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Pickling is one of the methods for preserving food. However, this term may refer to both types of products, that is, to those subjected to lactic acid fermentation and to marinated ones (acidified) that are usually produced by the addition of acetic acid. Various raw materials are subjected to lactic acid fermentation (vegetable and animal origin), which yields food products with high nutritional and dietary value. In many regions of the world, the process of lactic fermentation is also traditionally used to preserve fruiting bodies of edible mushrooms. Mushrooms are appreciated for their organoleptic qualities as well as the presence of many different bioactive substances exhibiting healing and health‐promoting properties. This article reviews the literature related to the use of lactic fermentation in the process of mushroom preservation. Particular attention has been paid to the aspects of the technological process and its impact on the quality and suitability of the final products. Moreover, research results concerning the influence of lactic fermentation on chemical and physical changes in fruiting bodies of edible fungi are also presented.
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Lactic Acid Fermentation of Edible Mushrooms:
Tradition, Technology, Current State of Research:
A Review
Ewa Jabło´
nska-Ry´
s, Katarzyna Skrzypczak , Aneta Sławi´
nska , Wojciech Radzki , and Waldemar Gustaw
Abstract: Pickling is one of the methods for preserving food. However, this term may refer to both types of products,
that is, to those subjected to lactic acid fermentation and to marinated ones (acidified) that are usually produced by the
addition of acetic acid. Various raw materials are subjected to lactic acid fermentation (vegetable and animal origin),
which yields food products with high nutritional and dietary value. In many regions of the world, the process of lactic
fermentation is also traditionally used to preserve fruiting bodies of edible mushrooms. Mushrooms are appreciated
for their organoleptic qualities as well as the presence of many different bioactive substances exhibiting healing and
health-promoting properties. This article reviews the literature related to the use of lactic fermentation in the process of
mushroom preservation. Particular attention has been paid to the aspects of the technological process and its impact on
the quality and suitability of the final products. Moreover, research results concerning the influence of lactic fermentation
on chemical and physical changes in fruiting bodies of edible fungi are also presented.
Keywords: edible mushrooms, lactic acid fermentation, fermented mushrooms
Introduction
Macrofungi constitute a group of approximately 14,000 species
(Kirk, Cannon, David, & Stalpers, 2008). Due to their culinary im-
portance, an informal group—edible mushrooms, which includes
at least 1,000 to 2,500 species of macrofungi can be distinguished
(Boa, 2004; Chang, 1999). As reported by Chang and Miles (2008)
and Erg¨
on¨
ul, Akata, Kalyoncu, and Erg¨
on¨
ul (2013), only about 25
species are widely accepted as food, some of which are grown for
commercial purposes. The centuries-old tradition of cultivation
of edible mushrooms originates from China (Boa, 2004; Zhang,
Venkitasamy, Pan, & Wang, 2013). Also, this country is nowadays
considered as the main producer of cultivated edible mushrooms
(Royse, Baars, & Tan, 2017). Nearly 100 species of mushrooms
can be grown (Boa, 2004); however, 85% of current world mush-
room production is the cultivation of 5 species: Lentinula (22%),
Pleurotus (19%), Auricularia (18%), Agaricus (15%), and Flammulina
(11%) (Royse et al., 2017).
The concept of inclusion of mushrooms as a separate kingdom
appeared in the middle of the last century. Since then, the sys-
tematics of fungi has been transforming due to the occurrence of
new information regarding their phylogenesis and species affinity.
However, edible mushrooms are still perceived as plants by average
CRF3-2018-0229 Submitted 10/5/2018, Accepted 12/22/2018. Authors are
with the Dept. of Plant Food Technology and Gastronomy, Dept. of Fruits, Veg-
etables and Mushrooms Technology, Univ. of Life Science in Lublin, Skromna
8, 20–704, Lublin, Poland. Direct inquiries to author Jabło´
nska-Ry´
s (E-mail:
ewa.jablonska-rys@up.lublin.pl).
consumers (Feeney, Miller, & Roupas, 2014). In many of the food
grouping systems, mushrooms are often classified into vegetables
due to their culinary usage, but their umami flavor makes them
also a suitable substitute for meat. Mushrooms that are used in
popular dishes as a partial substitute for ground beef enhance the
attractiveness of the products through improvement of flavor as
well as texture and thereby increase consumer attention to such
dishes (Feeney et al., 2014). Mushrooms also provide significant
amounts of iron, while the content of bioavailable proteins con-
tained in the dry mass of fruiting bodies is greater than that in
most fruits and vegetables. Moreover, fungal proteins contain all
exogenous amino acids; thus, mushrooms are often referred to as
the ‘meat of the forest’ (Rajewska & Bałasi´
nska, 2004; Siwulski,
Sobieralski, & Sas-Golak, 2014) or the ‘meat of the poor’ due to
the possibility of obtaining them from the natural environment
(Dimitrijevic et al., 2018).
Owing to their attractive sensory features, mushrooms have been
used in many regions of the world for ages. They are particularly
popular in the Slavic countries of Europe and the Far East (mainly
China). They are also highly appreciated as a source of food in the
countries of Latin America and central and southern Africa (Boa,
2004). However, in some nations (including Anglo-Saxon regions)
considered as mycophobic countries, inhabitants exhibit great fear
and reluctance to consume mushrooms derived from their natural
environment (Łuczaj & Nieroda, 2011). The terms “mycophilia”
and “mycophobia” appeared at the end of the 19th century and
are commonly used to describe the relative attitudes of individ-
uals and communities to mushrooms (Boa, 2004; Hawksworth,
1996; Peintner et al., 2013). An important indicator of the public
C2019 Institute of Food Technologists®
doi: 10.1111/1541-4337.12425 Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 1
Lacto-fermented edible mushrooms . . .
attitude to mushrooms is connected with the presence of laws and
regulations in certain countries regarding collection and trade of
wild mushrooms (Peintner et al., 2013).
Mushrooms are eaten in a processed form obtained after the
following processing methods: drying, marinating, sterilizing,
and freezing. Mushrooms can also be used as a fresh ingredient
in soups, sauces, salads, stuffings, and meat dishes (Berna´
s,
Jaworska, & Kmiecik, 2006; Berna´
s, Jaworska, & Lisiewska, 2006;
Diamantopoulou & Philippoussis, 2015). Popular products, for
example, fried, canned, and frozen mushrooms, as well as the
innovative and unconventional mushroom processing techniques
are the subject of many scientific articles. There are many studies
conducted by various authors analyzing the impact of these
processing methods on the basic quality parameters and the
content of nutrients and various biologically active compounds,
which are abundant in mushroom raw material (Arumuganathan,
Rai, Chandrasekar, & Hemakar, 2004; Barros, Baptista, Correia,
S´
a Morais, & Ferreira, 2007; Berna´
s & Jaworska, 2007; Berna´
s
& Jaworska, 2012; C¸ aglarlrmak, ¨
Unal, & ¨
Otles, 2001; Muyanja,
Kyambadde, & Namugumya, 2014; Zhou et al., 2017).
In many regions of the world, the lactic fermentation process is
traditionally used to preserve the fruiting bodies of wild-growing
and cultivated edible fungi.
Biological approaches to food preservation are one of the oldest
processing methods that have been investigated intensively in the
case of other raw materials (for example, fruit, vegetables). Lactic
fermentation facilitates preservation of food products, renders
foods resistant to microbial spoilage, provides food products with
new attractive sensory traits, and enhances the health-promoting
properties of the product through enrichment thereof with
metabolites of lactic bacteria and the presence of the viable
beneficial microflora (Hutkins, 2006; Rhee, Lee, & Lee, 2011;
Steinkraus, 2002). Additionally, lactic fermentation is regarded to
be a widely available and cheap method (Holzapfel, 2002). There
are not many investigations of lactic fermentation of the fruiting
bodies of edible mushrooms; therefore, the current knowledge
in this field undoubtedly needs to be systematized and areas of
future research should be indicated. Review studies are a good
and accessible source of knowledge not only for researchers but
also for consumers and food producers. Therefore, in this article,
the process of lactic fermentation of edible mushrooms and its
impact on the quality, durability, and physicochemical properties
of the final products are discussed in detail.
Lactic Acid Fermentation as a Method of Food
Preservation
Presumably, fermented food appeared early among the first
processed foods consumed by people. Fermentation was an
inevitable process occurring in leftover and unprotected or
insufficiently protected food. Probably, in this way, mankind
learned about the taste of sour milk, wine made from fermented
fruits, and also pickled vegetables which plausibly fermented as
a result of insufficient salinity. Salting was a common method
of preserving food of both vegetable and animal origin. Salting
vegetables has been practiced for thousands of years, mainly in
Europe, the Middle East, and Asia (Hutkins, 2006). When the
concentration of salt was insufficient, appropriate conditions were
created for the existence and development of lactic acid bacteria.
The lactic acid resulting from the fermentation showed additional
preservative properties, at the same time significantly changing the
taste and odor of the obtained products (Hutkins, 2006). This new
type of food soon gained acceptance and probably gave birth to
the biological method of stabilization, that is, lactic fermentation,
which was perfected over the centuries. Fermented products are
highly popular in Asian and African countries, where they are the
basic ingredients of the daily diet and lactic fermentation is the
simplest and often the only method for preservation of fruits and
vegetables (Holzapfel, 2002; Rhee et al., 2011; Tamang, 2012).
Currently, mainly three fermented vegetable products are
produced and consumed in the world—sauerkraut (in South
Korea, Chinese cabbage is fermented to obtain a more spicy
version called kimchi), pickles (fermented cucumbers), and olives
(Di Cagno, Filannino, & Gobbetti, 2016; Erten, Boyacı-G¨
und¨
uz,
A˘
gırman, & Cabaroglu, 2015; Hutkins, 2006; Steinkraus, 2002).
In Europe, approximately twenty different vegetable species are
fermented, but it must be remembered that there are many
acidified or pickled plant products that are simply produced by
adding vinegar, salt, and flavor ing mixtures to fresh vegetables. In
fact, most pickled products are not fermented, but rather simply
‘marinated’ using organic acids, mainly acetic acid (vinegar)
(Erten et al., 2015; Hutkins, 2006).
Mushrooms as a Raw Material for Lactic Acid
Fermentation
The chemical composition of edible mushrooms determines
their nutritional value and sensory properties. Scientific papers
describing the health-promoting properties of fungi and their nu-
tritional value appear mainly in the last twenty years. Table 1 shows
the content of the basic nutrients of three most commonly grown
species of mushrooms in the world.
The largest part of the dry matter of edible mushroom fruiting
bodies (from 35% to 70%) are carbohydrates (Guillam´
on et al.,
2010), that is, the most important ingredient for the use of
mushrooms as a raw material in the lactic fermentation process.
Fungal carbohydrates include mono- and disaccharides, sugar
alcohols, polysaccharides (including glucans), glycogen, and
chitin (Kalbarczyk & Radzki, 2009). Glucose, trehalose, and
mannitol are the main representatives of the monosaccharides,
disaccharides, and sugar alcohols present in the fungi, respectively.
Typically, the glucose and trehalose contents are low, in the order
of g per 100 g of dry matter. The mannitol content varies greatly
depending on the fungus species in the range from 0.2% to
13.9% of dry weight (Barros et al., 2007; Barros, Cruz, Baptista,
Estevinho, & Ferreira, 2008). Glycogen is a reserve polysaccharide
in fungi accounting for 5% to 10% of dry matter, whereas chitin
is a water-insoluble structural polysaccharide (Kalaˇ
c, 2009, 2013).
