoms related
to the cancer, such as perspiration or insomnia, improved when they were treated
with Ganopoly three times a day (dose: 1800 mg).
3. Immunomodulatory
An immunomodulatory is a substance that modifies (can increase or decrease)
the immune system’s capacity to perform one or more of its functions, such as the
production of antibodies, antigenic recognition or the secretion of inflammatory
mediators. Modulation of the immune system through its stimulation or suppression
can contribute to the maintenance of a good state of health. The use of agents that
activate the host’s defence mechanisms (immunostimulators or immunopotentiators),
would provide an additional therapeutic tool to conventional chemotherapy in
immunocompromised people.
Edible mushrooms comprise a source of compounds that “boost the host’s
defence” through their stimulatory activity on the immune system. Various
substances with an immunostimulant effect have been isolated from mycelium and
from the fruiting bodies of different mushrooms, basically polysaccharides with type βglucan structure, lectins and terpenes. These compounds stimulate different cellular
populations like macrophages, NK cells (a type of lymphocyte), neutrophils or
lymphocytes and induce the synthesis of cytokines (Chen and Seviour, 2007). Thus,
some polysaccharides or polysaccharide-protein complexes of mushrooms are able to
stimulate the non-specific immune system and perform antitumoral activity through
the stimulation of the hosts’ defence mechanisms (Rathee et al., 2012).
34
Health and nutritional properties of mushrooms
Depending on the molecular weight of the polysaccharides extracted from
mushrooms, the immunomodulatory action mechanism will be different. Low
molecular weight polysaccharides can penetrate into the cells and thus have a booster
effect on the immune system. When those with greater molecular weight cannot enter
the cell, they attach to specific receptors of the cellular membrane and propagate the
response in this way (El Enshasy and Hatti-Kaul, 2013).
Figure 20. Action mechanism of a β-glucan as modulator of the immune system (www.progalbt.com).
There are many mushroom species that have immunomodulatory activity. One
of the most representative is Ganoderma. Studies carried out with polysaccharides of
Ganoderma lucidum show that these compounds are able to stimulate the immune
system of immunodepressed mice. The authors state that these compounds could be
used as potentiators to palliate immunosupression induced through chemotherapy
(Zhu et al., 2007).
The immunomodulatory activity of Grifola frondosa must also be taken into
account since various investigations suggest that the antitumoral activity mechanism
of the grifolan polysaccharide is strongly related to immunomodulation. It has been
shown that this polysaccharide activates the macrophages in vitro to produce the
tumoral necrosis factor (TNF-α) (Ishibashi et al., 2001).
Bioactive compounds of other mushrooms like Agaricus brazei, Lentinula edodes,
Hericium erinaceus and Pleurotus ostreatus are able to induce the production of TNF-α
and increase the expression of cytokines and interleukins (IL-1β, IL-4, IL-8, IL-12), thus
activating the immune system and thereby acting as immunomodulatories (Lee et al.,
2009; El Enshasy and Hatti-Kaul, 2013).
35
Health and nutritional properties of mushrooms
4. Anti-Obesity and Antihyperlipidemic Properties
Obesity is a serious public health problem that has reached epidemic proportions
in many developed countries. In fact, the World Health Organisation (WHO) has
defined it as the "Epidemic of the 21st Century". Increased body fat accompanying
obesity may be due to a change in the number and/or size of adipocytes, the most
abundant adipose tissue cells. Excess energy intake is stored inside adipocytes as
triglycerides and when the body needs energy, these triglycerides are hydrolysed into
free fatty acids and glycerol in a process called lipolysis
In recent years several studies have shown the
beneficial effects of certain mushroom varieties in the
prevention of obesity and associated disorders
(Handayani et al., 2014; Kanagasabapathy et al., 2013;
Schneider et al., 2011). Jeong and colleagues (2010)
found that oral administration of Agaricus bisporus to
rats fed a hypercholesterolemic diet reduces both plasma triglycerides and glucose
levels, so it follows that this mushroom is beneficial in lipid metabolism, which could
be very advantageous in the treatment of obesity.
