Abstract
Mushrooms are a great source of nutritionally valuable compounds, including proteins, lipids, polysaccharides, polyphenols, micronutrients and vitamins. In particular, they are a significant dietary source of B group vitamins and can be an ideal vehicle in order to supply these vitamins for vegetarians. Conventional extraction methods usually involve water or organic solvents and may results in the noticeable degradation of components. This review describes the potential use of the novel non-conventional methods including enzyme-assisted extraction, pulsed electric fields, ultrasounds, microwaves, subcritical and supercritical fluid extraction for recovery of valuable compounds from mushrooms. Recent studies have shown the great potential of these environmentally friendly methods for green production of specific compounds for use as nutraceuticals or as ingredients for functional foods.
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Introduction
Mushrooms have been part of human diet for thousands of years, and recently their consumption is increasing around the world [1, 2]. Over the last years, they have been used as source of food additives for human nutrition, nutraceuticals, and nutritional supplements as they are a good source of valuable compounds with high nutritional properties. Most of these bioactive compounds have demonstrated the potential for the treatment and prevention of human diseases, mainly attributed to their antioxidant properties [3]. They can efficiently interact with proteins, DNA, and other biological molecules to produce a desired outcome, which could be exploited for designing natural products-derived therapeutic agents [4].
One of the main problems to obtain nutritionally valuable compounds from mushrooms in energy-efficiently and economically sustainable way is the difficulty to release them from their complex matrix and intracellular location, avoiding the use of large amounts of solvent and long extraction time. Conventional methods usually involve water or organic solvent for extraction depending on the target compound and their end use. However, these techniques are time consuming and may result in the degradation and coagulation of valuable compounds that can be found in mushrooms. Moreover, organic solvent extraction involves the use of high cost solvents (i.e., ethanol). To avoid these limitations, the different non-conventional methods of extraction assisted by enzymes, pulsed electric fields (PEF), ultrasound, microwaves, and using of subcritical and supercritical fluids were recently developed.
This review focused on the present developments in application of the modern non-conventional techniques to recover nutritionally valuable compounds from mushrooms.
Mushroom Structure and Nutritional Profile
There are about 10,000 known types of mushrooms around the world. They can be divided in different categories and the most commonly used are the edible mushrooms. The edible mushrooms have no poisonous effects, display the desirable taste and aroma and have rich content of valuable compounds. The short information about the most commonly used edible mushrooms is presented in Table 1.
Different mushrooms can provide a significant content of nutritionally valuable compounds including proteins, lipids, polysaccharides, microelement vitamins, and some important bioactive compounds (i.e., polyphenols) [5–7]. Figure 1 shows an example of a typical fungal cell and the location of some important compounds inside it. The structure of a fungal cell is similar to the structure of a plant cell. However, a fungal cell wall contains no chloroplasts inside the cell.
Table 2 presents macronutrients (proteins, carbohydrates, lipids) and amino acid profile (fresh weight basis) of some mushroom species [8, 9].
The content of macronutrients is ≈1.8–7.4 g/100 g for proteins, ≈4.5–6.3 g/100 g for carbohydrates and ≈0.2–1.7 g/100 g for lipids. The contents of the overall fatty acids and vitamins found in mushroom species are presented in Table 3 [10–13] and Table 4 [5, 7, 14–19], respectively.
Techniques of Extraction
Short Information on Conventional Methods
Traditionally, solvent-assisted extraction of valuable components has been used to recover valuable compounds from mushrooms [20, 21]. For instance, water extraction is a widely employed technique as it is an economic method, and does not requires any special equipment. However, water extraction requires high temperatures (T = 50–80 °C) [22, 23] and long treatment times (t = 1.5–5 h) [23, 24], thus favoring the degradation of valuable thermolabile compounds that can be found in mushrooms.
On the other hand, hydroalcoholic extractions have been also widely used for the recovery of high-added value compounds from mushrooms. This technique requires a moderate temperature (T = 25–60 °C). However, it needs long treatment times (t = 1–24 h) and high concentrations of solvents (from 30 to 98.6 %) [23, 24]. Moreover, hydroalcoholic extraction involves the use of high cost solvents (i.e., ethanol) and it is difficult to recycle the remaining residues.
Conventional organic solvent extraction using chloroform–methanol 2:1 (v/v), maceration (soaking), percolation, countercurrent extraction, pressurized liquid extraction, and Soxhlet have been used to extract nutritionally valuable compounds from plant materials [25]. However, conventional extraction techniques usually imply the use of large amounts of solvents, and the risk of thermal degradation (over 100 °C) or transformation of molecules of interest remains important [25]. At this stage of development, there is an increased interest for food industry to find different technologies that can improve valuable compounds extraction from mushrooms in a sustainable way.
Novel Extraction Methods
Enzyme-Assisted Extraction
Enzyme-assisted extraction is a non-conventional methodology that offers the possibility of processing with lower temperature, rather short time, less energy consumption and high extraction yield in the food industry.
The cell walls of some mushrooms (shiitake mushroom) are mainly composed of the polysaccharides chitin (β-1,4-N-acetylglucosamine) and glucans (β-1,3 and β-1,6), which can be degraded by hydrolytic enzymes containing either chitinase or glucanase activity [26]. Hence, enzymes involved in the breaking of bonds between the polymers in fungal cell walls could be used for the intensification of the extraction. For example, a multicomponent carbohydrase preparation originating from Trichoderma harzianum has been used for the extraction of the bioactive compound eritadenine [27]. Eritadenine (a purine alkaloid) is a cholesterol reducing agent in shiitake mushrooms. An enzyme mixture composed of various α- and β-glucanases, but also some side activities like chitinases and proteases was used. This enzyme mixture showed a fairly high activity at pH 4.8 and 50 °C. Results showed that pre-treatment of mushrooms with hydrolytic enzymes before methanolic extraction resulted in an insignificant increase in the amount of eritadenine released. These results indicated the potential for delivery of therapeutic amounts of eritadenine from the ingestion of extracts or dried concentrates of shiitake mushroom strains.