Given the content of polysaccharides, such as chitin, hemi-
cellulose, α-andβ-glucans, mannans, xylans, and galactans,
fruiting bodies of edible mushrooms are perceived as prebiotic raw
materials (Aida, Shuhaimi, Yazid, & Maaruf, 2009). Prebiotics
are defined as food ingredients that are not digestible in the
digestive tract and have the ability to stimulate the growth and
activity of beneficial bacteria in the digestive tract, mainly in the
large intestine. Synytsya et al. (2009) showed that the extracts
of Pleurotus ostreatus and Pleurotus eryngii stimulate the growth
of probiotic bacteria—Lactobacillus spp., Bifidobacterium spp., and
Enterococcus faecium. Tupamahu and Budiarso (2017) found that
the addition of fungal powder obtained from Pleurotus ostreatus to
yogurt contributes to an increase in the lactic acid content and
increases the survival of lactic bacteria in the final product.
Protein is an integral part of the dry mass of fungal fruiting
bodies. The amount of protein, based on dry matter, is usually
2Comprehensive Reviews in Food Science and Food Safety rVol. 0, 2019 C2019 Institute of Food Technologists®
Lacto-fermented edible mushrooms . . .
Table 1–Nutritional values in 100 g of dry matter for the three most-cultivated species of edible mushrooms.
Chemical component Pleurotus ostreatus Agaricus bisporus Lentinula edodes
Energy (kcal) 362.6a353.5a359.9a
Protein (g) 24.63e27.14eto 33.71b21.42e
Total fats (g) 1.40a3.75b1.73a
Total carbohydrates (g) 85.86a74.0a87.14a
Ash (g) 5.72a9.74a6.73a
Thiamine (B1) (mg) 0.90cto 4.25d0.60c0.60c
Riboflavin (B2) (mg) 2.5cto 2.84d3.37b1.80c
Niacin (B3) (mg) 65.0c37.3b31.0c
Cobalamin (B12)(μg) 0.6c0.8c0.8c
Folic acid (μg) 640c450c300c
Ergocalciferol (D2)(μg) 0.3cto 76.35f5.5 to 410.9b5.16gto 36.35f
Ascorbic acid (C) (mg) 20.0c<14b25.0c
aReis, Barros, Martins, & Ferreira, 2012.
bSimon, Phillips, Horst, and Munro, 2011.
cMattila et al., 2001, Simon, Phillips, Horst, & Munro, 2011.
dWatanabe, Tsuchihasi, Takai, Tanaka, & Suzuki, 1994.
eMattila, Lampi, Ronkainen, Toivo, & Piironen, 2002.
fJasinghe, Perera, & Sablani, 2007.
gJasinghe & Perera, 2005.
20% to 40%. It is more easily digested than the protein from
some plants, for example, soy or peanuts (Chang & Buswell,
1996; Chang & Mshigeni, 2001; Siwulski, Jasi´
nska, Sobieralski, &
Sas-Golak, 2011). The high protein content along with the low
dry matter content and high enzymatic activity contribute to
the low durability of mushroom fruiting bodies, and their rapid
spoilage is associated mainly with maturation and senescence
processes. The activity of metabolic enzymes such as proteases,
ribonuclease, and deoxyribonuclease increases (Tseng & Mau,
1999). Deterioration of the quality of fresh fungi is mainly related
to the degradation of proteins, autolytic processes, and deamina-
tion of amino acids (Kwa´
sniewska-Karolak & Krala, 2017). Fresh
mushrooms have high moisture content, water activity of 0.98 or
higher, and a neutral pH value, which is also an indirect cause of
rapid spoilage of fruiting bodies and the growth of putrefactive
bacteria (Venturini, Reyes, Rivera, Oria, & Blanco, 2011). The
rate of spoilage of mushrooms depends on the temperature
(Oliveira, Sousa-Gallagher, Mahajan, & Teixeira, 2012). Perish-
able fruiting bodies darken and change their taste and odor. There
are also putrefactive processes that may lead to the formation of
substances that are harmful to health. Button mushrooms (Agaricus
bisporus) stored for 12 days at 12 °C showed a 9% decrease in
the content of 5-nucleotides, that is, compounds responsible for
the characteristic organoleptic characteristics of fungi, while a
significant decrease in total sugars was observed, including almost a
10-fold decrease in fructose content and an almost double decline
in mannitol (Tseng & Mau, 1999). This may be a significant
problem in the case of raw material used for pickling, as carbo-
hydrate is the basic medium for lactic bacteria and their presence
is essential for the proper course of the fermentation process.
During storage, the amino acid content increases as well (Tseng
& Mau, 1999). It is worth mentioning that, during a five-day
storage of Volvariella volvacea at 4 and 25 °C, there was a signifi-
cant increase in the content of tryptamine and histamine, that is,
amino acids whose presence indicates progressive deterioration of
the quality of fruiting bodies. The level of these compounds was
positively correlated with the storage temperature (Yen, 1992).
Free amino acids are natural food ingredients or are released as a
result of the proteolysis reaction. However, in the process of their
microbiological decarboxylation occurring during controlled or
spontaneous fermentation, biogenic amines are formed, that is,
compounds with toxic and sometimes even carcinogenic proper-
ties, as precursors of carcinogenic N-nitrocompounds (Karoviˇ
cov´
a
& Kohajdov´
a, 2005). Therefore, mushrooms require refrigeration
storage at 0 to 2 °C and 90% relative humidity (Lopez-Briones
et al., 1992; Minato, Mizuno, Terai, & Tsuchida, 1999).
Lactic Fermentation of Mushrooms
Tradition of mushrooms fermentation
In many regions of the world, fermented mushrooms used to
be or are still a valued delicacy. Several species of fungi have been
lacto-fermented by Eastern Slavs, Estonians, and Poles. As re-
ported by S˜
oukand et al. (2015), formerly this was the primary
way of preserving fungi for the winter. In Poland, 5 taxa of wild
fungi are used for lactic fermentation: Boletus edulis,Armillaria spp.,
Lactarius deliciosus,L. salmonicolor,andTricholoma equestre (Łuczaj &
K¨
ohler, 2014; S˜
oukand et al., 2015). Fruiting bodies of Leccinum
spp., Suillus spp., Xerocomus spp., Lactarius deliciosus,andTr i c h o l o m a
equestre are fermented in Belarus and Leccinum spp., Lactarius de-
liciosus,L. deterrimus,L. rufus,L. torminosus,andRussula spp. are
fermented in Estonia. The most common types of mushrooms
used for this purpose are various species of milk caps (Lactarius).
Some of them, that is, L. rufus and L. torminosus,aretoxicintheir
raw state, and fermenting is the only method of detoxification
thereof (S˜
oukand et al., 2015). Lacto-fermented mushrooms are a
well-known and valued product also in the countries of southeast
Asia, where fermentation processes are commonly used in food
production, which allows utilization of waste or inedible material
(Stanton & Owens, 2003). In Japan, in the prefecture of Nagano,
a popular snack is fly agaric (Amanita muscaria), which is salted
after slicing and cooking and subjected to lactic fermentation.
Probably most toxic substances are removed in the technologi-
cal process and the mushrooms are safe for consumption in the
pickled form (Phipps, Bennett, & Downum, 2000). As shown
by Rai and Arumuganathan (2008), pickling mushrooms is also
a popular method for preservation thereof in India. The authors
enumerate several examples in their work and give recipes for both
lacto-fermentation and typical marinating of mushrooms.
Biological preservation of mushroom fruiting bodies using lac-
tic acid fermentation is currently not applicable on an industrial
scale; nonetheless, in the middle of the last century this method
was very popular. During harvest seasons, it facilitated the pro-
cess of quick and cheap management of excess raw material and
therefore played a similar role to salting. However, it was generally
accepted that lactic fermentation of fungi yielded a product with
better properties than salted mushrooms, due to both significantly
C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 3
Lacto-fermented edible mushrooms . . .
lower salt content in the silage and smaller losses of nutrients.
The salting process usually required exchange of brine three times
with which some of the soluble components acquired from the
fungi were discarded (Mering, 1955). Fermented fruiting bodies
of mushrooms, likewise salted ones, could serve as an interme-
diate for further processing, for example for making marinades
(Horubała & Wi´
sniewska, 1978).
In the first half of the last century, mainly red pine mushrooms
(Lactarius deliciosus) and less often the king bolete (Boletus
edulis) and other forest fungi were lacto-fermented in industrial
conditions. Mering (1955) reported that this method of preser-
vation was very popular in the countries of the former Soviet
Union, Czechoslovakia, and Poland. Red pine mushrooms were
fermented in internally paraffinized 200-L oak barrels or spruce
barrels. After pre-treatment processing (cleaning, sorting, and
washing), the mushrooms were placed, in 6-cm-thick layers, into
cleaned and paraffinated barrels, and each layer was covered with
4 kg of salt per 100 kg of raw material. Red pine mushrooms
were usually raw. In the case of other edible mushrooms, thermal
treatment consisting of short-term (2 to 5 min) cooking was
recommended (Mering, 1955, 1959; Miguła & Miguła, 1964). In
order to create better conditions for the process of lactic fermen-
tation, sugar (sucrose) was added at an amount of 1% to 1.5% in
relation to the mass of mushrooms, mixed with salt or in the for m
of syrup and soured milk or whey in the amount of 0.5% as a
carrier of lactic bacteria. It was very important to strictly arrange
the cap of mushrooms in each layer, which caused quick leakage
of the mushroom juice under the influence of salt and the disposal
of air (Mering, 1959). After a few days, the volume of mushrooms
in barrels was usually reduced, so they were topped with fresh
caps of the same species (Mering, 1959; Miguła & Miguła, 1964)
or fermented mushrooms from another barrel (Mering, 1955).
In some cases, it was necessary to top up the brine so that the
mushrooms were constantly covered with the liquid. Then 4%
brine or lactic acid was added (Mering, 1955, Miguła & Miguła,
1964). Fermentation was carried out at a temperature of 13 to
18 °C for several days until the acidity reached 1% to 1.5% in terms
of lactic acid. The barrels were then stored in cool basements or
ice-cold storage rooms for a maximum of 1 year (Mering, 1955).
Currently, there are no lacto-fermented mushrooms on the Eu-
ropean market and this technology has been replaced by other
methods of preservation, mainly freezing, marinating, and steril-
ization. In some regions of Europe, there is still a tradition of home
lactic fermentation of mushroom fruiting bodies (Grochowski,
1990). Locally, also fermented food products including mush-
rooms are available, for instance “sauerkraut with forest fungi”
(Zivanovic, 2006).
Raw material
The biological method of preserving cultivated and forest
mushrooms has been the subject of laboratory research, mainly
aimed at a thorough improvement of the process. These studies
involved various species of mushrooms, but most of the work was
devoted to button mushrooms—Agaricus bisporus (Jabło´
nska-Ry´
s
&Sławi
´
nska, 2012; Jabło´
nska-Ry´
s, Kalbarczyk, & Sztaba, 2005;
Jabł o ´
nska-Ry´
s, Sławi´
nska, Radzki, & Gustaw, 2016a; Joshi,
Kaur, & Thakur, 1996; Milanoviˇ
c, Davidoviˇ
c, & Saviˇ
c, 2010;
Niksic, Stojanovic, Zivanovic, & Veljic, 1997; Sk ˛
apska et al.,
2008; Stojanovic, Niksic, Veres, & Petrovic, 1994) and oyster
mushroom—Pleurotus ostreatus (Jabło´
nska-Ry´
s&Sławi
´
nska,
2012; Jabło´
nska-Ry´
s, Sławi´
nska, & Szwajgier, 2016b; Kreß,
1989; Kreß & Lelley, 1991; Sk ˛
apska et al., 2008; Stojanovic,
Figure 1–Button mushrooms fermented with spices—final product (photo
by Jabło´
nska-Ry´
sE.)
Niksic, & Krnjaja, 1996). Figure 1 presents the final products
obtained from the button mushrooms. Other species were
also studied: Pleurotus sajor-caju (Kreß, 1989; Kreß & Lelley,
1991; Liu et al., 2016), Pleurotus cornucopiae (Liu et al., 2016),
Pleurotus eryngii (Zheng, Chen, & Ahmad, 2018), Flammulina
velutipes (Gao & Liu, 1995), Paxillus spp. and Lactarius spp. (Zhuk-
Yu, Papilinia, & Bakaitis, 1985), Auricularia auricula (Khaskheli
et al., 2015), and Cantharellus cibarius (Jabło´
nska-Ry´
s et al., 2016b).