It has been shown that the Pleurotus species prevents weight gain and
hyperlipidemia in C57BL/6J mice fed a high-fat diet, as it is capable of inducing lipolysis
and inhibiting adipocyte differentiation. For example, β-glucans from the Pleurotus
sajor-caju mushroom prevent the development of obesity and oxidative stress in mice
fed a high-fat diet (Kanagasabapathy et al., 2013). Previous studies carried out in the
CTICH in collaboration with the CIBIR showed that applying a Pleurotus ostreatus
extract treatment in cell cultures of subcutaneous adipocytes increased lipolysis, this
could be a mechanism with which the extracts of this mushroom are able to decrease
the adipocyte size, and therefore, the adipose tissue (Aguilera-Lopez et al., 2013).
Additionally, treatment with P. ostreatus decreased leptin levels in subcutaneous
adipocytes, a hormone that is normally found at higher levels in obesity. Cumulatively,
all this data suggests that the oyster mushroom offers potential protective effects for
obesity and its associated disorders.
Continuing with the lipid lowering effects of the Pleurotus species, it has been
found that polysaccharides of the Pleurotus eryngii are capable of lowering the level
of blood lipids in mice fed a high-fat diet (Chen et al., 2012). It has also been shown to
be more effective in inhibiting the accumulation of lipids than other polysaccharides
extracted from mushrooms such as Hericium erinaceus, Ganoderma lucidum, Lentinula
edodes or Pleurotus ostreatus (Chen et al., 2013).
Shiitake mushrooms are also known for their beneficial effects in relation to
obesity, since they may help reduce the level of lipids in plasma and prevent weight
gain. Administration of this mushroom to rats with a high-fat diet led to a 55%
reduction of plasma cholesterol levels and lower fat accumulation, compared to
another group of rats that consumed only a high-fat diet without shiitake mushrooms
(Handayani et al., 2011). A later study by the same author correlated a β-glucan of
shiitake mushrooms with a lower level of blood triglycerides, reduction of fat
36
Health and nutritional properties of mushrooms
accumulation, lower body weight gain and decreased fat accumulation in the liver
(Handayani et al ., 2014).
The PNPS-1 polysaccharide of Pholiota nameko also has a significant
hypolipidemic effect, since it has been confirmed that it can decrease both serum and
liver lipid levels. Moreover, it has also been found that this polysaccharide reduced
weight gain and visceral fat accumulation, which is very interesting since the increase
of visceral fat is one of the primary causes of metabolic syndrome (Li et al., 2010).
5. Cholesterol-lowering properties
Mushrooms and their extracts could be considered as a new source of
compounds with hypocholesterolemic effects, as they are rich in ergosterol
derivatives, β-glucans and inhibitors of the HMG-CoA reductase enzyme. There are
different studies, some of which are already mentioned above, which describe the
beneficial effects of mushrooms on blood cholesterol levels (Gil-Ramirez et al, 2011;
Gil-Ramirez et al, 2013a).
Among various species of mushrooms, the Pleurotus species stands out as a
potential regulator of cholesterol metabolism. These mushrooms are able to
synthesise lovastatin, a highly hypocholesterolemic statin that inhibits the HMG-CoA
reductase enzyme, a key enzyme in the regulation of cholesterol biosynthesis in the
liver (Gil-Ramirez et al., 2013b). Lovastatin also increases the activity of LDL cholesterol
receptors. Moreover, some beta-glucans of Pleurotus are capable of binding to bile
acids, reducing the formation of micelles and cholesterol absorption (Fidge, 1993;
Bobek and Galbavy, 1999).
Figure 21. Effect of mushrooms on cholesterol metabolism (Guillamón et al., 2010).