Other enzymes (cellulase, pectinase, protease) can also hydrolyze the cellulose, pectin and crude protein, and break down the cell walls. Enzyme-assisted extraction technology of polysaccharides was performed for the extraction of polysaccharides from Ganoderma lucidum [28]. The optimal extraction conditions were shown as follows: complex enzyme (cellulase/pectinase/protease) amount of 3 %, extraction temperature at 45 °C, extraction time of 3 h, and extraction at pH 7. Under these conditions, the experimental amount of extract was 8.9 %, and the polysaccharides yield was 1.1 %. Another study has shown the positive effect of enzyme by comparing this technology to microwave- and hot water boiling-assisted extraction [29]. The extraction effect of a mixture of cellulase/pectinase/protease (1/1/1, w/w/w) on the polysaccharide content from Clitocybe maxima stipe was compared and optimized (hydrolysis and extraction conducted for 96 min at 47 °C and pH 4.64). Results showed that the extraction yield and the polysaccharide amount were significantly different: 5.86 and 40.23 % for hot water extraction, 9.4 and 52.62 % for microwave-assisted extraction, 10.26 and 53.13 % for enzyme-hydrolysis extraction, respectively. Another interesting point to note is the reduced required time (96 min) with enzyme and the highest extract purity (53.1 %) as compared to the other extraction methods.
Pulsed Electric Fields (PEF)
Over the last years, the use of pulsed electric fields (PEF) has been shown to be promising for intracellular extraction from plant food materials [30–36], by-products [37–40], and bio-suspensions [41–43] mainly due to its ability to cause lethal damage to cells or induce sub-lethal stress by transient permeabilization of cell membranes and electrophoretic movement of charged species between cellular compartments.
The cell electroporation theory is based on the concept of transmembrane potential. Numerous experimental data prove that the cytoplasm always has a negative electric potential [the entire cytoplasmic anion producing the electric potential (φ c) unlike the electric potential of the intercellular space (φ e)]. This physiological potential (natural) µ ph = φ c–φ e ≈ 0.1 V, influences the transport of ions and small molecules. Thus, the cell has a transmembrane electric potential and a ζ-potential (zeta potential) at the electric double layer between the external liquid and the solid surface.
For a spherical cell an applied pulsed electric field E (V/cm) generates a time-dependent transmembrane potential (TMP) u m (t), with a rise time τ [43]:
where α = 0.75 is a constant (in general case the value of α value depends on the shape of the cell, e.g., α = 1 for a rectangular cell), f is a parameter that depends on geometrical and electrical properties of a cell, d c is a cell diameter (for the plant cells d c ≈ 20–100 μm [44]), θ (rad) is the angle between a point of interest on the membrane surface and the electric field direction, and Δu m (V) is a physiological potential of a cell.
The rise time τ can be evaluated as [45]:
where C m is the specific capacity of the membrane (the different estimations give C m ≈ 3.5–3.9 µF/cm2 [46], C m ≈ 0.1–3 µF/cm2 [47], C m ≈ 0.95 µF/cm2 [48], C m ≈ 0.2–0.4 µF/cm2 [49]), σ c is the electrical conductivity of the cell (the different estimations give σ c ≈ 0.1–1 S/m [47], σ c ≈ 0.5 S/m [48], σ c ≈ 0.05–0.5 S/m [49]).
Finally the parameter f can be evaluated as [44]:
where σ e is the electrical conductivity of intracellular compartments (≈10−3–10−4 S/m [49]), σ m is the electrical conductivity of the membrane (the different estimations give σ m ≈ 10−4–10−6 S/m [44], σ m ≈ 10−10–10−6 S/m [49]), and d m is the membrane thickness (≈5–10 nm) [44].
The cell permeabilization or disintegration index Z can be quantified by measuring the electrical conductivity of the tissue using the following equation [31]:
where σ is the electrical conductivity at time t (S/m), σ i is the electrical conductivity of the intact tissue (S/m), and σ d is the electrical conductivity of the completely damaged tissue (S/m). The application of this equation gives Z = 0 for an intact tissue and Z = 1 for a completely damaged tissue.
The value of Z can be used for characterization of the recovery of intracellular compounds such as bioactive compounds, as they are located in different cell substructures, and their extraction is highly dependent of cell damage.
An example of typical pulsed electric field system is represented in Fig. 2. It is mainly composed of three parts: a pulse generator, a treatment chamber, and a pumping system to handle the product. The system is generally controlled and monitored by an oscilloscope and a computer. The pulse generator is running basically on DC high voltage associated with a pulse forming unit and, occasionally, a pulse transformer to increase the voltage. The treatment chamber contains basically two electrodes (high voltage and ground) separated by insulating material. Direct current electric pulses of high voltages (up to 40 kV) for a very short time (<10 ms) allow the extraction of selectively high-added value compounds from complex matrices without degrading the material [50]. Two configurations are usually used: a batch system or continuous flow mode. The gap fixed between the electrodes reflects the intensity of the electric fields (most often below 10 kV/cm) applied to the material being processed. When performing PEF-assisted extraction experiments, not only the electric field strength, the pulse width and the repetition rate are being controlled, but also the number of pulses, the treatment time; consisting of multiplying the number of pulses by the pulse width, expressed in µs or ms, and finally the total specific energy (kJ/kg), which is generally below 20 kJ/kg [51]. The total specific energy depends mainly on the applied voltage, the treatment time, and the resistance of the treatment chamber. Several other parameters influence the PEF-assisted extraction efficiency. In fact, besides the PEF processing parameters, the extraction medium (temperature, pH, solvent type and concentration) and the physicochemical properties of the treated matrix (product size, electric conductivity, cell structure and membrane characteristics) being the most influencing [31, 51]. Moreover, the cell location (cytoplasm or vacuoles) of the targeted molecules being extracted influences the electropermeabilization procedure [50].