Termitomyces robustus was fermented as well; it is a specific mush-
room with edible and, as commonly agreed, very tasty fruiting
bodies grown by termites in their nests (Bello & Akinyele, 2007).
For processing, including the lactic acid fermentation, raw ma-
terial should be used immediately after collection due to its low
durability.
Preliminary processing
An important step during the processing of mushrooms, directly
affecting their quality, is the pre-treatment. It consists of cleaning,
sorting, washing, cutting, and blanching.
Cleaning and washing. A particularly important process is the
cleaning of mushrooms obtained from natural stands, whose fruit-
ing bodies should be thoroughly cleaned of forest debris, removing
infested and rotten fruiting bodies and cutting the stem (Jabło´
nska-
Ry´
s et al., 2016b). Good quality fruiting bodies can be sorted, for
example, according to the diameter of the cap. This parameter is
important if the fungi are further processed as a whole, without
cutting. In the case of cultivated mushrooms, cleansing is usually
less time-consuming. The stem of the button mushrooms should
be cut perpendicularly to the axis at the collection time, and the
fruit bodies should be clean. Mushrooms are sorted initially at the
time of collection according to classes depending on the diameter
of the cap and they are placed in separate containers (Dami˛
ecka &
Szudyga, 2006.)
Mushrooms intended for lactic fermentation should be washed
in cold running water (Liu et al., 2016). In the research usu-
ally carried out at laboratory-scale, the authors of studies on
fermented mushrooms used hand-washing (Jabło´
nska-Ry´
s et al.,
2016a; Jabło´
nska-Ry´
s et al., 2016b; Liu et al., 2016; Zheng et al.,
2018). On a larger scale, due to their susceptibility to mechanical
damage, fungi are washed with water-air washers with additional
spray (Jarczyk & Płocharski, 2010). A washing process carried out
properly enables removal of dirt after dry cleaning and partial
4Comprehensive Reviews in Food Science and Food Safety rVol. 0, 2019 C2019 Institute of Food Technologists®
Lacto-fermented edible mushrooms . . .
reduction of surface microflora. However, this treatment may also
induce deterioration of the quality of the fruiting body. Even mi-
nor mechanical injury leads to damage to the delicate cell struc-
tures and activation of enzymes responsible for darkening (Berna´
s
et al., 2006). During manual cleaning of button mushrooms in-
tended for lactic fermentation, a significant decrease in the L
(lightness) parameter from 93.23 in the case of fresh fungi to
88.74 in the case of washed fungi and an increase in the a(red-
ness) value from 0.57 to 3.12, and the b(yellowness) parameter
from 12.75 to 16.16 has been noted (Jabło´
nska-Ry´
s et al., 2016a).
Therefore, while washing fungi for processing, various substances
that counteract the darkening of fruiting bodies are used, for ex-
ample, sodium and potassium metabisulfite (Czapski & B ˛
akowski,
1995) or hydrogen peroxide, cysteine isoascorbate, and versenic
acid, which all affect the color and reduce the activity of the
polyphenol oxidase enzyme (Burton & Noble, 1993). Washing
fruiting bodies of mushrooms in an aqueous solution of hydrogen
peroxide (5%), sodium isoascorbate (4.5%), cysteine hydrochlo-
ride (0.2%), and Na2EDTA (0.1%) resulted in a brightness value
higher by 3 units than the initial value (Czapski, 2002).
During the process of washing, soluble substances are washed
out into the water. The use of some additives may inhibit this
process. As reported by Sapers, Miller, Choi, and Cooke (1999),
washing mushrooms in water containing 2 to 5 ppm of chlor ine
caused a slight decrease in the content of soluble polyphenols
from 2.9–3.1 to 2.5–3.0 mg/g dry matter. An increase in the
polyphenol content to 3.8 to 4.7 mg/g dry weight was observed
in mushrooms washed in a5% aqueous hydrogen peroxide solution
and then sprayed with a 4% sodium erythorbate solution.
Cutting. Only mushroom caps are usually used for lactic fer-
mentation, whereas the stems are discarded. In the study con-
ducted by Jabło´
nska-Ry´
s et al. (2016a), small mushroom fruiting
bodies with a cap diameter of 3.5 to 4.5 cm with the stems cut
short were chosen. In most studies, caps were pickled as a whole;
however, Auricularia auricula and Pleurotus eryngii fruiting bodies
were cut into slices (Khaskheli et al., 2015; Zheng et al., 2018).
Blanching process. Most authors subjected mushrooms to the
blanching process in boiling water for 2 to 5 min. The detailed
values of the parameters of this process are given in Table 2. Fer-
mented mushrooms have better quality if subjected to blanching
(Zhuk-Yu & Papilina, 1983; Zhuk-Yu, Suslova, & Papilina, 1982).
In India, mushroom fruiting bodies for lactic fermentation are
blanched or fried in oil (Rai & Arumuganathan, 2008). The main
purpose of blanching is to remove excess air from the raw material
and to reduce its volume. This allows putting in a unitary pack-
aging of a larger mass of fruiting bodies. In addition, during the
blanching process, enzymes are inactivated and partial destruction
of the microflora is observed (Jarczyk & Płocharski, 2010).
Typically, mushrooms intended for lactic fermentation are
blanched in water without any additives; however, Khaskheli et al.
(2015) recommend blanching in a 0.05% potassium metabisulfite
solution. Fruiting bodies of mushrooms intended for other
forms of processing are usually blanched with the addition of
substances to prevent darkening. For this purpose, 0.05% to
0.5% aqueous solutions of citric acid are used (Mart´
ın-Belloso &
Llanos-Barriobero, 2001; Rodrigo, Calvo, Sanchez, Rodrigo, &
Mart´
ınez, 1999). Some mushrooms, for example king boletes and
chanterelles, require a higher concentration of acid, that is, 1%
(Jarczyk & Płocharski, 2010). In addition to citric acid, ascorbic
acid (Jaworska & Berna´
s, 2009a; Jaworska, Berna´
s, Cicho´
n, &
Possinger, 2008) and potassium or sodium metabisulfite (Czapski
& Szudyga, 2000; Gapi´
nski, Wo´
zniak, & Ziombra, 2001; Jaworska
&Berna
´
s, 2009a; Jaworska et al., 2008) are used in blanching
as well. Hydrogen peroxide, versene acid, sodium isoascorbate,
cysteine hydrochloride, calcium chloride, sodium chloride, and
low-methylated pectins are also applied (Beelman, Kuhn, &
McArdle, 1973; Cos¸kuner & ¨
Ozdemir, 2000; Czapski, 2001,
2002; Jaworska, Berna´
s, & Mickowska, 2011; Kukura, Beelman,
Peiffer, & Walsh, 1998).
It should be noted that, besides the benefits mentioned above,
the blanching process is a cause of large losses of nutrients,
mainly the water-soluble ones, and destruction of substances
sensitive to high temperatures (Biekman, Kroese-Hoedeman, &
Schijvens, 1996; Jaworska & Berna´
s, 2009b, 2009a,b). It also
contributes to significant weight loss, ranging from 30% to 40%
(Erbay, Kucukoner, & Orhan, 2011; Lespinard, Go˜
ni, Salgado,
& Mascheroni, 2009; Vivar-Quintana, Gonzalez-San Jose, &
Collado-Fernandez, 1999) and volume loss by denaturation of
proteins in the cellular structures, cytoplasmic coagulation, and
disruption of intracellular membranes, which leads to partial loss
of water retention capacity (Berna´
s & Jaworska, 2007; Zivanovic
& Buescher, 2004). It can also have an adverse effect on the
mushroom texture, because it contributes to an increase in
the hardness and gumminess of fruiting bodies (Czapski, 1994;
Steinbuch, 1979). As shown by Berna´
s, Jaworska, Maciejaszek,
and Biernacka (2007), a significant reduction in hardness and an
increase in springiness in fruiting bodies was noticed as a result
of pre-treatment of mushrooms (blanching in water or soaking
and blanching in an aqueous solution of 1% lactic acid and 0.1%
l-ascorbic acid). In addition, appearance of wateriness in blanched
samples was demonstrated by means of a profile analysis of sensory
features.
The influence of blanching on the quality of mushrooms sub-
jected to this process depends on many parameters, mainly on
the temperature and the time of heat treatment. The duration
of the procedure can range from 20 s to even 15 min. It should
be remembered that complete inactivation of peroxidase can be
obtained by only a 15-min blanching (Berna´
s & Jaworska, 2007).
The authors of the work on fermented mushrooms did not per-
form blanching of mushrooms intended for pickling for such a
long time.
It is possible to use unconventional methods of blanching, for
example a combination of microwave blanching with traditional
blanching in hot water. Such a treatment method inactivates
polyphenoloxidase within a short time (3 min of treatment). In
mushrooms, polyphenoloxidase is considered the primary enzyme
responsible for browning. In the microwave treatment, both
shrinkage and weight loss were considerably improved due to the
reduction in the blanching time. The lower weight loss with re-
spect to shrinkage is explained by the microwave water-pumping
effect. Weight loss or shrinkage related to water evaporation occur-
ring during thermal processing usually ranges between 30% and
40%. It is a major problem in commercial mushroom processing.
Unfortunately, microwave blanching for 3 min at 85 °C produced
a substantial loss in total antioxidant activity. Better results in
terms of temperature distribution, polyphenoloxidase inactivation,
weight loss, shrinkage, total antioxidant activity, and browning of
samples were obtained using a mixed method (1 min microwave at
85 °Cplus20s92°C water bath) (Devece et al., 1999). Research
was also carried out on the use of ohmic heating in the process
of blanching fungi. Ohmic heating is an alternative method
allowing even and quick heating of the raw material. In addition,
in contrast to traditional blanching, it allows thermal processing
in a relatively small amount of water; the share of the raw material
C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 5
Lacto-fermented edible mushrooms . . .
Table 2–Methods of blanching mushrooms before fermentation.
Blanching parameters References
Agaricus bisporus In boiling water or by using microwave oven Niksic et al. (1997)
In boiling water for 5 min Jabło´
nska-Ry´
s et al. (2005)
In boiling water for 2 min Sk˛
apska et al. (2008); Jabło´
nska-Ry´
s et al. (2016a)
Auricularia auricula 96 to 98 °C for 5 min in 0.05% potassium metabisulfite solution Khaskheli et al. (2015)
Cantharellus cibarius In boiling water for 4 min Jabło´
nska-Ry´
s et al. (2016b)
Pleurotus cornucopiae 96 to 98 °C for 4 min Liu et al. (2016)
Pleurotus ostreatus In boiling water for 4 min Sk˛
apska et al. (2008); Jabło´
nska-Ry´
s et al. (2016b)
96 to 98 °C for 4 min Liu et al. (2016)
Pleurotus sajor-caju 96 to 98 °C for 4 min Liu et al. (2016)
Termitomyces robustus In boiling water Bello and Akinyele (2007)
is about 40% to 50%. In such conditions, blanched fungi reach a
temperature of 70 °C after 40 s. Unfortunately, this method, like
traditional blanching, contributes to large losses of 40% of raw
material mass (Sensoy & Sastry, 2004). Nonstandard methods of
blanching mushrooms intended for lactic fermentation, namely
using microwaves, were used only in one publication (Niksic et al.,
1997).