In the case of mushrooms, their cholesterol-lowering effect has been described
in many studies, such as the study by Jeong et al. (2010), which supplemented a highfat diet with mushrooms for rats and found that blood cholesterol decreased in these
animals compared to controls without mushrooms. The same effect was observed
years before in another study when this mushroom was added to a fibre-rich diet. It
37
Health and nutritional properties of mushrooms
also showed that the cholesterol level was lower when the animals consumed the diet
with mushrooms (Fukushima et al., 2000) .m
Mushrooms
Agaricus bisporus
Auricularia auricula
Lentinus edodes
Hypocholesterolemic properties
↓ LDL Cholesterol ↓ Total serum cholesterol
↓ HDL Cholesterol
↑ Hepa`c LDL receptor
↓ Faay deposits ↓ Triglycerides in liver
↓ LDL Cholesterol ↓ Total serum cholesterol
↓ Cholesterol level
↓ Plasma phospholipids
Modification of hepatic phospholipid metabolism
Pleurotus citrinopileatus ↓ Total lipids ↓ Total cholesterol
↓ Triglycerides in liver and plasma
↑ Excre`on of bile acids
HMG-CoA reductase inhibitors
Pleurotus ostreatus
↓ VLDL Cholesterol ↓ LDL Cholesterol
↓ Total serum cholesterol
↓ Plasma triglycerides
↓ Blood pressure
↓ An`oxidant ac`vity of glutathione peroxidase
HMG-CoA reductase inhibitors
Table 4. Hypocholesterolemic properties of mushrooms (Guillamón et al., 2010).
Compounds obtained from Ganoderma lucidum such as ganoderic and
triterpene acids, have been shown to posses hypocholesterolemic properties, as well
as polysaccharides from the Auricularia auricula (Hobbs, 1995; Rowan et al., 2002).
Hypocholesterolemic properties are also attributed to the shiitake mushroom,
in particular the effect is due to eritadenine, this compound exerts its effect by
reducing cholesterol secretion from the liver into the bloodstream and/or through
increased distribution of cholesterol from the plasma to the peripheral tissues
(Shimada et al., 2003). Additionally, it has been shown that supplementation with
shiitake mushrooms and eritadenine compound inhibits the development of
hypercholesterolemia resulting from a high-fat diet (Yang et al., 2013).
38
Health and nutritional properties of mushrooms
6. Antidiabetic Properties
According to the WHO, diabetes is a chronic disease that occurs when the
pancreas does not produce enough insulin or when the body does not effectively use
the insulin it produces. Insulin is a hormone that regulates blood sugar. The effect of
uncontrolled diabetes is hyperglycemia (excess blood sugar), which gradually causes
serious damage to many organs and systems, especially to nerves and blood vessels.
A great number of studies have been carried out regarding the role of
mushrooms in the dietary management of diabetes, which conclude that mushrooms
are the ideal food for the prevention of hyperglycemia due to their high content of
fibre and protein and for the bioactive compounds they posses, such as
polysaccharides and lectins (Alarcon-Aguilara et al., 1998; Horio et al., 2001; Kiho et al.,
2002).
Glucans extracted from the Agaricus blazei reduce the level of glucose,
triglycerides and blood cholesterol simulating the effect of insulin. The study was
conducted on rats with induced diabetes who were fed daily with sweet potato
(Ipomoea batatas) and A. blazei. Researchers observed decreased plasma glucose,
when on an empty stomach, and glycated hemoglobin, as well as a decrease in body
weight loss due to the diabetes (Mascaro et al., 2014).
In another study, in this case with the Agaricus sylvaticus, it showed a beneficial
effect in controlling type I diabetes by reducing blood glucose levels, cholesterol and
triglycerides. Additionally, it improved pancreatic function by increasing the number of
cells of the islets of Langerhans with good results in the symptoms of the disease
(Mascaro et al., 2014).
Experimental studies with the Pleurotus species show very good results regarding
the hypoglycemic effect of these mushrooms. Oral administration of P. ostreatus to
rats reduced blood sugar levels in both insulin-dependent animals and those who
were not dependent on insulin (Chorváthová et al., 1993). Subsequent studies, in vitro,
in which subcutaneous adipocytes were treated with this mushroom showed
significant insulin-sensitizing effects by significantly increasing glucose intake while
releasing glycerol (Aguilera-Lopez et al., 2013). Introducing P. eryngii at 7% in the diet
also led to an improvement in insulin sensitivity as well as a decrease in glucose and
cholesterol levels in rats with induced diabetes (Kim et al., 2010). The aqueous extract
of P. pulmonarius and P. citrinopileatus also revealed a powerful antidiabetic effect,
lowering glucose levels of diabetic rats (Badole et al, 2008; Hu et al., 2006).