The impact of PEF alone and/or combined with other methodologies on the recovery of valuable compounds from mushrooms has been evaluated by different authors. For instance, the effects of PEF-assisted extraction to recover exopolysaccharides (EPS) from Tibetan spiritual mushrooms were evaluated [52]. The authors found that PEF treatment significantly enhanced EPS recovery. Moreover, it was found that under the optimal conditions (electric field intensity E = 40 kV/cm, number of pulses n = 8 and pH 7), the EPS extraction yield was increased by 84.3 %.
The efficiency of PEF-, microwave- and ultrasonic-assisted methods was compared for extraction of active components from Chinese mushroom Jew’s ear [53]. These extracts have anti-coagulant effects and are applied in a Chinese herbal medicine. Highest yield of fungal polysaccharide with anti-coagulant activity was observed for PEF-assisted technique at field strength of 24 kV/cm.
In a different study, the effects of PEF (100–1000 V/cm) alone and/or combination with pressure for proteins, polyphenols and polysaccharide’s recovery from mushrooms (Agaricus bisporus) were recently investigated [54]. Pressure extraction (PE) was done using the laboratory-pressing cell, equipped with a PEF treatment system. Figure 3 shows the example of the pressing curve for electric field strength of 800 V/cm. For conventional pressure extraction without application of PEF, the maximum yield of extract was Y PE ≈ 0.26. The PEF-assisted extraction gave the highest yield of extract, Y PE+PEF ≈ 0.42 ± 0.01 [54, 55].
Moreover, the results were compared with hot water extraction (WE, 70 °C, 2 h) and ethanol extraction (EE, 25 °C, 24 h). The method of WE gave relatively high contents of proteins, total polyphenols and polysaccharides. However, the extracts were cloudy and their colloid stability was low. This method did not allow preservation of the fresh protein quality, and the proteins were presumably in the coagulated state. The extracts produced using EE method were also cloudy and unstable.
These authors concluded that at temperature T = 343 K the relative extraction, A/A m, of valuable compounds from mushrooms after applying PEF can be explained by the first-order kinetic law [54]:
Here, A represents the absorbance of the extract (1/10 dilution, λ = 260 nm) at time t, A m corresponds to the maximum absorbance of extract, obtained at long time of extraction (t ≈ 2 h) and τ e is the characteristic time of extraction.
PEF-assisted pressure extraction gave clear extracts with high colloid stability. It was concluded that PEF was a suitable technology for the recovery of valuable compounds in the used conditions, because PEF increased the selective extraction of nutritionally valuable compounds mainly due to cell permeabilization obtaining clear extracts with high colloidal stability, thus facilitating the separation and the purification processes after extraction in comparison with conventional hot water and ethanol extraction. Moreover, it was found that the combination of PEF with pressure extraction gave higher nucleic acid/proteins ratio as compared with that of pressure extraction alone. In addition, PE + PEF allowed production of mushroom extracts with high contents of fresh-like proteins and polysaccharides.
Ultrasound-Assisted Extraction (UAE)
Ultrasound-assisted extraction (UAE) has attracted much interest in recent years due to their many advantages in the recovery of valuable compounds from different matrices compared to conventional extraction methods [56–58]. In the ultrasonic process, mushroom cells are disrupted by shock waves from cavitation bubbles, thus facilitating mass transfer hence an absolute increase in the extraction yield and kinetics. In addition, the recovery of valuable compounds from plant food materials assisted by ultrasounds is an inexpensive and simple method [59]. This technique can be combined with solvents and allows to decrease the extraction time and the temperature of the extraction, which can be a potential tool for the preservation of thermolabile compounds [59].
UAE has been widely used by several authors to extract nutritionally valuable compounds from mushrooms [60–63]. Table 5 summarizes some studies applying UAE to extract high-added value components from mushrooms.
In this line, it was revealed that pulsed countercurrent ultrasound-assisted extraction demonstrated the best extraction yield with significant short time (40 min less), higher yield of polysaccharides (1.5 % more) at 16:1 liquid–solid ratio at lower temperature (30 °C lower) than hot water extraction [61]. In addition, introduction of ultrasonic probe and concurrency increased the mass transfer and effective contact surface between solid and liquid therefore a better yield than those by normal ultrasonic extraction was observed [61]. In another study, it was indicated that UAE promoted the extraction of bigger molecules like polysaccharides from mushroom compared with those from hot water extraction (52–129 % increase) [62]. Response surface methodology was used to optimize the UAE of polysaccharides from Trametes orientalis [60]. Even though positive indication was shown by using UAE, most of these studies generalized the application power of ultrasound without discussing about the power density and adsorbed power during the extraction which are essential parameters to monitor UAE process [58, 64].