Additives and spices
The most important additive used in the lactic acid fermenta-
tion of mushrooms is salt, used mainly to evoke exosmosis and
to improve the taste. In most cases, NaCl in fermented fungi is
not a preservative due to the insufficient concentration. In most
studies, sodium chloride was added at an amount of 2% in relation
to the mass of the raw material (Table 3). Salt can be added dry
(dry-salting) or as an aqueous solution if the fungi are fermented
in brine. During the process of dry-salting, it is very important
to mix the raw material with salt thoroughly and put it in con-
tainers in which the fermentation process will take place. Precise
mixing, and even leaving the mushrooms with spices for 2 to 3 hr,
ensures anaerobic conditions, because the released liquid filling
empty spaces in the vessel displaces the air (Jabło´
nska-Ry´
s et al.,
2016a; Sk ˛
apska et al., 2008). If the amount of the natural brine
is too small, the mushroom surface can be covered with a 2%
aqueous salt solution (Jabło´
nska-Ry´
s et al., 2016b). As shown by
Khaskheli et al. (2015), Auricularia auricula fruiting bodies were
mixed with 10% NaCl and left overnight. After this time, the
excess liquid was removed and the mushrooms were mixed with
the remaining spices specified in the recipe. The pre-treatment of
various species of fungi processed in India was very similar (Rai &
Arumuganathan, 2008). In the case of fermentation mushrooms in
brine, it is recommended to use the raw material at an amount of
4:1 to 1:1.5 in relation to brine containing 2% to 5% salt (Zheng
et al., 2018; Zivanovic, 2006).
Besides salt, sugar is also an important addition considered in
most studies. It is used as an easily available source of carbon for
lactic bacteria. It is recommended that sugar should be added at
an amount of not more than 3.3% in order to accelerate lactic
fermentation (Zivanovic, 2006); in most studies, this supplement
was added as sucrose in a range of 1% to 3% (Table 3).
Milanoviˇ
c et al. (2010) used a 2% addition of sucrose, glucose, or
fructose as a medium for lactic bacteria. The authors observed the
fastest decrease in the pH value and an increase in the lactic acid
content in samples of pickled fungi supplemented with glucose,
while the fermentation process was carried out the most slowly in
samples with the addition of sucrose. Nevertheless, after 10 days
of fermentation, the lactic acid content was at a similar level in all
samples, regardless of the type of sugar added.
In addition to salt and sugar, different spices can be added dur-
ing fermentation of mushrooms (Table 3), thereby influencing
the taste and odor of the finished product. Jabło´
nska-Ry´
sand
Sławi´
nska (2012) conducted fermentation of oyster mushrooms
and button mushrooms with the use of three different starter cul-
tures and with the addition of spices. Salt, sugar, black ground
pepper, onion, and laurel leaves were used at an amount of 2%;
1%; 0.1%; 5%, and 0.2%, respectively, in relation to the weight
of blanched mushrooms. The finished products scored high marks
in the organoleptic assessment carried out after the end of fer-
mentation (the seventh day of the experiment) and after a 4-week
refrigerated storage period.
Zheng et al. (2018) subjected Pleurotus eryngii fruiting bodies
to lactic fermentation, according to three traditional recipes for
vegetables, sauerkraut, pickled cucumbers, and kimchi, using 3%
red pepper and 2% garlic as a spice in all combinations. The most
varied additives were proposed by Khaskheli et al. (2015), that is,
mustard oil and vinegar besides basic spices (Table 3).
Starter cultures
In a majority of studies on fermented mushrooms, lactic fer-
mentation was carried out with the participation of starter cul-
tures of lactic acid bacteria (LAB). The use of selected LAB strains
ensures a correct and repeatable course of the process and yields
a finished product with high sensory quality. The use of targeted
lactic fermentation simultaneously increases the health-beneficial
value of mushrooms due to the presence of viable cells of lac-
tic acid bacteria (Sk ˛
apska et al., 2008). Currently, in processing,
spontaneous fermentation is more often being replaced by a con-
trolled process based on the use of specific LAB strains. Starter
cultures of Lactobacillus plantarum (dedicated to fermentation of
raw materials of plant origin) were mainly used for the fermen-
tation of fruiting bodies of edible mushrooms (Jabło´
nska-Ry´
s&
Sławi´
nska, 2012; Jabło´
nska-Ry´
s et al., 2005, a, b; Joshi et al., 1996;
Milanoviˇ
c et al., 2010; Niksic et al., 1997; Sk ˛
apska et al., 2008;
Zheng et al., 2018). Other species, for example, L. bulgaricus,L.
delbrueckii,L. brevis,L. casei,L. helveticus,L. pentosus,Streptococ-
cus lactis,Lactococcus lactis,Leuconostoc mesenteroides,andPropionibac-
terium freudenreichii were successfully used as well (Jabło´
nska-Ry´
s&
Sławi´
nska, 2012; Jabło´
nska-Ry´
s et al., 2005; Joshi et al., 1996; Liu
et al., 2016; Sk ˛
apska et al., 2008). In the above-mentioned studies,
starter cultures were added in quantities from 104to 108cfu/g
of the raw material. Zheng et al. (2018) used the LAB powder
starter additive at an amount of 0.1%. Three- and 7-day sauerkraut
juice was also used as a source of lactic bacteria (Kreß & Lelley,
1991). Natural fermentation of fruiting bodies of the edible mush-
room Termitomyces robustus was used in the research conducted by
Bello and Akinyele (2007), while Rai and Arumuganathan (2008)
6Comprehensive Reviews in Food Science and Food Safety rVol. 0, 2019 C2019 Institute of Food Technologists®
Lacto-fermented edible mushrooms . . .
Table 3–Ingredients used for lacto-fermented mushrooms.
Salt and sugar Other ingredients References
Agaricus bisporus 2% or 3% salt, optionally additive
lactose
Joshi et al. (1996)
Brine with 0.1% to 2% salt, 0.1% to
2% sucrose
Niksic et al. (1997)
2% salt, 1% sucrose 0.1% black pepper, 2 crushed bay
leaves, 10% onion slices
Jabło´
nska-Ry´
s et al. (2005)
2% salt, 1% sucrose Sk˛
apska et al. (2008);
Jabło´
nska-Ry´
setal.
(2016a)
2% salt, 1% sucrose 0.1% black pepper, 0.2% crushed
bay leaves, 5% onion slices
Jabło´
nska-Ry´
s and Sławi´
nska
(2012); Jabło´
nska-Ry´
setal.
(2016a)
Brine with 2% salt, 2% sucrose Milanoviˇ
c et al. (2010)
Auricularia auricula 10% salt, kept overnight Next day mixed with mustard oil,
vinegar (5% acetic acid) and spices
(turmeric powder, black mustard
seed powder, red chili powder,
cumin seed powder, carom seed,
nigella seed, fennel seed powder)
Khaskheli et al. (2015)
Cantharellus cibarius 2% salt, 1% sucrose Jabło´
nska-Ry´
s et al. (2016b)
Pleurotus cornucopiae Brine with 2% salt, 3% sucrose Liu et al. (2016)
Pleurotus eryngii Brine with 2% salt, 1% sucrose 3% red pepper, 2% garlic Zheng et al. (2018)
Soaked in a solution of 4% salt and
2% sugar for 5–6 hr
3% red pepper, 2% garlic Zheng et al. (2018)
Brine containing 2.06 M NaCl, 2%
sugar
3% red pepper, 2% garlic, 50 mM
acetic acid
Zheng et al. (2018)
Pleurotus ostreatus 2% salt, 1% sucrose Sk˛
apska et al. (2008);
Jabło´
nska-Ry´
setal.
(2016b)
2% salt, 1% sucrose 0.1% black pepper, 0.2% crushed
bay leaves, 5% onion slices
Jabło´
nska-Ry´
s and Sławi´
nska
(2012)
Brine with 2% salt, 3% sucrose Liu et al. (2016)
Pleurotus sajor-caju Brine with 2% salt, 3% sucrose Liu et al. (2016)
Termitomyces robustus Soaked in a solution of 10% salt Bello and Akinyele (2007)
described the process of natural fermentation used to preserve
oyster mushrooms.
Natural fermentation was also adopted in the case of Auricularia
auricular fruiting bodies, but this time the authors decided to use
vinegar as an additive, as in the case of the production of marinades,
so it was not a typical technology of lacto-fermentation. Next, the
pickles were stored at ambient temperature of 26 ±4°C for about
3 to 4 weeks for fermentation (Khaskheli et al., 2015). To promote
the growth of desirable microflora in the spontaneous fermentation
process, adequate anaerobic conditions and optimal temperatures
should be ensured. The initiation of spontaneous fermentation
takes a relatively long time (24 to 48 hours), which is associated
with the highest risk of development of undesirable microflora. In
numerous traditional processes, material from a previous successful
batch is added to facilitate the initiation of a new process. Repet-
itive use of back-slopping results in selection of the best-adapted
strains, some of which may possess features that are desirable for
use as starter cultures (Holzapfel, 2002). In industrial conditions,
the product is sometimes acidified by addition of acetic or lactic
acid, especially to those fermented with low salt content. The pH
reduced in this way immediately at the onset of the process pro-
tects the product against the development of unwanted microflora
(Guizani, 2011). However, this is not a typical lactic fermenta-
tion process, as there is no full generation of metabolites of lactic
bacteria and the finished product exhibits different sensory traits.
McFeeters (2004) showed that the fermentation process is cer-
tainly necessary for the development of typical sauerkraut flavor,
because acidification of cabbage does not result in a product with
sauerkraut odor or flavor. In Poland, some producers add acetic or
lactic acid in the process of fermentation of cabbage or cucum-
bers to achieve instantaneous reduction of the pH value. However,
in Poland according to the current provisions on the commercial
quality of agri-food products (Act of 21 December 2000 on the
commercial quality of agri-food products, Journal of Laws 2014,
item 669) and the regulations of labeling of foodstuffs (Regulation
of the Minister of Agriculture and Rural Development of 10 July
2007 on the labeling of foodstuffs, Journal of Laws 2014 item 774),
such a product cannot be labeled as a fermented food (opinion is-
sued by IJHARS-Agricultural and Food Quality Inspection).
In another study, Khaskheli et al. (2017) investigated the physic-
ochemical and sensory properties of shiitake mushroom pick-
les. The authors described the product as a fermented one but
did not specify the conditions and parameters of this process in
the methodology. They only referred to the study reported by
Wakchaure, Shirur, Manikandan, and Rana (2010). In the source
method, the mushrooms pickles were obtained in the process of
blanching, salt treatment (overnight), mixing mushrooms with
spices, and preserving using acetic acid and sodium benzoate.
Therefore, it was not a process of lactic fermentation but typi-
cal marinating.
In the process of lactic fermentation of mushroom fruiting bod-
ies, probiotic bacterial species or strains can be successfully used
as starter cultures. The probiotic L. plantarum 299v strain used
in the process of fermentation of mushroom fruiting bodies con-
tributed to a rapid reduction of the pH value and stabilization
of this parameter during the 5-week refrigerated storage, and
the finished products were characterized by high sensory quality
and high LAB number of 9.2 ×107cfu/g (Jabło´
nska-Ry´
s et al.,
2016a).
Conditions of Lactic Fermentation and Durability of
the Finished Product
The course of the lactic fermentation process is influenced by
many factors, such as the type of pretreatment used (including
C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 7
Lacto-fermented edible mushrooms . . .
Table 4–Conditions of the fermentation process.
Temperature and
time
of fermentation
pH parameter and
acidity
in the final product
LAB content in
the final product Product durability References
Agaricus bisporus 18 to 20 °C for 7 days pH ˂4.1 9 log cfu/g 7 weeks at 4 to 6 °C
or pasteurized
Sk˛
apska et al. (2008)
21 to 22 °C for 7 days pH ˂4.0; acidity 0.6
to 0.9%
4 weeks at 5 °C Jabło´
nska-Ry´
sand
Sławi´
nska (2012)
20 to 21 °C for 8 days pH 3.6 to 3.75 9.2 ×107–5.5
×108cfu/g
5 weeks at 5 °C Jabło´
nska-Ry´
setal.
(2016a)
Auricularia
auricular
26 ±4°C for about 3
to 4 weeks
pH 4.5 to 5.5 94 ×101to 49 ×
103cfu/g 90 days at 26 ±4°C Khaskheli et al. (2015)
Cantharellus
cibarius
21 to 22 °C for 8 days pH 3.5 – 4.0 6 months at 5 °C Jabło´
nska-Ry´
setal.