There is not only evidence of hypoglycemic activity in the Pleurotus species from
animal testing, but studies on humans have also been carried out. Agrawal et al. (2010)
an experimental study on 120 diabetic patients obtained the following results: the
consumption of Pleurotus sajor-caju significantly reduced blood glucose levels on an
empty stomach (P<0.005), and blood cholesterol (P<0.05) and HbA1c (glycosylated
hemoglobin) (P<0.05).
Administration of Grifola frondosa at 20% in the diet of rats with induced
diabetes resulted in increased excretion of insulin and decreased levels of blood
glucose (Kurushima et al., 2000).
39
Health and nutritional properties of mushrooms
A polysaccharide of Ganoderma lucidum, Ganopoly, is also known for its
hypoglycemic effect. In a study of 71 type II diabetic patients treated with Ganopoly, it
was observed that postprandial glucose levels decreased significantly compared to the
group not taking the extract (Gao et al., 2004).
7. Antihypertensive Properties
Arterial hypertension is a chronic disease characterized by a continued increase
in arterial blood pressure. It is associated with significantly high morbidity and
mortality rates, thus considered one of the most serious public health problems,
especially in developed countries, affecting nearly one billion people worldwide.
Various antihypertensive compounds have been
identified in vegetables and other foods. Many
antihypertensives are inhibitors of the angiotensin
converting enzyme (ACE inhibitors), which inhibit a
series of reactions (renin angiotensin aldosterone
system) that regulate blood pressure. ACE inhibitors
have been detected in various mushrooms: Grifola
frondosa (Choi et al., 2001), Ganoderma lucidum
(Morigiwa et al., 1986) or Pleurotus cornucopiae (Jang
et al., 2011), among others.
Mushrooms
Agrocybe sp.
www.powerofmushroom.com
ACE inhibitor activity
IC50 (mg/ml)
0.890 ± 0.046
Auricularia auricula-judae
0.510 ± 0.018
Ganoderma lucidum
0.050 ± 0.009
Hericium erinaceus
0.580 ± 0.023
Pleurotus cystidiosus
0.054 ± 0.002
Pleurotus eryngii
0.067 ± 0.026
Pleurotus flabellatus
0.058 ± 0.002
Pleurotus florida
0.050 ± 0.013
Pleurotus sajor-caju
0.056 ± 0.012
Schizophyllum commune
0.320 ± 0.007
Volvariella volvacea
0.760 ± 0.023
Table 5. ACE inhibitor activity of various mushrooms. IC50 values are interpolated from the
dose-response curve for ACE inhibitors for each mushroom species (Abdullah et al., 2012).
The following describes certain studies that show antihypertensive effects of
mushrooms. Aqueous extracts of the Hypsizygus marmoreus mushroom showed a
clear antihypertensive effect with ACE inhibitor activity in a study of rats with
hypertension (Kang et al., 2013). Another mushroom, Maitake, with which several
40
Health and nutritional properties of mushrooms
studies have been carried out, has also shown favourable effects for hypertension.
Talpur et al. (2002) also showed potential antihypertensive effects of the Maitake
mushroom in a study with hypertensive rats. Years earlier, Kabir and Kimura (1989)
carried out another study feeding hypertensive rats with Maitake mushrooms for 8
weeks and found that blood pressure decreased significantly.
Abdullah et al. (2012) analysed the potential of ACE inhibitors in several species
of mushrooms, the results are shown in Table 5, with the Ganoderma lucidum
mushroom showing more antihypertensive effects.
In addition to the many beneficial properties already described for the Pleurotus
species, these mushroom species also have antihypertensive effects through ACE
inhibitors. Oral administration of P. nebrodensis and P. cornucopiae extracts reduced
blood pressure in hypertensive rats in an experimental study (Miyazawa et al, 2008;.
Hagiwara et al., 2005).