In another study, the optimal UAE conditions to recover polysaccharides from black fungus were studied. It was concluded that ultrasounds treatment at 350 W, solid–liquid ratio 1/5, and 35 min of extraction time at 90 °C allowed to obtain the maximum polysaccharide yield [65]. Moreover, the recovery of polysaccharides from A. bisporus mushrooms was also studied. The optimal conditions to extract the maximum polysaccharide content from this type of mushroom using UAE were ultrasonic power 230 W, at T = 70 °C for t = 62 min [66]. At these conditions, a highest A. bisporus polysaccharides yield of 6.02 % was achieved. It was also indicated that extracted polysaccharides have good antioxidant activity, e.g., at 250 μg/ml concentration, mushroom polysaccharides were observed to possess significantly higher (86.1 %) free radical-scavenging activity when compared to reference. The effect of ultrasound-assisted extraction on melanin recovery from dried fruit bodies of Auricularia auricula (A. auricula) was evaluated [67]. The optimal conditions were obtained following ultrasound power 250 W, T = 63 °C, a liquid–solid ratio of 43 ml/g and a duration of 36 min. Under these conditions, two extractions sufficiently reached the maximal melanin yield (120.05 mg/100 g). Moreover, in another study, it was also determined the proximate composition, total phenolic compounds, antioxidant capacity and antimicrobial activities of different extracts of Laetiporus sulphureus [68]. Optimum extraction methodologies (classical and ultrasound-assisted) provided one fraction containing neutral and polar lipids and the other fraction containing fungal carotenoids and pigments. Fatty acid analysis indicated a predominant level of polyunsaturated fatty acids followed by saturated and mono-unsaturated fatty acids. Both the aqueous methanolic and water extracts contained higher TPC and showed better antioxidant capacity than the ethanolic extract. Irrespective of the type of extraction applied, L. sulphureus showed good antimicrobial activity against all the tested bacteria and fungi, being in some cases stronger than the used antibiotics and mycotics.
Microwave-Assisted Extraction (MAE)
Microwave-assisted extraction (MAE) is a process that includes heating the material causing moisture to evaporate, which generates tremendous pressure and the rupture of cells facilitating the release of the desired intracellular contents [58]. The electromagnetic spectrum of microwave ranges between far infrared light and radio frequencies. The frequency range is situated from 300 MHz to 300 GHz, corresponding to 1 m–1 cm wavelength range. For industrial and scientific microwave heating, 915 ± 25, 2450 ± 13, 5800 ± 75 and 22,125 ± 125 MHz, are the most applied frequencies [69]. The heating effect of microwaves is mainly associated with the dielectric properties of materials. Two parameters: the dielectric constant and the dielectric loss defined these properties. The ability of a molecule to be polarized by the electric field is symbolized by ε, namely the former. When processing at low frequencies, the maximum amount of energy is stored by the material and given by ε. The efficiency of converting the electromagnetic radiation energy into heat is measured by the dielectric loss ε′. When the dielectric constant decreases, the dielectric loss increases [70]. The ratio between the dielectric loss and dielectric constant represents the dissipation factor symbolized by tan δ.
Materials that are transparent to microwave energy have an infinite penetration, whereas reflective ones (e.g., metals) have a zero penetration. The half-power depth is considered as one of the efficient ways to characterize penetration. This parameter characterizes the distance at which the power density is reduced to the half from the sample surface and varies not only with the sample’s dielectric properties but also slightly with the inverse of the square root of the frequency. The power absorption is then given by the Lambert’s expression described in Eq. (6).
In this equation, P 0 and P represent the incident power and the power at the penetration depth, respectively. α′ and d represent the attenuation factor and the penetration depth, respectively [69].
Depending on the electric field strength’s local time-average and the dielectric properties, the dissipated power in a medium is given by Eq. (7) [71].
where ε 0 represents the permittivity of the free space (8.85 × 10−12 F/m), and ε″ represents the imaginary part of the relative permittivity or ‘loss factor’. P, f, |E|rms, and V represent the power (W), the frequency (Hz), the root-mean-square electric field (V/m), and the volume (m3), respectively.
Fundamental difference hence exists between conventional heating and microwave. In fact, the heat transfer is occurring differently; from the heating device to the medium in conventional heating, and by dissipation inside the irradiated medium in microwave heating. The Fourier heat equation contains thus an extra term, reflecting this difference, given by Eq. (8) [71].
where ρ, C P, κ, T and t represent the specific density (kg/m), specific heat capacity (J/kg/K), thermal conductivity (W/m/K), temperature (K), and time (s), respectively.
Microwaves heat up the molecules by ionic conduction and dipole rotation. If the extraction medium offers a resistance to the ion migration, a friction is generated and the minute microscopic traces of moisture occurring in the sample are heated. This process generates tremendous pressure on the cell wall until rupture and release of active compounds from the sample. In this case heating occurs only in a selective and targeted material; consequently, there is no heat release into the environment [72–74]. This technique, widely used in the extraction of bioactive compounds, provides a rapid sample preparation with reduced amounts of solvent.
There are several studies which have shown the higher efficiency of MAE to recover nutritionally valuable compounds from mushrooms in comparison with other conventional technologies [75]. Table 6 summarizes most of the performed studies [29, 75–83].
MAE showed obvious advantages of high extraction efficiency from Terfezia boudieri Chatin, Boletus edulis, and Lactarius volemus with lower solvent consumption in terms of high antioxidant capacity/activity of extracts achieved within the shortest time [75]. Authors found that methanol concentration ≈80 %, extraction temperature 80 °C, and extraction time ≈5 min were the optimal extraction conditions. They found that high contents of phenolic and flavonoid compounds were the major contributors to the observed high antioxidant activities of these extracts.