(2016b)
Pleurotus
cornucopiae
20 °C for 18 days pH ˂3.8 7.5 log cfu/mL Liu et al. (2017)
Pleurotus eryngii 4°C for 30 days pH 4.4; acidity 0.45% 7.4 log cfu/g Zheng et al. (2017)
20 °C for 30 days pH 3.3; acidity 1.3% 7.5 log cfu/g
30 °C for 30 days pH 3.5; acidity 0.6% 7.5 log cfu/g
Pleurotus
ostreatus
18 to 20 °C for 7 days pH ˂4.1 9 log cfu/g 7 weeks at 4 to 6 °C
or pasteurized
Sk˛
apska et al. (2008)
21 to 22 °C for 8 days pH 3.5 – 4.0 6 months at 5 °C Jabło´
nska-Ry´
setal.
(2016b)
21 to 22 °C for 7 days pH ˂4.0; acidity 0.6
to 0.8%
4 weeks at 5 °C Jabło´
nska-Ry´
sand
Sławi´
nska (2012)
20 °C for 18 days pH ˂3.8 7.5 log cfu/mL Liu et al. (2017)
Pleurotus
sajor-caju
20 °C for 18 days pH ˂3.8 7.5 log cfu/mL Liu et al. (2017)
Termitomyces
robustus
30 ±2°C for 6 days pH 4.03 – 4.6 Bello and Akinyele
(2007)
total bacterial count
blanching parameters), additives used (salt, sugar, spices), the
addition or absence of a starter culture, fermentation in brine
(spices plus water) or natural brine (with dry salting) and, finally,
the temperature. Fermentation of fruiting bodies of edible
mushrooms is usually carried out at a temperature of 18 to 26 °C
for a period of several to 30 days (Table 4). As indicated by some
authors, mushrooms fermented at a lower temperature (around
20 °C) are characterized by better sensory quality (Zhuk-Yu &
Papilina, 1983; Zhuk-Yu et al., 1982).
Zheng et al. (2018) used three traditional technologies in the
process of lactic fermentation the fruiting bodies of Pleurotus
eryngii, with varying temperatures during fermentation, that is, 4,
20, or 30 °C, respectively, for kimchi, sauerkraut, and fermented
cucumber technology. The initial population of LAB in the inoc-
ulated king oyster mushrooms was 5.3 log cfu/g, which increased
sharply to a high level of 9.0 log cfu/g within 2 days for the
sauerkraut fermentation process. For the kimchi process, the LAB
counts grew much slower to reach the maximum of 8.5 log cfu/g
on the 15th day. However, after 30 days of fermentation in all
experimental combinations, the LAB content stabilized at a similar
level of about 7 log cfu/g. This value was indicated by most au-
thors of studies focused on fermented mushrooms (Table 4). Only
in the case of the research reported by Khaskheli et al. (2015), the
bacterial count after 3 to 4 weeks of fermentation of Auricularia
auricula fruiting bodies at a temperature of 26 ±4°C was slightly
above 3 log cfu/g, depending on the experimental combination.
However, as mentioned previously, these studies did not reflect a
typical lactic fermentation process, as the recipe contained acetic
acid. Despite the low number of bacteria in the finished product
and at the same time a relatively high pH, which reached 4.5 to
5.5 after 25 days, depending on the experimental combination,
the authors declared high durability of the product. Processed
Auricularia auricula stored at 26 ±4°C for 90 days demonstrated
no significant qualitative changes. As shown by many authors,
preservation of vegetables via lactic fermentation is regarded as
a simple and valuable biotechnological method, which helps to
preserve the nutritional and sensory qualities of the raw material
and, primarily, to produce fully safe and durable food. However,
to achieve this, an appropriate amount of lactic acid must be
produced during the fermentation process, as it acidifies the envi-
ronment, thus preventing the growth of undesirable microflora. As
demonstrated by Steinkraus (2002), fermented vegetables retain
long-term stability at pH 4.0 and anaerobic conditions. Biopreser-
vation is also a result of synthesis of other primary and secondary
metabolites accompanying fermentation, e.g. carbon dioxide,
ethanol, hydrogen peroxide, diacetyl, fungicides, bacteriocins,
and antibiotics (Di Cagno, Coda, De Angelis, & Gobbetti, 2013).
Lactic acid is mainly responsible for the durability of fermented
fungi. Its content in the finished product ranged from 0.45% to
1.3% (Table 4). In oyster mushroom fruiting bodies, fermented
with the addition of L. plantarum, the general acidity was at 0.45%
(Kreß, 1989), whereas it reached 1.29% when the mushrooms were
fermented together with fresh cabbage and 0.55% and 0.71% when
3- and 7-day sauerkraut juice was used as inoculum, respectively
(Kreß & Lelley, 1991).
It is believed that a fermented product is durable when acids pro-
duced during fermentation decrease the pH to 4.0 to 4.1 (Joshi
et al., 1996; Steinkraus, 2002). Liu et al. (2016) subjected oyster
mushrooms to lactic fermentation with the participation of Lacto-
bacillus pentosus. The process was carried out for 18 days at 20 °C.
On the third day of the experiment, the pH dropped below 4.0
and reached about 3.5 in all samples after 18 days of fermentation.
After the fermentation process, the lactic acid content in the brine
was at the level of 3.72 to 4.49 mg/mL.
In many studies, investigations were focused only on the fer-
mentation process and the product obtained was not stored (Bello
& Akinyele, 2007; Liu et al., 2016; Zheng et al., 2018). In some
scientific studies, the issue of storage stability of fermented fungi
8Comprehensive Reviews in Food Science and Food Safety rVol. 0, 2019 C2019 Institute of Food Technologists®
Lacto-fermented edible mushrooms . . .
is discussed. Finished products were stored for a period of 4 weeks
to 6 months (Table 4).
The shelf-life of pickled products is influenced by their chemical
composition (acidity, pH) as well as storage conditions. As demon-
strated by Kreß and Lelley (1991) and Jabło´
nska-Ry´
s et al. (2016b),
the finished product is microbiologically stable for six months of
storage under refrigeration conditions. Pasteurization is not re-
quired to preserve the products, but it can improve the quality
of the stored product. In the research conductedby Sk ˛
apska et al.
(2008), pasteurization of fermented mushrooms did not reduce
the antioxidant capacity and the content of phenolic compounds
in the products. Most authors suggest storing the finished product
in refrigeration conditions at 4 to 6 °C (Table 4). Only Khaskheli
et al. (2015) stored the finished product at room temperature (26
±4°C). The authors found that the durability and microbio-
logical stability of fermented mushrooms were influenced by the
addition of oil, which created a thin layer on the surface of the
product protecting it from deterioration.
Quality of fermented mushrooms
Chemical composition. Khaskheli et al. (2015) studied the con-
tent of polysaccharides in fermented Auricularia auricula. The au-
thors demonstrated that the polysaccharide content, determined
with the phenolsulfuric acid method, declined during processing
from about 4.25% to 1.64–2.35% depending on the type of fer-
mented product. This means that lactic acid bacteria are able to
use fungal sugars, and lactic fermentation of fungal fruiting bodies
is possible without the addition of sugars. Similar to Bello and
Akinyele (2007), the authors of this study did not include addition
of sugar in the recipe.
Liu et al. (2016) analyzed the content of organic acids produced
during lactic fermentation of oyster mushrooms (Pleurotus spp.).
The authors showed that lactic acid, whose content in the brine
was at the level of 3.72 to 4.49 mg/mL, is the main product of lactic
fermentation. In addition to this compound, the authors identified
four other organic acids: acetic, citric, malic, and succinic acids in
the amounts of 0.74 to 0.92; 0.04 to 0.22; 0.17 to 0.24; and 0.46
to 0.52 mg/mL in the final product.
Bello and Akinyele (2007) studied the effect of fermentation
on the mineral content in Termitomyces robustus.Raw,blanched,or
salted material was fermented. They showed that salted and fer-
mented fungi contained most minerals. The fermentation process
increased the content of calcium, magnesium, potassium, man-
ganese, iron, and sodium. This fact is explained by the authors by
the influence of the technological process. Probably, during the
thermal processing and fermentation, the content of antinutritive
compounds that bind certain metals is reduced, contributing to
their increased bioavailability. The content of zinc, calcium, and
magnesium decreased in the samples when the mushrooms were
fermented in the fresh form. As explained by the authors, these re-
sults may be related to the use of these minerals by microorganisms
in the processes of their growth.
Fungi are a valuable raw material because of the content of phe-
nolic compounds and the associated antioxidant activity. Sk ˛
apska
et al. (2008) determined changes in the antioxidant capacity
and the content of phenolic compounds in the process of lactic
fermentation of fruiting bodies of button mushrooms and oyster
mushrooms by lactic fermentation carried out using a starter cul-
ture. As a result of mushroom blanching, the total phenol content
decreased by 60% to 67% and the antioxidant capacity by 54% to
79%. During fermentation, there was a further reduction in these
parameters, whereas an upward trend was observed after 3 weeks
of refrigeration storage. The increase in these parameters observed
during the storage of the samples is explained by the author
by the acidic processes of hydrolysis and the release of phenolic
components that take place. The release of phenols associated with
cell walls in the form of esters and glycosides may also occur as a
result of the action of bacterial enzymes. The research conducted
by Jabło ´
nska-Ry´
s et al. (2016a) confirmed the negative impact of
blanching on the content of phenolic compounds in mushrooms;
however, in this case the lactic fermentation process did not cause
a further decrease in the content of these compounds. It was
also shown that the use of the L. plantarum 299v probiotic strain
enhanced an increase in the antioxidant activity of fermented
mushrooms to a level similar to that of fresh mushrooms. The type
of the starter culture used has a significant effect on the content of
phenolic compounds, antioxidant activity (Jabło´
nska-Ry´
s et al.,
2016a), and the content of individual phenolic acids in fermented
mushrooms (Jabło´
nska-Ry´
s et al., 2016b). When L. plantarum
was used as a starter culture in fermented fruiting bodies of the
oyster mushrooms and chanterelles, higher contents of gallic,
homogentisic, and ferulic acids were found than in the case of L.
helveticus or L. casei. In addition, it was noted that the content of
ferulic acid in the fermented oyster mushrooms was remarkably
higher than in the fresh fruiting bodies. In the case of the
chanterelle (C. cibarius), vanillic acid was found in the fermented
samples, but it was not present in the fresh and blanched fungi.
The authors found that the content of phenolic acids in fermented
fungi depended on many factors, such as mushroom species, the
LAB strain, and the conditions applied during fermentation.
Physical properties and organoleptic qualities. Lactic fer men-
tation affects the color of fungi. It has been shown that during the
pre-treatment, the brightness of mushroom fruiting bodies is sig-
nificantly reduced. The change in the color is a result of washing;
next, it deepens in the process of blanching. During lactic fermen-
tation, the brightness stabilizes (the value of this color parameter
does not change further) and a significant reduction of the a(red-
ness) parameter takes place. The bparameter (yellowness) is also
subjected to changes, increasing its value at every stage of the tech-
nological process, that is, washing, blanching, and fermentation
(Jabło´
nska-Ry´
s et al., 2016a). As shown by Jaworska et al. (2008),
deterioration of the brightness of blanched mushrooms can range
from 9% to 26%. The change in the color in the case of mush-
rooms, especially their brightness, is usually perceived by the con-
sumer as deterioration of quality (Erbay et al., 2011). As demon-
strated in the study conducted by Jabło´
nska-Ry´
s et al. (2016a), the
addition of spices can affect the color of fermented mushrooms;
product with the addition of onion were characterized by a lighter
color. This may be explained by the bleaching properties of onion.