8. Hepatoprotective Properties
The liver is one of the most complex and important organs in our body. It
performs singular vital functions such as the synthesis of plasma proteins, vitamin and
glycogen storage, etc. Additionally, it is in charge of removing substances from the
blood that may be harmful to the body, transforming them into other harmless
substances. The liver is involved in the metabolism of proteins, fats and carbohydrates,
it maintains a stable level of blood glucose, storing it when in high quantity in the
blood (gluconeogenesis) and releasing it (glycogenolysis) as needed.
The role of mushrooms and their bioactive compounds in liver functions has
been undergoing research for several years. It has been found that these compounds
can repair liver damage from toxins, protect against toxic agents, regenerate
damaged hepatocytes, reduce inflammation, etc.
Most studies on the hepatoprotective role of mushrooms have been conducted
with Ganoderma lucidum or extracts. Isolated Sterols from Ganoderma lucidum exert a
powerful anti-inflammatory effect on butyl hydroperoxide or carbon tetrachloride
induced liver cell line damage (Ha do et al, 2013; Sudheesh et al, 2012.). It has also
been found that G. lucidum, through an antioxidant mechanism, may protect liver cells
poisoned with alpha-amanitin (one of the most potent liver toxins, obtained from the
Amanita mushroom family) (Wu et al., 2013). Another study found that pure spore
powder of the Ganoderma lucidum is particularly beneficial for liver cell damage
caused by cadmium poisoning (Jin et al., 2013). It has even been shown that G.
lucidum acts against hepatitis B. A clinical study was carried out in which treatment
using polysaccharides of this mushroom reduced hepatitis B in HIV patients after 12
weeks (Gao et al., 2002).
The hepatoprotective effect has also been attributed to the Pleurotus species.
There are studies using animals which confirm the protective effect of P. ostreatus
(Jayakumar et al., 2006) and P. florida (Arunavadas and Umadevi, 2008) against
carbon tetrachloride induced liver damage. Additionally, P. ostreatus, P. sajor-caju
and P. florida can protect the liver from lipid peroxidation according to studies carried
41
Health and nutritional properties of mushrooms
out on liver tissue samples in hypercholesterolemic conditions (Hossain et al, 2003;.
Alam et al, 2009). In another study with an aqueous extract of P. eryngii, rich in
polysaccharides, an increase in the activity of antioxidant enzymes and lower
concentration of free radicals in the damaged liver was observed (Chen et al., 2012).
Based on these studies, it follows that the potential of Pleurotus mushrooms against
liver damage is due to its antioxidant effect.
Finally, it has also been found that the polysaccharides of the Hericium erinaceus
mushroom possess strong antioxidant effects in vitro and a power hepatoprotective
effect in vivo. The authors suggest that these polysaccharides may be used as
antioxidant supplements in the prevention of liver diseases (Zhang et al., 2012).
9. Antiallergenic Properties
An allergy is a hypersensitivity to a particle or substance, which, if inhaled,
ingested or touched, produces certain characteristic symptoms. It is a type of
exaggerated immunological response to a non-pathogenic stimulus for the majority of
the population. Its clinical manifestations are diverse, since they depend on the
causative agent and the affected organ. Currently, more than one third of the world
population suffers from some disease of allergic origin.
Extracts of certain mushrooms are able to stimulate the immune system, which
might be interesting for the treatment of allergies. As is the case of aqueous extracts
obtained from H. marmoreus, F. velutipes, P. nameko and P. eryngii, which have
shown significant antiallergic effects in studies carried out on allergy induced mice
(Sano et al., 2002).
Certain compounds extracted from Ganoderma lucidum (ganoderic acids C and
D) can inhibit histamine release from rat mast cells, reducing allergic reaction (Kohda
et al., 1985; Tasaka et al., 1988).
The isolated β-glucan of the Pleurotus ostreatus, Pleuran, has also been studied
in relation to the antiallergenic effect of mushrooms. The prevalence of atopy in a
group of children with recurrent respiratory tract infection and antiallergenic effect of
Pleuran on markers of inflammation was researched. Active Pleuran treatment showed
a potential antiallergic effect (Jesenak et al., 2014).