In another study, it was shown that microwave-based DNA extraction method for subsequent DNA amplifications by PCR on mushrooms of different Agaricomycetes requires tiny amounts of fungal material, is rapid and achieved within minutes [84], that is why MAE is superior to classical extraction methods which are work intensive and require larger amounts of starting material and hours of time for performance [84]. In addition, specific expensive and hazardous chemicals for cell lysis and DNA purification were utilized for conventional extraction. The authors showed that microwave method with highest reliability (≈90 %) was suitable for vegetative mycelium harvested from fresh and also from aged fungal cultures. Another author utilized MAE technique for isolating the fungal metabolite ergosterol from mushrooms (A. bisporus) [76]. It was found that MAE-derived ergosterol values were comparable to those obtained by classical solvent extraction and significantly exceeded those obtained by supercritical fluid extraction (SFE). However, MAE procedure is simple, rapid, reliable, and economical with respect to amounts of reagents required, especially when compared with classical solvent and SFE.
On the other hand, nine kinds of mushrooms including Hazel, Slippery, Shiitake, Hericium erinaceu, Citrinopileatus, Flammulina, Comatus, Tricholoma giganteum, and Xian mushrooms were used for MAE nicotine extraction [83]. They found that the optimal high-throughput dynamic microwave-assisted extraction (HTDMAE) conditions were as follows: the extraction solvent was water, the microwave power was 1000 W, the extraction solvent volume was 18 ml, and the extraction solvent flow rate was 2 ml/min. It was found that under optimal conditions of HTDMAE, nicotine yield was 34.9 μg/kg; which was 1.29 times higher than that obtained for solvent extraction and even 1.14 times higher than for pressurized microwave-assisted extraction. The extraction effect on the polysaccharide of C. maxima stipe was compared, and the extraction conditions were optimized [30]. With three of the above mentioned mushrooms, the extraction yield and the polysaccharide amount were greatly different, which were 5.86 and 40.23 % for hot water extraction, 9.4 and 52.62 % for microware-assisted extraction, 10.26 and 53.13 % for complex–enzyme–hydrolysis extraction, respectively.
Microwave-assisted extraction technique has been employed for the extraction of polysaccharides from Agaricus blazei Murrill [77]. The optimum conditions for a 12.35 % recovery were: 29.37 min extraction time, 400 W microwave power, 74.64 °C extraction temperature and 32.7:1 ratio of water to material. In the case of Cordyceps militaris, the optimal conditions to obtain the highest polysaccharide yield were a microwave power of 744.8 W for 4.2 min and a ratio of solution to solid of 31.1 ml/g [78]. Similarly, three polysaccharide fractions were separated from Lycoris aurea [79]. The microwaves technique can be hyphenated with ultrasound-assisted extraction in order to reduce the extraction time, increase the efficiency and save the energy. The experimental results confirmed that ultrasonic/microwave-assisted extraction (UMAE) of polysaccharides had great potential and efficiency compared with traditional hot water extraction. This coupled method was employed for the separation of polysaccharides from Lycium barbarum at the following optimized operating conditions: microwave power of 500 W for 10 min and ultrasonication for 30 min at 50 °C and pH 9 [80].
In the case of polysaccharides from G. lucidum, the optimal extraction conditions were 50 W ultrasonic power, 284 W microwave power, 701 s extraction time and 11.6:1 water/solid ratio [81]. Using this coupled method, the yield of polysaccharides could be significantly improved compared with that of classical hot water extraction, reaching nearly 100 % yield, and increased by 27.7 % compared to ultrasound-assisted extraction. Polysaccharides were also separated from Inonotus obliquus by microwave and ultrasound-assisted extraction at 90 W microwave power with 40 kHz ultrasonic frequency, and 1:20 (w/v) solid–water ratio for 19 min [82]. Under these conditions, the recovery and purity of polysaccharides were 3.25 and 73.16 %, respectively, which are above those of traditional hot water extraction.
Besides the degradation risks caused by traditional water extraction, this method requires high-energy demands compared to heating by microwaves [85]. In fact, it has been reported that coupling conventional method such as hydrodistillation with microwaves, leads to the reduction in the energy cost by almost twofold compared to hydrodistillation alone; decreasing thus from 0.12 kWh/kg (430 kJ/kg, $6/t) to 0.07 kWh/kg (270 kJ/kg, $3.5/t) [86].
Moreover, microwave heat transfer is much faster than conventional one, as it is not limited to thermal conduction or convection currents, and the maximum temperature is only dependent on the rate of heat loss and power applied [71].
Subcritical and Supercritical fluid Extraction
In recent decades, both subcritical and supercritical fluid extraction techniques have emerged as useful tools to replace conventional extraction methods. These techniques are considered environmentally friendly and have the potential to provide higher extraction yields of nutritionally valuable compounds from different sources, including mushrooms compared to classic extractions [87].
Subcritical Water Extraction (SWE)
SWE, also referred as hot pressurized water extraction, is a technique that consists in using hot water (from 100 to 374 °C, the latter being the water critical temperature) under high pressure to maintain water in the liquid state. The most important factor to consider in this type of extraction procedure is the variability of the dielectric constant with temperature [55]. At low temperature, compounds with high polarity easily solute in water while super-heated water (above 100 °C) can act as organic solvent and solute lower polar compounds [88].
Figure 4 illustrates the semi-continuous prototype SWE apparatus to extract hydrophilic compounds from G. lucidum, adapted from Askin et al. [89]. Table 7 summarizes the results of application of SWE technique for the extraction of nutritionally valuable compounds from mushrooms [89–93].