Berna´
s and Jaworska (2015) reported that an aqueous onion ex-
tract inhibited enzymatic browning of Agaricus bisporus fruiting
bodies and had a beneficial effect on the color of mushrooms dur-
ing the 8-month frozen storage. Fermented mushrooms with the
addition of onion and other spices obtained significantly higher
notes in the 5-point sensory evaluation compared to fermented
mushrooms without spices. In addition to the color, taste and odor
were also better rated. The varied recipe did not affect the texture
of fermented mushrooms (Jabło´
nska-Ry´
s et al., 2016a).
Fermented oyster mushrooms were also subjected to color anal-
ysis. In this case, during 18 days of fermentation, a systematic
decrease in the value of the Lparameter was observed as well as
an increase in the values of the aand bparameters. As suggested
by the authors, the decrease in the Lparameter value representing
a shift toward darker coloration could be attributed to enzymatic
C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 9
Lacto-fermented edible mushrooms . . .
and nonenzymatic browning (Liu et al., 2016). In this study, the
sensory characteristics of fermented fungi were evaluated on a
10-point scale. Out of three types of Pleurotus spp., P. cornucopiae
obtained the highest scores for appearance, taste, texture, and gen-
eral acceptance.
Fermented fruiting bodies of Auricularia auricula were evaluated
according to a 7-point hedonic scale. All sensory results were
moderately acceptable, except for the texture. After 3 months
of preservation, significant changes were observed in the texture
and color of fermented fungi. The deter ioration may have been
associated with the storage method, as the finished products were
stored at room temperature (26 ±4°C) (Khaskheli et al., 2015).
In the study conducted by Joshi et al. (1996), fermented button
mushroom along with brine were successfully converted into sauce
with desirable physico-chemical characteristics, sensory qualities,
and shelf-life. A similar trend in using fermented fruiting bodies
of Termitomyces robustus is suggested by Bello and Akinyele (2007).
Threats resulting from this method of preservation
Microbial safety of fermented food. Due to their high moisture
and neutral pH, fresh mushroom fruiting bodies are an excellent
medium for microbial growth. Venturini et al. (2011) studied the
microbiological quality and safety of 22 species of cultivated and
wild mushrooms, including Agaricus bisporus and Pleurotus ostrea-
tus, that is, species that are most commonly used in investigations
of lactic fermentation of fungi. Microbial counts of mesophilic
microorganisms, Pseudomonas genus, Enterobacteriaceae family, lac-
tic acid bacteria, moulds and yeasts were investigated. The total
number of microorganisms ranged from 4.4 to 9.4 log cfu/g, and
no pathogens were isolated. Gram-negative bacteria, Pseudomonas
genus, and Enterobacteriaceae were the dominant microorganisms.
Lactic acid bacteria were present in low numbers. Their count
was below 2 log cfu/g in a majority of the analyzed species or
they were absent in many cases. The lowest amount of yeasts and
molds was detected in Agaricus bisporus fruiting bodies. Impor-
tantly, mushrooms intended for lactic fermentation are subjected
to short-term blanching treatment, which contributes to partial
reduction of microflora (Jarczyk & Płocharski, 2010).
Liu et al. (2016) and Zheng et al. (2018) subjected fermented
mushrooms to microbiological analysis for yeast content and Enter-
obacteriaceae. Yeasts and molds co-existed with lactic acid bacteria in
the process of fermentation. The content of yeast in the fermented
fungi was the highest on the fifth-sixth day of fermentation (the
15th day in the case of fungi pickled like kimchi, i.e., at 4 °C).
InthecaseofPleurotus eryngii, the number of yeasts decreased to
the initial level of 2.3 log cfu/g in all samples after 30 days of fer-
mentation. In products obtained from P. cornucopiae,P. sajor-caju,
and P. ostreatus after 18 days of fermentation, the number of yeast
was much higher, that is, about 6.5 log cfu/g, which was lower by
about 1 log cfu/g than the initial value.
Yeasts pose a significant threat of microbial spoilage of food, as
they can develop in low pH environments, high salt concentra-
tions, and low temperatures (Stratford 2006). The negative activity
of yeast in the lactic fermentation process may lead to an increase
in pH. Yeasts present in fermented vegetables can utilize sugars,
which should be fermented by bacteria to lactic acid. They can
also utilize organic acids as a carbon source, which reduces acidity
and creates conditions for the development of putrefactive bacte-
ria that cause spoilage (Franco & P´
erez-D´
ıaz, 2012; Satora, Celej,
Skotniczny, & Trojan, 2017).
During the fermentation process, Enterobacteriaceae may increase
the probability of product spoilage, especially in the initial period
when the pH of the product is still relatively high. At pH of
the environment above 5.0, the bacteria are able to utilize lactic
acid, produce propionic and acetic acids, and increase the pH of
the medium. These processes do not occur at pH 4.5 and below
(Franco & P´
erez-D´
ıaz, 2012).
As reported b Liu et al. (2016), the Enterobacteriaceae population
increased during the first 3 days of fermentation and then it signifi-
cantly decreased. No Enterobacteriaceae were detected in fermented
P. sajor-caju,P. ostreatus,andP. cornucopiae after15days.Inthecase
of P. e r y n g i i , the number of Enterobacteriaceae strongly depended
on the diversified fermentation process. For the sauerkraut-type
process, a transient increase in the Enterobacteriaceae count from
2.5 to 3.9 log cfu/g was noted after 1 day of fermentation. After
30 days of fermentation, this value dropped to 0.7 log cfu/g. For
the kimchi-type process, the highest content of Enterobacteriaceae
(3.3 log cfu/g) was observed on the fifth day of the experiment.
The number of bacteria after 30 days of fermentation decreased
in this case to about 1.3 log cfu/g. For the fermentation process,
there was no increase in the content of Enterobacteriaceae, and only
a rapid drop in its number to the final undetectable level was noted
after 5 days of fermentation. This satisfactory result was achieved
by adopting the preacidification procedure, where an initial addi-
tion of acetic acid made the brine pH drop to around 4.4 (Zheng
et al., 2018).
Microbiological tests were also carried out in the case of
naturally fermented fruiting bodies of Termitomyces robustus (Bello
& Akinyele, 2007). In finished products, a diversified microflora
was found, depending on the pre-treatment method. Pseudomonas
aeruginosa,P. capacia,Proteus vulgaris,andBacillus subtilis were
isolated from the untreated fermented sample, Bacillus licheniformis,
Aerococcus viridians,andLeuconostoc mesenteroides were detected in
the salted sample, and Staphylococcus aureus and Bacillus subtilis were
isolated from the blanched fermented sample. An increase in the
bacterial load was observed at 0 and 48 hr, while a decrease was
noticed at 72 hr of fermentation. All samples contained fungi.
Penicillium italicum,Aspergillus flavus,andPaecelomyces species
were isolated from the untreated fermented sample and Candida
albicans,Brachysporum nigrum,andAspergillus niger were detected in
the salt-treated sample. The blanched fermented sample contained
Penicillium italicum and Aspergillus flavus. It should be noted that
the finished fermented products were obtained through natural
fermentation, as the authors did not use starter cultures. Initiation
of fermentation through application of selected starter LAB
cultures ensures fast growth of desirable microflora, shortens the
fermentation process, and significantly reduces the risk of micro-
biological spoilage (Chabłowska, Piasecka-J´
o´
zwiak, Rozmierska,
& Szkudzi´
nska-Rzeszowiak, 2012; Di Cagno et al., 2013; Leroy &
De Vuyst, 2004). In the case of lactic fermentation of fungi, the use
of an autochthonic starter culture seems essential. Autochthonous
starters are those isolated from and reused on the same raw matrix
(Di Cagno et al., 2013). Endogenous strains of lactic acid bacteria
contained in the raw material are responsible for the characteristic
sensory quality of fermented products. Isolation and inclusion of
these strains in starter cultures intended for fermentation of raw
material of their origin ensure that the characteristic traditional
taste of the products is retained. The main criterion for the selec-
tion of such strains is their antagonistic activity against undesirable
bacterial and yeast species, which enhances the microbiological
safety of the finished product (Chabłowska et al., 2012).The
available literature provides no information on an autochthonous
starter culture dedicated specifically to lactic fermentation of
fungi.
10 Comprehensive Reviews in Food Science and Food Safety rVol. 0, 2019 C2019 Institute of Food Technologists®
Lacto-fermented edible mushrooms . . .
Nitrite accumulation. The accumulation of nitrite during veg-
etable fermentation is a common problem associated with food
safety. However, as presented in the research by Liu et al. (2016)
and Zheng et al. (2018), the level of nitrite in fermented mush-
rooms is relatively low and it does not pose a threat to the health
of the consumer. The process of fermentation can significantly re-
duce the nitrite content in the finished product. Liu et al. (2016)
observed a decrease in the content of these compounds from the
level of 3.14 to 4.46 mg/kg in fresh oyster mushrooms to the value
of 1.85 to 2.56 in oyster mushrooms subjected to 18-day lactic fer-
mentation with the participation of L. pentosus. As demonstrated
by Zheng et al. (2018), the nitrite content on the first days of
fermentation increased from 0.25 to 0.7–1.0 mg/kg depending
on the fermentation method; however, after 30 days of fermenta-
tion, it dropped to the initial level and it was the same as in the
control test, including salted fungi. According to the FAO/WHO
directive, the acceptable daily intake (ADI) of nitrites is 0.2 mg/kg
body weight; in an average 60 kg adult, the acceptable daily intake
of nitrite should not exceed 12 mg per person.
Biogenic amines. The presence of biogenic amines, namely pu-
trescine and cadaverine, was detected in fresh fruiting bodies of
fungi (Kalaˇ
c&K
ˇ
r´
ıˇ
zek, 1997; Yen, 1992). As demonstrated by
Kalaˇ
candK
ˇ
r´
ıˇ
zek (1997), freshly harvested fruiting bodies of Bo-
letus scaber contain over 70 mg of putrescine and nearly 7 mg of
cad aver ine in 100 g of average mass, and Boletus variegatus fruiting
bodies contain more than 40 mg of putrescine. Biogenic amines
can be formed in the microbial process of decarboxylation of
amino acids occurring during controlled or spontaneous fermen-
tation. No such studies have been carried out so far in the case
of fermented mushrooms. However, it is known that the use of
starter cultures with amine oxidase activity may contribute to re-
duction of biogenic amines in fermented products. This effect was
confirmed in studies carried out using Lactobacillus plantarum and
L. caseistrains (Fadda, Vignolo, & Oliver, 2001).
Lacto-Fermented Mushrooms as an Alternative to
Other Fungal Products
Lactic fermentation of mushrooms is certainly not a competitive
method for the two most popular methods of preservation of
this raw material, namely drying and freezing. Freezing potently
maintains the properties of fresh mushrooms; therefore, it is a way
of preserving recommended by authors in many studies. Frozen
mushrooms are often used as a half-finished product for the
preparation of other products, such as marinades. Dried mush-
rooms are also used as a half-finished product; additionally, due
to the possibility of using natural drying methods (sun-drying),
this technology can be cheap and is easily available. Sun-drying is
the cheapest and oldest method among various drying methods.
In some countries, the method is still popular, as it does not
require specialized equipment and energy expenditure and is
only dependent on climatic and weather conditions. Drying
mushrooms with this method usually proceeds at a temperature of
25 to 30 °C and lasts approximately 7 days (Muyanja et al., 2014).
Additionally, during the sunlight exposure, the content of vitamin
D2in mushrooms increases under the influence of UV-B radiation
and photoconversion of ergosterol (Ko, Lee, Lee, & Park, 2008;
Urbain, & Jakobsen, 2015; Urbain, Valverde, & Jakobsen, 2016).