Most of the published research uses extracts or compounds derived from
mushrooms, but there are very few publications that administer the entire mushroom,
such as the case studying Tricholoma populinum, which observed that consumption of
this mushroom led to a disappearance of the allergy symptoms in patients with hives
(Kreisel et al., 1990).
10. Antimicrobial Properties
Natural antimicrobial compounds have the ability to inhibit the growth of
microorganisms and are synthesized by some types of plants and vegetables.
Mushrooms and fungi also produce antibacterial and antifungal substances to fend off
other species, which confer antimicrobial properties against bacteria, yeasts and other
42
Health and nutritional properties of mushrooms
fungi. Different antimicrobial compounds have been isolated from the mushrooms
(Rathee et al., 2012). Many of the secondary metabolites secreted by mushrooms
and fungi are used to fight bacterial and fungal infections and prolong the shelf life
of other food products.
One of the most studied mushrooms, in terms of its antimicrobial properties, is
Lentinula edodes. Extracts isolated from this mushroom are shown to be active against
some bacteria such as Actinomyces spp., Lactobacillus spp. and Pophyromonas spp.
(Hirasawa et al., 1999). It seems that oxalic acid is one of the agents responsible for the
antimicrobial effect of L. edodes against Staphylococcus aureus and other bacteria
(Bender et al., 2003). Additionally, a protein called lentina has been extracted from the
fruiting bodies of L. edodes with significant antifungal effect (Ngai and Ng, 2003). This
protein with a molecular weight of 27.5 kDa inhibits mycelium growth in a large
number of fungi, including Physalospora piricola, Botrytis cinerea and Hycosphaerella
arachidicola.
Studies carried out with Ganoderma lucidum and other Ganoderma species show
that these mushrooms produce several antimicrobial compounds that are capable of
inhibiting growth of gram positive and/or gram negative bacteria. Aqueous extracts of
G. lucidum fruiting bodies are capable of inhibiting growth of 15 types of gram positive
and gram negative bacteria, especially of Micrococcus luteus (Yoon et al., 1994). It has
also been found that extracts of G. pfeifferi inhibit the growth of microorganisms
responsible for skin diseases (Pityrosporum ovale, Staphylococcus epidermidis,
Propionibacterium acnes) (Mothana et al., 2000).
Pleurotus mushrooms, extracts and bioactive compounds also have notable
antimicrobial activity. Some volatile compounds extracted from the fruiting body of
Pleurotus ostreatus had strong antibacterial effect against B. cereus, B. subtilis, E. coli
and S. typhimurium (Beltran-Garcia et al., 1997). Additionally, from this fungus was
extracted a peptide with antifungal capability, called pleurostrin, which inhibits
mycelial growth of the fungi Fusarium oxyporum, Mucosphaerella arachidicola and
Phycalospora piricola (Chu et al., 2005). From the Pleurotus eryngii mushroom, another
antifungal peptide, called erygin, which inhibits growth of Fusarium oxyporum and
Mycosphaerella arachidicola was isolated (Wang and Ng, 2004).
43
Health and nutritional properties of mushrooms
Although there have been few studies on wild mushrooms regarding
antimicrobial effects and corresponding bioactive compounds, some studies found
show that a peptide produced by the Boletus species exhibited antimicrobial effects
against gram positive bacteria (Lee et al., 1999; Barros et al., 2007b). Isobaric acids and
10-hydroxy-8-decanoic obtained from Cantharellus cibarius have also shown some
antimicrobial effects (Anke et al., 1996).
11. Antiviral Properties
Viral diseases cannot be treated with common antibiotics, rather specific drugs
against viruses that cause these infections are required. Antiviral activity in
mushrooms is described for both entire mushrooms as well as and for bioactive
compounds extracted therefrom. In the case of mushrooms, antiviral action can occur
directly by inhibiting certain viral enzymes, through the synthesis of some nucleic acids
of the virus or by absorption and replication of the virus in the cells; and also indirectly,
by stimulating the immune system (Brandt and Piraino, 2000). The type of action
against the virus is determined by the size of the fungi molecules.