The impact of temperatures (100–300 °C), and extraction apparatuses (batch and semi-continuous) on extracting polysaccharides from G. lucidum was investigated [89]. The authors suggested that the optimal temperature for extracting water-soluble polysaccharides was 200 °C at which up to three times more of soluble content was extracted in batch system and up to nine times more in the semi-continuous system [89]. In another work, subcritical water extraction was used to recover bioactive compounds from golden oyster mushroom with high temperatures (50–300 °C) and different pressures (0.002–5 MPa) and it was revealed that extracts possessed higher antioxidant activities when higher temperatures (250–300 °C) and longer times were used. Moreover, the effects of subcritical water to recover antioxidant compounds from medicinal mushroom Chaga mushroom (I. obliquus) under similar conditions to the above mentioned were also studied [91]. The authors obtained the highest antioxidant activities when SWE was applied under 250 °C.
SWE application on mushroom remains untapped. Studies so far mostly focused on extracting phenolic and polysaccharides from mushroom by SWE. However, the success of extracting essential oils from herbs by subcritical water [94] might also indicate that compounds with low polarity (i.e., fatty acids) from mushroom by subcritical water is worthy of investigating. In addition, the modeling kinetics between pressure/temperature of SWE and bioactive compounds are also interesting to study because manipulation of pressure and temperature indicates the change of water polarity, which might to different extraction outcomes.
The suitability of pressurized water extraction (PWE) of crude polysaccharides as secondary metabolites from Lentinula edodes was investigated [95]. A series of experiments were carried out to examine the effects of extraction times and pressures. The results indicated that the maximum recovery of polysaccharides was about 90 % of the crude polysaccharides from mycelia pellets when the pressure was at 10.1 MPa for 70 min (28 °C). This was a drastic improvement over that of boiling water extraction (BWE) at 0.1 MPa for 40 min, which gave only 27.9 % recovery. A nitroblue tetrazolium (NBT) reduction assay was used to examine the macrophage stimulating activities (MSA), and it was found that the PWE polysaccharides retained the MSA. The morphology of the macrophage cells treated by PWE polysaccharides was also examined and found to be similar to that of the positive control lipopolysaccharides treated. Finally, gel chromatographic and NMR experiments revealed that both PWE and BWE polysaccharides showed the presence of four similar molecular mass components and the α-(1 → 4)-d-Glcp and β-(1 → 6)-d-Glcp linkage residues. The improved PWE efficiency is probably due to the possibility that under high pressure, the solid polysaccharide’s hydrogen binding is partially destroyed to increase structure elasticity and water solubility [95].
On the other hand, the impact of subcritical carbon dioxide extraction on the extraction of fatty acids from B. edulis mushroom was investigated [96]. It was found that this method could improve the extraction yields of fatty acids as compared to conventional extraction methods.
Supercritical Fluid Extraction (SFE)
A supercritical fluid is any substance that is at a temperature and pressure above its critical point, where distinct liquid and gas phases do not exist. At these conditions, some fluid properties are placed between those of a gas and those of a liquid. Although the density of a supercritical fluid is similar to a liquid and its viscosity is similar to a gas, its diffusivity is intermediate between the two states, thus favoring the extraction of intracellular compounds. The diffusivity D could be calculated using the mathematical model developed by Goto et al. [97], and adapted by Mhemdi et al. [98]. The proposed model allows the estimation of the effective diffusivity D e from the experimental data on the time dependence of extraction ratio Y(t), using the simplified exponential model given by Eq. (9) [98].
where r is a radius of solid particles, the effective diffusivity D e can be easily obtained from fitting the plot of ln(1 − Y(t)) versus 15 t/r.
SFE has been used for several applications during the last decades, especially important has been its use in food and agricultural as well as fuel industries, followed by analysis/chromatography, pharmaceuticals, environmental contaminants, metal-ion extractions and pesticides. And, the last two decades have acquired a special relevancy for the extraction of nutritionally valuable compounds such as from different sources, including mushrooms. Figure 5 was adapted from [55] who briefly illustrated the set-up of a pilot plant scale SFE using CO2 and co-solvents in the extraction. Since under critical condition, CO2 supercritical fluid has low solubility that indicates low polarity, co-solvent extraction with organic solvents can diversify the polarities of solvents thus giving more extraction selections.
In the early development of introducing SFE-CO2 to extract compounds from mushroom, SFE-CO2 was reported to be used in order to quickly and easily prepare samples from A. bisporus for profiling carboxylic and fatty acids [99].
Recently, most of the published studies investigated the different supercritical conditions (pressure, temperature and solvents) and also compared the results with those obtained from traditional extractions, such as Soxhlet and maceration (Table 7) [100, 101]. To evaluate the performance of extraction methods, antioxidant activities, chemical compositions (i.e., fatty acid) and extraction yields are studied on mushroom. SFE did not necessarily retain the highest desirable properties in the mushroom extraction and traditional extractions (Soxhlet, ethanol, or ethyl acetate) showed better results (Table 7).
In addition, co-solvent SFE (ethanol-CO2) could enhance hydrophilic antioxidants but reduce the yield of fatty acid because of the increase in polarity in the extraction fluid [101]. In another study, the effects of supercritical carbon dioxide extraction on the recovery of fatty acids from B. edulis mushroom were evaluated [96]. It was observed that fatty acid yields were augmented when pressure and extraction time increased. The authors also found a selective extraction of linoleic acid in the extracts obtained by supercritical carbon dioxide.
The prophylactic effect of CO2, considered as an “inert” fluid for food processing, has often been reported in literature as one of the major benefits when it is used in its supercritical form, especially, when processing oxygen sensitive compounds. The application of supercritical CO2 for such processes has been contrasted with the apparition of subcritical and supercritical water. This fluid, especially in its supercritical form, was applied in a wide range of applications, such as a medium for both organic [102] and inorganic [103] synthesis reactions, for the production of functional monomers from biomass [104], and for the conversion and destruction of either chemical wastes or toxic compounds [105].