As demonstrated by Rai and Arumuganathan (2008), mod-
ern methods of mushroom preservation, for example, canning
and freeze-drying, are usually expensive; therefore, such prod-
ucts are not popular in many regions of the world. In India and
China, salting (heavy salting with a salt concentration 20%)
is one of the most popular methods of preservation of fungi,
since this technique is easy, cheap, and generally available and
does not require advanced technologies (Rai & Arumuganathan,
2008; Zheng et al., 2018). Salted mushrooms are used as a half-
finished product for the production of other foods (marinades,
sterilized mushrooms, and mushrooms stewed in fat) after de-
salination. When the salt is removed in the multiple rinse pro-
cess, there are large losses of minerals and vitamins (Gapi´
nski &
Wo ´
zniak, 1991; Horubała & Wi´
sniewska, 1978). Lacto-fermented
mushrooms are a great alternative to salted mushrooms due to the
much lower salt content (Zheng et al., 2018). In addition, be-
cause of the easy and cheap technology, fermented foods play a
major role in the diet of numerous regions in Africa and Asia.
Traditional fermentation process still is as a substitute where re-
frigeration or other means are not available for the safekeeping of
food (Holzapfel, 2002).
An important and often used method of preserving mush-
rooms is preservation thereof in hermetically sealed vessels, that
is, making marinades and sterilized preserves. Button mushrooms,
chanterelles, king boletes, and red pine mushrooms are used for
the production of this type of preserves (Cos¸kuner & ¨
Ozdemir,
1997; Jaworska et al., 2008; Jaworska, G ˛
ebczy´
nski, & Gołyszny,
2003; Vivar-Quintana et al., 1999). Marinades from mushrooms
are fruiting bodies in sweet and salt-and-sour pickle, preserved
by pasteurization, while sterilized canned mushrooms are kept in
salt-sweet-and-sour brine, or only salted, and preserved by ster-
ilization. In the case of marinades, the acetic acid content in the
finished product is usually from 1.5% to even 4%. The fruiting
bodies of edible shiitake can be marinated in high concentra-
tions of acetic acid, up to 5% (Siwulski, Czerwi´
nska-Nowak, &
Sobieralski, 2007). In mushrooms subjected to lactic acid fermen-
tation, the major organic acid found in the highest amount is lactic
acid, whereas acetic acid is produced in small amounts of 0.74 to
0.92 mg/mL (Liu et al., 2016).
In the production of sterilized preserves, about 2% of sodium
chloride is added to the brine and sometimes citric acid, L-ascorbic
acid, and pyrosulfates are used as well (Cos¸kuner & ¨
Ozdemir, 1997,
2000; Jaworska et al., 2003). The fixing factor here is high tem-
perature, usually above 120 °C. Thermal treatment that takes place
during pasteurization of marinades or sterilization leads to reduc-
tion of nutrients and antioxidants (Barros et al., 2007; C¸ aglarlrmak
et al., 2001; Cos¸kuner & ¨
Ozdemir 1997). A major problem in
commercial production of pasteurized or sterilized canned mush-
rooms is the weight loss or shrinkage due to water evaporation
in the thermal preservation process. The losses vary from 35% to
40% and seriously affect the profitability of the production (Devece
et al., 1999; Rai & Arumuganathan, 2008).
Lacto-fermented mushrooms do not have to be additionally sub-
jected to the process of thermal fixation. In the technological pro-
cess of production, only brief blanching takes place. It has an im-
pact mainly on thermolabile components. In addition, fermented
mushrooms are characterized by the presence of a live microflora;
therefore, this product may potentially have probiotic properties,
especially if the fermentation process is carried out by a strain with
documented probiotic properties (Jabło´
nska-Ry´
s et al., 2016a).
Conclusions
Fermented food is produced and consumed all over the world,
and the most common type of fermentation is based on lactic
acid bacteria. Fermentation is one of the cheapest methods of
processing, yielding products with high durability without the use
C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 11
Lacto-fermented edible mushrooms . . .
of chemical preservatives or thermal preservation processes. Due
to the preliminary digestion by bacterial enzymes in fermented
products, it is possible to increase the content and bioavailability
of nutrients. At the same time, the fermentation process may
contribute to a reduction of the content of compounds with anti-
nutritive or even toxic effects. In 1998, the FAO recommended
that fermented food should be recognized as part of the cultural
heritage of each country and efforts should be made to maintain
this method of producing and preserving food. Certainly, this
should also be applied to the lactic fermentation of fruiting bodies
of edible mushrooms.
As shown by available studies, fungal raw material can be suc-
cessfully preserved via lactic acid fermentation and the finished
product can be an alternative to salted, marinated, or sterilized
mushrooms. There are many investigations on the improvement
of this conservation method, which focus mainly on technological
aspects. The research on the nutritional and health value of fer-
mented fungi is limited. It seems advisable to analyze the impact
of the fermentation process on the content of bioactive com-
pounds present in mushrooms. Greater emphasis should be placed
on the microbiological safety of the finished product; addition-
ally, there are no investigations of the content of biogenic amines.
Undoubtedly, an important trend in further research should be tar-
geted at acquisition of indigenous starter cultures (autochthonous
starters) dedicated specifically to mushroom fermentation, which
will ensure control of the fermentation process and production of
a standardized product, as is the case with other fermented food
products.
There is a need to conduct studies in this field, because mush-
rooms are undeniably a valuable source of nutrients and biologi-
cally active compounds with a “pro-health” and, possibly, healing
nature.
Acknowledgments
This research received no specific grant from any funding agency
in the public, commercial, or not-for-profit sectors. The authors
declare no conflict of interest.
Author Contributions
Ewa Jabło´
nska-Ry´
s collected the data, interpreted the results,
and drafted the manuscript. Aneta Sławi´
nska collected the data and
helped draft the manuscript. Katarzyna Skrzypczak and Wojciech
Radzki helped draft the manuscript. Waldemar Gustaw critically
revised the draft.
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C2019 Institute of Food Technologists®Vol. 0, 2019 rComprehensive Reviews in Food Science and Food Safety 15
... Images of the mushrooms are given in Figure 1. Fresh fruiting bodies were cleaned and boiled in water (1/1; mushroom mass by water volume) for 5 min with 3% salt (the concentration of salt was calculated from the fresh mushroom mass) [6]. After boiling, mushrooms were cooled to room temperature (22 ± 2 • C) and used for fermentation. ...
... Images of the mushrooms are given in Figure 1. Fresh fruiting bodies were cleaned and boiled in water (1/1; mushroom mass by water volume) for 5 min with 3% salt (the concentration of salt was calculated from the fresh mushroom mass) [6]. After boiling, mushrooms were cooled to room temperature (22 ± 2 °C) and used for fermentation. ...
... The darkening of the mushroom surface is mainly related to microbial contamination, enzymatic activity, or mechanical injuries [26]. Lactic acid fermentation influences the colour of mushrooms, and this is mainly related to pre-treatment procedures such as blanching [6]. According to Jabłońska-Ryś et al. [27], the stabilisation of the L* value and the reduction in the a* value could be observed during the LAB fermentation of mushrooms, while the b* value increases at every stage of this technological process (washing, blanching, and fermentation). ...
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... It is one of the oldest preservation methods widely used in many countries of the world, mainly in Africa and Asia and in Eastern European countries [1][2][3]. This method can be used to preserve raw materials of plant (vegetables, fruits, grains, herbs) and animal (milk, meat, fish) origin, as well as mushrooms [3][4][5][6]. The lactic fermentation process contributes to the extension of product shelf life, protection against the growth of undesirable microorganisms, improvement of nutritional values (enrichment with some vitamins, elimination of anti-nutritional compounds), increased digestibility, reduction of calorific value, and modification of the flavor of fermented raw materials [2,4,5]. ...
... Mushrooms do not undergo spontaneous fermentation readily [6], due to the blanching process that has to be applied to this raw material. Therefore, the use of starter cultures is necessary in this case; both autochthonous microflora, isolated from fresh raw material or material subjected to spontaneous lactic fermentation, and allochthonous microflora, isolated from other sources, can be used as starters in the fermentation process [9,10]. ...
... These results were similar to the findings reported in our previous studies [17] and those described by Skąpska et al. [26] in a study on mushrooms. The pH value in other fermented mushroom species has been reported to range from 3.3 to 4.6 and depends on, e.g., the fermentation temperature, the amount of available carbohydrates, or the additives used in the fermentation process [6]. As reported by Steinkraus [4], a pH value below 4.0 ensures stability of fermented vegetables with simultaneous maintenance of anaerobic conditions. ...
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The aim of the study was to assess changes in the basic quality parameters induced by controlled lactic fermentation of fruiting bodies of the button mushroom (Agaricus bisporus). Lactiplantibacillus plantarum 299v with documented probiotic properties and L. plantarum EK3, i.e., an isolate obtained from spontaneously fermented button mushrooms, were used as starter strains. The fruiting bodies of fresh, blanched, and fermented mushrooms were analyzed at different stages of the lactic fermentation process. The content of free sugars (high-performance liquid chromatography with charged aerosol detector method; HPLC-CAD) and organic acids (high-performance liquid chromatography with diode array detector method; HPLC-DAD) was determined both in the mushroom fruiting bodies and in the brine. Five free sugars (ribose, trehalose, sucrose, glucose, and fructose), mannitol, and six organic acids (lactic, malic, succinic, citric, acetic, and fumaric acids) were detected in the samples. Lactic acid dominated in the final products. The starter cultures exhibited varying degrees of utilization of available mushroom sugars and sucrose used as an additional substrate. Sucrose was utilized at a higher rate and in greater amounts by the L. plantarum EK3 isolate. This starter culture was characterized by a significantly higher final amount of produced lactic acid, a lower pH value, and higher numbers of LAB (lactic acid bacteria). These important quality parameters largely determine the stability of fermented products. Based on the analysis results and the high scores in the organoleptic evaluation of the fermented mushrooms, the L. plantarum EK3 isolate can be recommended as an appropriate starter culture for lactic fermentation of mushroom fruiting bodies.
... An increasing knowledge of how mushrooms grow has led to the cultivation of over 90 species (Boa, 2004), of which around 30 are grown commercially for food and consumed widely (Chang & Miles, 2004). The remaining cultivated species are grown for medicinal purposes (Lu, Lou, Hu, Liu, & Chen, 2020;Ma et al., 2018;Roncero-Ramos & Delgado-Andrade, 2017;Yang, Belwal, Devkota, Li, & Luo, 2019), as functional foods (Jabłońska-Ryś, Skrzypczak, Sławińska, Radzki, & Gustaw, 2019;Reis, Martins, Vasconcelos, Morales, & Ferreira, 2017) and extracts used as food additives (Hadar & Dosoretz, 1991;Sun et al., 2020). ...
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Background Few studies to date have evaluated the use of Lactobacillus and Bifidobacterium in edible fungus fermentation. To obtain a fermented Lentinus edodes (L. edodes) liquid product with good taste and effects, a strain with good fermentation performance from 9 tested strains was selected, and the physicochemical properties and antioxidant capacity of the resulting product were evaluated. Results Lactobacillus fermentum 21828 exhibited adhesion, tolerance to low pH and bile salts, and good fermentation performance. The number of viable bacteria was 1.05×10⁸ CFU mL ⁻¹, and the extraction rate of crude polysaccharide from L. edodes was 2.79% after fermentation. The effects of fermentation on the contents and composition of nutrients in L. edodes liquid were marked, with changes in total soluble protein, total soluble sugar, total acid, and total phenol levels. The DPPH (2,2-diphenyl-1-picrylhydrazyl) radical-scavenging rate in the fermentation liquid was 93.01%, which was significantly higher than that in non-fermented liquid (80.33%). Furthermore, analysis of volatile and 5′-nucleotide contents showed that fermentation altered the flavor of the product, whereas sensory evaluation showed that the fermented product was preferred. Conclusion Our study demonstrated that the fermented Lentinus edodes liquid exhibited better nutritional and functional properties as well as sensory characteristics, compared to unfermented. This article is protected by copyright. All rights reserved.