Among the smaller molecules isolated from different mushrooms are several
triterpenes isolated from Ganoderma lucidum, ganoderic acid for example, which has
demonstrated significant antiviral activity against HIV type 1 (HIV-1) (El- Mekkawy et
al., 1998). In the same way, the ganodermadiol, licidadiol and aplanoxídico acid, from
Ganoderma pfeifferi, posses antiviral effects against the type A influenza virus.
Additionally, ganodermadiol also inhibits replication of the herpes simplex type 1 virus
(Mothana et al. , 2003).
As for the antiviral activity of more complex molecules, it has been shown that
water soluble lignins, isolated from Fuscoporia obliqua are active against HIV (Ichimura
et al., 1998). Also, water soluble lignins isolated from L. edodes and a polysaccharide
called lentinan are capable of inhibiting the development of HIV to some extent
(Lindequist et al., 2005). In this sense, a polysaccharide isolated from Agaricus
brasiliensis has been shown to inhibit infection by the poliovirus type 1 (Faccin et al.,
2007). Furthermore, proteins bound to polysaccharides isolated from Ganoderma
lucidum are also capable of delaying development of the herpes viruses, as it inhibits
the binding and subsequent penetration of the virus into cells (Eo et al., 2000).
Also noteworthy is the antiviral effect of the Pleurotus species, scientific studies
show that P. ostreatus, an enzyme isolated from this mushroom, is capable of
inhibiting the entry of the hepatitis C virus into blood cells, thus preventing replication
(El-Fakharany et al., 2010). Another enzyme, extracted this time from P. cornucopiae,
can reduce the activity of the HIV type 1 virus (Wong et al., 2010). Other Pleurotus
species, such as P. sajor-caju and P. citrinopileatus, have also shown to have a strong
antiviral effect against the HIV virus (Kidukuli et al., 2010). Additionally,
polysaccharides obtained from the sclera of P. tuber-regium show antiviral effects
against the herpes simplex type 1 and type 2 viruses (Zhang et al., 2004).
44
Health and nutritional properties of mushrooms
12. Role of mushrooms in neurodegenerative diseases
Neurodegenerative diseases, particularly Alzheimer's, are diseases related to
ageing and increasingly affect the population over 65 years of age. The number of
cases increases every year worldwide; according to the WHO, 0.5% of the world
population suffers from some form of dementia.
Among the species of mushrooms known for their biological effects related to
the nervous system and brain health are: Sarcodon scabrosus, Ganoderma lucidum,
Grifola frondosa and Hericium erinaceus (Sabaratnam et al., 2013). Ganoderma
lucidum contains neuroactive compounds that can induce neural differentiation and
prevent apoptosis of NGF-dependent neurons (Transforming growth factor) (Cheung et
al., 2000). However, up until now, the mushroom that has more effect against
neurodegenerative diseases and has received more attention from the scientific
community is Hericium erinaceus (common name: Lion's Mane).
One of the functions of H. erinaceus for
the nervous system is that it can regulate the
growth and development of neurons. It has
been shown that exopolysaccharides of
mycelium of H. erinaceus enhance growth of
adrenal nerve cells of rats and neurite
extension of PC12 cells (Park et al. 2002; Mori
et al., 2008).
Another study by Kolotushkina et al.
(2003) found that extracts of this mushroom
promote the development of cerebellar cells and regulates the process of myelination
in vitro. In line with these results, Moldavan et al. (2007) reported that H. erinaceus
improved the process of myelination of mature myofibers and that it could also exert
neurotrophic action. This mushroom is even involved in the expression of certain
genes and proteins that can promote regeneration of axons and reinnervation of
motor end plates (Jiang et al., 2014).
In Alzheimer's there is a progressive loss of neural function. Studies that have
been carried out to date show that H. erinaceus relieves mild cognitive impairment
resulting from Alzheimer's (Mori et al., 2009) as well as some symptoms associated
with the disease, for example, it improves sleep quality and ameliorates depression
(Nagano et al., 2010). In order to examine the effectiveness of oral administration of H.
erinaceus, a study was conducted in 2009 with Japanese men and women, aged 50 to
80 years, diagnosed with mild cognitive impairment, demonstrating that subjects of
the group that took H. erinaceus (3 times a day for 16 weeks) improved cognitive
function compared to the control group (Mori et al., 2009).