SWE allows thus both extraction and reaction modes, when processing under specific conditions. However, although commonly considering CO2 in both liquid and supercritical forms as unreactive media, it represents a potent catalytic medium, mainly due to the conducting hydrolytic-based reaction chemistry. Due to the presence of water in agricultural products, even in traces, this phenomenon is usually occurring, facilitating thus the equilibrium of carbonic acids [106] and a hydronium ion for acid-based catalysis.
The occurring reactions in subcritical water have been well described and reviewed in literature [107]. As reported, the role of subcritical and supercritical water depends on the type of application; it could therefore be used to alter selectively the composition of the extract, to obtain polymeric moiety and functional monomers from polymers, to enhance a polymerization reaction, or to produce mixtures for fermentation through depolymerized products degradation.
SWE and supercritical CO2 are known to contribute and facilitate the formation of Maillard reaction products, as flavor precursors during food processing. Additionally, the hydrolysis in water of biopolymers leads to the generation of polyphenolic or flavonoid moieties, enhancing thus the food characteristics. For example, lignin could be treated using gas-expanded solvents to produce vanillin [108].
All of these phenomena occurring during the extraction of valuable compounds from agricultural products, depend on their thermal stability and the susceptibility of their conversion (e.g., polymer hydrolysis in aqueous media) to other products. Such competition is then occurring between the selective extraction process and its conversion to another compound by temperature and/or hydrolysis, even if the kinetics associated with the reaction are very slow or barely detectable. To describe this competitive situation, a model has been proposed by Duan [109], in which the time dependence of solute solid-phase concentration C Si is given in the differential form by Eq. (10) [109].
Here, k pi represents the solute mass transfer being extracted from the solid phase, a p is the specific surface area of the solid, m i represents the thermodynamic distribution coefficient, and C ti is the solute concentration in the solid phase at time t. The differential equation describing the solute concentration mass balance C Li as a function of time in the liquid phase is given by Eq. (11) [71].
where ρ L and ρ S represent the density of the liquid and solid phases, respectively. F represents the water to solid mass ratio, and K Di is the constant of the degradation rate for the ith component.
In conclusion, SWE and SFE both present the possibility of clean chemical process to extract bioactive compounds from mushroom. Depending on characteristics of target compounds, researchers could change the solubility and polarity of extraction solvent by altering pressure, temperature, extraction solvent components, and extraction time.
Benefits and Limitations of Non-conventional Assisted Extraction Methodologies
Replacing the burdensome solvents (i.e., hexane, acetonitrile, methanol, dichloromethane, and toluene), used for long time in the extraction processes and the recovery of high-added value compounds, with green solvents such as CO2, ethanol, and water is undoubtedly one of the challenges in both food and nutraceutical sector. Non-conventional methods are mainly devoted to such solvent replacement as well as the decrease in temperature and treatment time compared to conventional methods. Some of the technologies reviewed here are mature enough and already used at industrial scale (i.e., PEF); others (i.e., HVED) require more research developments, but, in any case, it is important that new steps be taken to help build a more rational use of our natural resources.
PEF treatment is one of the main non-conventional processes used in food and nutraceutical industries. The success of this process is related to its continuous operability associated with the very short treatment times. These features make it a suitable and an easy process to be adapted, in a sustainable way, to the integrated processes including pre-treatments, extractions, reactions, and transformations. By permeabilizing the cell membranes at relatively low temperatures, PEF treatment is a useful tool to protect thermolabile compounds from degradation. Furthermore, it is highly selective and allows the release of soluble intracellular matter, whereas application of solvents is needed for conventional methods, requiring further purification steps. Finally, PEF treatment increases the shelf life and preserves the product quality and freshness. However, the major concern for commercialization of PEF technology is the relatively high installation cost for industrial processes. Besides this point, the applicability of PEF process is highly dependent to the electrical conductivity of the treated product, making the process relatively complicated and requiring numerous pre-treatment processes (i.e., washing, centrifugation, etc.), especially for salty solutions. Furthermore, PEF technology showed limitations on solid and particulate food treatment and was mainly applied for pumpable foods.
The application of HVED is based on the phenomenon of electrical breakdown in water. Water vapor bubbles that are initially present in the solution or formed due to local heating are involved in this phenomenon and accelerate the process. HVED pre-treatment, causing even small cell damage, has shown high yield of extracted proteins from plant matrices, without quality degradation. This green extraction technique allows the recovery of nutritionally and high-added value compounds at low energy input compared to other non-conventional techniques (i.e., PEF, US, and MAE), as well as the reduction in the required diffusion temperature, the extraction time, and the amount of solvent. However, the HVED application for selective extraction of intracellular compounds showed limitations compared to PEF. Additionally, HVED treatment involves usually the fragmentation of the plant matrix and the release of small particles, requiring additional purification steps. Like PEF treatment, HVED presents applicability limitations with high solution’s conductivity. Finally, up to now, no industrial scale application of HVED treatment was reported, requiring thus more deep researches.
UAE is an alternative affordable, effective, reproducible, simple and cheap method for the improved recovery of nutritionally valuable compounds (yields and kinetics) from different vegetal matters. This technique can be used alone and/or combined with conventional extraction method, and it requires low capital cost. Moreover, this methodology can reduce the temperature, thus being a potential alternative to preserve thermolabile compounds. In addition, can minimize solvent consumption, allowing the use of green solvents. However, one of the main limitations of UAE is that its effects are highly dependent of the matters and the presence of a disperse phase, which can promote the wave attenuation and thus reducing the effectiveness of this method.