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The present study aimed to demonstrate Lentinus (formerly Pleurotus) sajor-caju (PSC) as a good source of pro-health substances. It has also shown that supplementation of its culture medium with cow milk may further improve its beneficial properties. Intracellular fractions from fungi grown on a medium supplemented with cow milk were analyzed using various biochemical methods for determination of the nutrient composition. Furthermore, anti-cancer properties of selected extracts were investigated on colorectal cancer cell lines (HT-29, LS 180, and SW948) in vitro. Biochemical analysis showed enrichment in health-enhancing compounds, such as proteins or polysaccharides (about 3.5- and 4.5-fold increase in concentration of proteins and carbohydratesin extracts of mycelia cultured on whole milk (PSC2-I), respectively), with a decrease in the level of free radicals (10-fold decrease in extract grown on milk and medium mixture (1:1) (PSC3-II)), which was related to increased catalase and superoxide dismutase activity (7.5-fold increase in catalase activity and 5-fold in SOD activity in PSC3-II compared to the control). Moreover, the viability of the cancer cells was diminished (to 60.0 ± 6.8% and 40.0 ± 8.6% of the control, on HT-29 and SW948 cells, respectively), along with pro-apoptotic (to 18.8 ± 11.8 and 14.7 ± 8.0% towards LS 180 and SW948 cells, respectively) and NO-secreting effects (about 2-fold increase) of the extracts. This study suggests that PSC has multiple nutritional and anti-cancer properties and can be used as a source of healthy biomolecules in modern medicine or functional foods.
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Mushrooms are universally valued for their dietary and therapeutic significance. Their importance could be attributed to numerous nutritive and dietary substances including polysaccharides, terpenoids, phenolics and other light molecular bioactive compounds. These compounds offer optimal health benefits and have been identified as a potential source of nutritional and medicinal products against several debilitating and food-related disorders. Here, we present an updated synopsis of the medicinal attributes of mushrooms, while also highlighting the technological advancements in their cultivation that have led to the birth of engineered species with improved traits that could alleviate malnourishment and contribute towards food security, offer health benefits, and provide efficient ways of waste management.
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Sauerkraut is a commonly consumed product in Poland. It is still traditionally produced using spontaneous fermentation by indigenous microorganisms colonizing cabbage leaves, mainly lactic acid bacteria. During fermentation, yeasts may also become active and their negative activity can cause pH to increase and spoilage bacteria to develop. The objective of the research study was to identify the yeast microbiota in sauerkraut produced industrially and by spontaneous fermentation in the farms in the region of Muszyna. The microorganisms were isolated using WL agar with 0.1 g/l of chloramphenicol added, and the isolates were differentiated by RAPD-PCR fingerprinting with an M13 starter and identified by sequencing the ITS region. The largest amount of yeasts was found in the sauerkraut samples produced using traditional methods in the farms located in the Muszyna commune (2.3 ÷ 15.9·10³ CFU/g) and in one commercial product (2.8·10³ CFU/g). In other commercial sauerkraut products analyzed, no yeast was found. Among the isolates, the representatives of two species: Cryptococcus macerans and Debaryomyces hansenii were identified; the second one was differentiated by RAPD-PCR into 3 different profiles. The identified microorganisms present were highly dependent on the sample under analysis; this could be linked with the production technology of sauerkraut and, also, with the variety of raw material used. The occurrence of the identified yeast species in the final product can cause the shelf-life of sauerkraut to diminish and the signs of its spoilage to appear. © 2018, Polskie Towarzystwo Technologow Zywnosci Wydawnictwo Naukowe PTTZ. All rights reserved.
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Mushrooms are perishable foods; they required processing technologies that preserves chemical and nutritional characteristics of fresh forms. The principal objective of this research was to analyze the physicochemical changes and sensory properties of Shiitake pickles with and without mustard oil in order to contribute to the diversification of food. The antioxidant activity of fresh shiitake mushroom pickles with and without mustard oil demonstrated a significant result in Scavenging free radicals except for DDPH.The pH of MOVS and SWVS was reduced to 3.92±010 and 2.80±0.26 over time during 20 days of storage and the acidity was gradually increased for up to storage. However HPLC analysis of both pickles revealed the presence of four acids were present in the MOVS pickle (malic acid at 4.354 with the retention time of 4.2 minutes). The second peak indicates lactic acid at 5.069 with the retention time of 4.3 min. The third peak indicates citric acid at 5.489 with the retention time of 4.5 min. The fourth peak indicates succinic acid at 7.301 with the retention time of 6.8min. Whereas the SWVS pickle showed the peak for three acids present in the pickle sample, where the first peak indicates malic acid at 4.303 with the retention time of 4.2 min, the second peak indicates acetic acid acid at 6.573 with the retention time of 6.2 min, and the final peak was found of succinic acid at 7.304 with the retention time of 6.8 min. The pickle formulated with (MOVS) showed 5.70 for overall acceptability of pickle.
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Mushroom has already been known as a good source of proteins,carbohydrates and some vitamins. It is then the objective of this research to find out the effect of oyster mushroom (Pleurotus ostreatus) powder addition on yoghurt fermentation. The resulting yoghurt product will be monitor by measuring its total lactic acids, acidity (pH), lactic acidbacteria (LAB) count, and the organoleptic properties, including colour, taste, flavour and texture. The mushroom were dried and grinded into powder up to 200 mashes, continued with its addition in yoghurt making process. Mushroom powder concentrations of 0%, 0.5%, 1%, and 1.5% were added on the milk to be fermented. The result showed that mushroom powder addition resulting in increase lactic acid concentration, reduced its acidity, and increased LAB viability. Based on the lactic acid counts, acidity, and LAB viability, a concentration of 1.5% powder addition is the optimal concentration for fermentation, but the product is not preferred by the panelists. The addition of 1% mushroom powder resulting in increased yoghurt quality, and the preferred yoghurt product by most of the panelists. It is then proven that the addition of mushroom powder will increase yoghurt quality and public acceptance.
Book
Since the publication of the first edition, important developments have emerged in modern mushroom biology and world mushroom production and products. The relationship of mushrooms with human welfare and the environment, medicinal properties of mushrooms, and the global marketing value of mushrooms and their products have all garnered great attention, identifying the need for an updated, authoritative reference. Mushrooms: Cultivation, Nutritional Value, Medicinal Effect, and Environmental Impact, Second Edition presents the latest cultivation and biotechnological advances that contribute to the modernization of mushroom farming and the mushroom industry. It describes the individual steps of the complex mushroom cultivation process, along with comprehensive coverage of mushroom breeding, efficient cultivation practices, nutritional value, medicinal utility, and environmental impact. Maintaining the format, organization, and focus of the previous edition, this thoroughly revised edition includes the most recent research findings and many new references. It features new chapters on medicinal mushrooms and the effects of pests and diseases on mushroom cultivation. There are also updated chapters on specific edible mushrooms, and an expanded chapter on technology and mushrooms. Rather than providing an encyclopedic review, this book emphasizes worldwide trends and developments in mushroom biology from an international perspective. It takes an interdisciplinary approach that will appeal to industrial and medical mycologists, mushroom growers, botanists, plant pathologists, and professionals and scientists in related fields. This book illustrates that mushroom cultivation has and will continue to have a positive global impact on long-term food nutrition, health care, environmental conservation and regeneration, and economic and social change.
Chapter
This chapter reviews various aspects related to fermentation and pickling of vegetables. Fermentation can be accomplished using one of three processes: spontaneous fermentation, back-slopping, or inoculation with the use of selected starter cultures. A variety of groups of microorganisms (Lactobacilli, Leuconostoc, Pediococci) are frequently used in fermented foods. Lactic acid bacteria and yeasts have been reported to be dominant in the fermentation of vegetables. Acidified vegetables are nonfermented products produced by the addition of an acid, commonly acetic acid, as an acidulant. At concentrations of 3.6% or above, acetic acidacidified foods can be preserved without the addition of any other antimicrobial agents or the use of heat treatments. Innovations in food biotechnology play an important role in improving both the nutritional features and, possibly, enhancing the sensory quality. Smoothies are an example of this trend to increase the consumption of vegetables and fruits, as an alternative and/or a complement to fresh products.
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Eleven species of wild mushrooms which belong to Boletaceae and Russulaceae families were examined by gas chromatography (GC) and gas chromatography–mass spectrometry (GC-MS) analysis for the presence of fatty acids. As far as we know, the fatty acid profiles of B. purpureus and B. rhodoxanthus were described for the first time. Twenty-six fatty acids were determined. Linoleic (19.5 – 72%), oleic (0.11 – 64%), palmitic (5.9 – 22%) and stearic acids (0.81 – 57%) were present in the highest contents. In all samples, unsaturated fatty acids dominate. Agglomerative hierarchical clustering was used to display the correlation between the fatty acids and their relationships with the mushroom species. Based on the fatty acids profile in the samples, the mushrooms can be divided into two families: Boletaceae and Russulaceae families, using cluster analysis. This article is protected by copyright. All rights reserved.
Chapter
Edible, medicinal, and wild mushrooms are the three major components of the global mushroom industry. World production of cultivated, edible mushrooms has increased more than 30-fold since 1978. China is the main producer of cultivated, edible mushrooms. Lentinus edodes is now the world's leading cultivated edible mushroom with about 22% of the world's supply. Lentinula and four other genera (Pleurotus, Auricularia, Agaricus, and Flammulina) account for 85% of the world's total supply of cultivated edible mushrooms. Beginning in about 1997, China became the world's largest producer of Flammulina velutipes. On average, consumers now enjoy about 5 kg of mushrooms per person per year. Per capita consumption is expected to continue to increase as consumers become more aware of the healthful benefits of incorporating mushrooms in their diet. Much more research is needed on the bioactive components in mushrooms to determine their biological responses in humans.
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Three typical lactic acid fermentation processes (i.e., sauerkraut, pickling, and kimchi) were used via inoculation with the starter culture of Lactobacillus plantarum, for the purpose of preserving King Oyster Mushrooms (Pleurotus eryngii). Notable differences were observed in chemical composition between King Oyster Mushrooms and common vegetable plants. Despite this, LAB still quickly colonized the fruit body of King Oyster Mushroom, and rapidly controlled the spoilage and pathogenic microorganisms. The final fermented products contained high population of LAB (>7 Log cfu/g). In addition, the concentrations of nitrite in final fermented products were lower than the current maximum allowable levels (<20 mg/kg) in China. These results indicated that it is effective and safe to preserve King Oyster Mushroom by the method of lactic acid fermentation. It is concluded that for long‐term preservation of mushrooms the inoculated lactic‐acid‐fermentation method is better than the age‐old heavy‐salting method. Practical applications Heavy salting (salt concentration ≥20%) is currently the most viable method to preserve the perishable mushroom in cultivation factories. However, to further make edible products from this salted mushroom, the excess salt must be washed out of the salted mushroom and discarded as waste. Disposal of such waste has become a costly problem for a mushroom‐cultivation company. To reduce the amount of brine waste released into the environment, introducing of lactic acid fermentation in preservation of surplus mushroom would be a good alternative for these mushroom‐cultivation companies. The present study aims to assess the safety and preservation effects of the three different fermentation processes for King Oyster Mushroom. The relevant results will help those technicians to choose the adequate fermentation methods in preservation of mushroom and also be helpful to reduce the brine sewage pollution caused by the preservation process of heavy salting.
Article
In order to explore a better method to process the fruiting body of Tricholoma lobayense. Through the determination of proximate compositions, total soluble protein, sugar content, amino acids composition and 5'-nucleotides content, the effects of thermal processing on the nutritional compositions and non-volatile flavor components of the fruiting body of Tricholoma lobayense were evaluated. Our study showed that the level of the proximate compositions, total soluble protein and sugar content in Tricholoma lobayense, reduced except the total phenolics during cooking. Amino acids composition analysis illustrated that the boiling raised total free amino acids content, but microwaving indicated an opposite effect. Boiling and microwaving could considerably raise the total 5'-nucleotides content. Microwaving reduced the EUC (Equivalent umami concentration) while boiling raised EUC. Both boiling and microwaving significantly raised the bio-accessibility of soluble sugar and protein but boiling was almost doubling that of control. All results suggested that boiling method could effectively preserve the nutritional characteristics of Tricholoma lobayense, and make Tricholoma lobayense more delicious and easier to be digested compared with microwaving.