45
Health and nutritional properties of mushrooms
CONCLUSIONS
Mushrooms are a food with valuable nutritional properties. Being low
in calories and a good source of fibre, they are ideal for daily consumption
and weight-loss diets. Mushrooms are also a good choice for low-salt diets
due to their low sodium content. They also have an aroma and taste,
which is highly valued by consumers.
Mushrooms are naturally very low in fat. Of the total lipid content,
about 80% are unsaturated fatty acids; commonly referred to as "good
fat" and contain no cholesterol. This makes mushrooms a highly
recommended food to prevent cardiovascular risk.
Mushrooms are considered a nutritious and healthy food, rich in
minerals and vitamins. They stand out as being an important source of B
vitamins, especially B2 and B3, and vitamin D precursors, such as
ergosterol, which promotes absorption of calcium and phosphorus. They
also contain essential minerals for the proper functioning of our body,
mainly selenium, phosphorus and potassium.
Numerous studies being carried out today on the presence of
bioactive compounds in mushrooms provide scientific evidence to what is
already known and applied in traditional oriental medicine, where
mushrooms are used in the treatment of many diseases. Mushrooms and
their bioactive compounds are currently considered a potential tool in the
maintenance and promotion of health, longevity and quality of life.
Their therapeutic implications are enormous. As reflected throughout
this report, they have significant health properties that make them
potential therapeutic agents for diseases such as cancer, Alzheimer's and
cardiovascular diseases. Mushrooms are also used for the prevention of
diseases such as atherosclerosis and diabetes due to their ability to reduce
cholesterol and blood glucose and also due to their high antioxidant
content.
In conclusion, mushrooms are an ideal food to be included in our
daily diet due to their nutritional and health properties, which improve
health and facilitate disease prevention.
46
Health and nutritional properties of mushrooms
BIBLIOGRAPHIC REFERENCES
Abdullah N., Ismail S.M., Aminudin N., Shuib A.S., Lau B.F. (2012) Evaluation of selected
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Páginas web consultadas para la elaboración de este informe
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http://www.progal-bt.com/usuario/anti-cancer-activities-of-ganoderma-lucidum-activeingredients-and-pathways.pdf
http://www.magrama.gob.es/es/alimentacion/temas/consumo-y-comercializacion-ydistribucion-alimentaria/panel-de-consumo-alimentario/base-de-datos-de-consumo-enhogares/resultado.asp
59
5 a day
The 5 a Day programme, an international movement that
promotes consumption of fruit and vegetables, is active in more
than 40 countries across 5 continents. Its name is based on the
minimum daily serving of fruit and vegetables recommended by the
scientific and medical communities for a healthy diet.
All fruit and vegetables, including fresh and packaged
mushrooms, count in achieving this objective (www.5aldia.org).
Mushrooms are a healthy, nutritious and tasty food; a perfect way
for children to eat one of the five daily servings of fruit and
vegetables.
Tips and tricks
In the store
Cultivated mushrooms can be found in the supermarket year-round.
Fresh mushrooms should be firm with a dry surface and display
their characteristic colour.
At home
Mushrooms are perishable products; it is recommended to consume them within a
few
days after purchase. Always store in the refrigerator.
They should be kept in an open container or bag to prevent condensation
and increase their shelf life.
Cleaning
Mushrooms should not be washed or left to soak. Clean with a damp kitchen
cloth. If they´re extremely dirty, rinse with water and dry quickly with a
paper towel to remove moisture.
In the kitchen
When eating uncooked mushrooms, for example in a salad or carpaccio, it
is recommended to heat them for about 10 seconds in the microwave, oven or
grill. Mushrooms are very easy to prepare and you can make delicious recipes
in just a few minutes.
Mushrooms:
healthy, nutritious and tasty food