On the other hand, MAE also allows improving the extraction yield of intracellular valuable compounds, decreasing the extraction time, and the solvent consumption compared to conventional methodologies. By contrast, the application of microwaves can have a negative impact in thermolabile compounds associated with microwave heating. Moreover, the polarity of compounds and solvent play an important role, thus difficulting the recovery of non-polar target compounds. In addition, the development of microwave equipment at large scale can require high investment costs.
The use of supercritical fluids for the extraction and recovery of high-added value compounds result as well in a “clean” extract when compared to other conventional extraction techniques. This technique leads obtaining highly purified extracts without residual organic solvents and interfering compounds extracted from the matrix. In spite of the potential of SFE technique, its usefulness could be related to the properties of the compound to be extracted from the matrix used. Furthermore, low polarity compounds are well extracted using SFE, considering especially the low polarity of supercritical CO2. It is also notable that mild pressures and temperatures, lead obtaining volatile compounds without affecting their properties, allowing thus their direct analysis when coupled with chromatographic equipment. Usually, the most used techniques are gas chromatography (GC) or supercritical fluid chromatography (SFC). One of the limitations related to the use of SFE technique concerns that targeted polar compounds require conceiving other strategies for their extraction (i.e., using co-solvents). Moreover, the industrial applications are still limited by the high amounts of supercritical fluids required, which is in most of the cases being recycled.
Patents and Commercial Applications
Asian countries have been studying on extracting bioactive compounds from mushrooms for a long time. For example, in the Global Patent Search Network database (gpsn.uspto.gov), 6884 results from 1985 to 2012 released by the State Intellectual Property Office (SIPO) of the People’s Republic of China were shown when searching with key word “mushroom extract”. In comparison, there were only 138 results when searching the same key word within the US patent database (patft.uspto.gov) since 1976.
Traditionally, mushroom extract patents usually used hot water extraction, solvent extraction, dialysis, and gel filtration to extract and purify bioactive compounds from mushrooms. Figure 6 illustrated the procedures of extracting dietary fiber, lentinan, and lentysine from Shiitake mushroom, adapted from [110]. The similar procedure was also described by others. For example, Zhuang et al. [111] obtained glycoprotein by soaking Grifola frondosa in hot water (100–120 °C) and ethanol before subjecting the resultant supernatant to dialysis. Similar extraction method was conducted to yield bioactive compounds with 100–2000 molecular weight from A. blazei Murill fruit bodies for suppressing breast cancer [112].
Using non-conventional methods to extract mushroom, however, was reported in only a few patents (Table 8) [113–115].
Non-conventional methods claimed to have the advantage of replacing hot water and alkaline extractions while shortening the extraction time [114]. By employing supercritical fluid extraction, about 37 % w/w of oleaginous substances were yielded and the compounds were later proven to be of positive effects on improving skin conditions [113–115]. MAE extracted 3 % of 100–800 kDa polysaccharides from Portebella mushroom in 4–5 min [113]. In addition, ionic liquid extraction method was recently introduced to extract lentinan from 11 mushrooms, which was not found in any other publication yet [114].
Under CFR §21 (Code of Federal Regulations Title 21) in US Food and Drug Administration (FDA) database, only canned mushrooms are regulated. Regarding to fresh mushroom, Pennsylvania State University and the American Mushroom Institute developed Mushroom Good Agricultural Practice Programs to better guide mushroom growing, harvesting and shipping to meet food safety standards [116]. However, guideline of applying mushroom extract in food or nutraceutical products remains unclarified in the USA. On the other hand, Europe Commission categorizes mushrooms as novel food ingredients defined as “food ingredients that have not been used for human consumption to a significant degree in the EU before May 15, 1997.” For example, in order to get approval under EU novel food category, Shiitake mushroom extract GlycaNovaTM was requested additionally substantial evidences to prove its safety for consumption as food ingredient [117]. The case to some extent indicates that the application of mushroom extracts as food ingredients in EU has more restriction rules.
Overall, most of the current patents use conventional extraction methods to extract bioactive compounds. Abundant patents have also proven the healthy effects of mushroom extracts. However, non-conventional extraction methods were only reported in several patents. In addition, regulation on mushroom and mushroom extracts in Western countries remains relatively unclear and under developed. More studies on toxicology of nutritionally valuable compounds from mushroom should be conducted.
Concluding Remarks
This review focuses on various technologies used for the extraction of bioactive compounds from mushrooms. Moreover, it provides a bird eye view on critical extraction parameters for maximum recovery of bioactive compounds. Overall, non-conventional cell disruption technologies may allow the extraction of nutritionally valuable compounds from mushrooms from an economical and environmental sustainable point of view. There is a need to develop a database to establish the optimum conditions to extract specific compounds with the appropriate technology and each mushroom family should be studied separately. Moreover, there is a need to study what compounds are better extracted and the nutritional quality of them. Some challenges must be addressed before non-conventional techniques become a reliable option for extractions, and they include production cost, scalability, and safety.
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The authors appreciate the support from the COST Action TD1104307 (EP4Bio2Med-European network for development of electroporation-based technologies and treatments).
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Roselló-Soto, E., Parniakov, O., Deng, Q. et al. Application of Non-conventional Extraction Methods: Toward a Sustainable and Green Production of Valuable Compounds from Mushrooms. Food Eng Rev 8, 214–234 (2016). https://doi.org/10.1007/s12393-015-9131-1
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DOI: https://doi.org/10.1007/s12393-015-9131-1