Mushroom Supplementation in Promoting Health and Performance of Poultry: Review

3.1. Nutrient Composition and Functional Components of Mushrooms

The constituents of commonly used mushrooms in the poultry rations are presented in Table 1. The highest crude protein (23.0%) and the lowest crude fiber (7.8%) have been reported in the fermented mycelium of Flammulina velutipes mushroom, followed by Pleurotus ostreatus powder. In another study conducted to evaluate the constituents of nine mushroom species, the crude protein content ranged from 16.47% in P. eryngii to 36.96% in P. ostreatus (black oyster) [ 25]. The presence of higher crude protein content in Flammulina velutipes mushrooms suggests its potential to be used as a protein source feed ingredient. Most of the mushroom preparations had CP content higher than maize grain (8.5%) [ 26], which is the most commonly used conventional feed ingredient in poultry rations. The value for crude fiber was higher in the stalk part of Flammulina velutipes (Table 1). Some findings have also shown high levels of dietary fibre (24.47–46.62%) [ 25]. With respect to energy content, mushrooms have been reported to be low calorific values [ 27]. The ether extract value ranged from 1.5 percent in the stalk waste of Flammulina velutipes to 3.8 percent in the waster medium of Cordyceps militaris mushroom. The variability in the nutrient composition could be attributed to the differences in strain, substrate development stage [ 28], climatic condition, and part of the mushroom used. Vargas-Sánchez et al. [ 29] reported about 3.9 and 7.9 g kg ^-1 of lysine and methionine, respectively, in Pleurotus ostreatus mushroom powder. Eun-Ju et al. [ 30] have reported about 4.1, 5.1 and 0.3 g kg ^-1 of lysine, cysteine and methionine in ethanolic extracted Lentinula edodes mushrooms, respectively. Consumption of mushrooms helps in obtaining all amino acids considered to be essential for simple stomached animals’ nutrition like chickens [ 25]. Pathania et al. [ 31] reported that mushrooms are also rich in vitamin B12 and folic acid, which are uncommon in vegetables.

In addition to the proximate constituents of mushrooms, different functional or active components are found in mushrooms fruiting bodies and mycelium [ 35]. The major functional components of mushrooms with their mode of action on broiler and layer chickens are summarized in Table 2. The beta-glucan is the main polysaccharide and bioactive component in medicinal mushrooms. It is recognized as potent immunological stimulators in animal cells, and the contents of β-glucan ranged from 1.58 to 16.91 mg g ^-1 of dry matter among the nine edible mushrooms [ 25]. It has also been reported that different medicinal mushrooms are rich in phenolic compounds, especially phenolic acid, which is the major naturally occurring antioxidant component found in mushrooms to help improve the antioxidant status of chickens [ 36].

3.2. Effects on Gut Health and Immunity

Experiments using different types and forms of mushrooms on gut health and immunity of broiler and layer chickens produced promising results. Mahfuz et al. [ 24] reported that winter Flammulina velutipes (Fig. 1) stalk helps to control pathogenic bacteria as well as increased beneficial bacteria in the cecum to keep sound gut health in layer chickens. Willis et al. [ 41] have shown that broiler chickens receiving Lentinula edodes extract had a significant increase in the population of bifidobacteria in the fecal samples than the control (no additive). Similarly, dietary spent mushroom (Cordyceps militaris) substrate resulted in significantly higher numbers of lactobacillus spp., and Bifidobacterium in the cecum and decreased numbers of Clostridium spp., Coliforms, and E.coli compared to the control group [ 42]. Supplementation of broiler chicken’s diets with Reishi, Ganoderma lucidum, Fungus Myceliated Grain (FMG) at 5% level of inclusion had significantly more oocysts shed in the fecal droppings at 49 days of age than any other treatment [ 20]. The observed improvement in the intestinal health of chickens is attributed due to the presence of biologically active compounds such as fibre, glucans, phenols, and other active ingredients in mushrooms [ 18, 43].

Results from Mahfuz et al. [ 24] suggested that supple- mentation of Flammulina velutipes mushrooms (3-5%) in laying hens' diet decreased the count of pathogenic bacteria ( Clostridium spp., Coliforms, and E.coli and increased that of beneficial ones ( Lactobacillus spp. and Bifidobacterium). These strong antimicrobial effects of mushrooms might be due to the ability to change cell membranes and cause ion leakage, thus making microbes less virulent [ 44]. In another study, Mahfuz et al. [ 19] demonstrated that feeding F. velutipes mushroom stalk waste at 2% level can be an effective way of improving the immunity in broilers. It has also been demonstrated that broilers experimentally challenged with Eimeria were more responsive to treatment with mushroom FMG than those who obtained a natural infection [ 45]. A trial conducted [ 46] using Eimeria-infected chickens showed that mushroom extract-fed group showed a significant development of gastrointestinal tract (GIT) compared with the non-fed group. Polysaccharides from medicinal mushrooms generally do have bioactive effects, and hence, these polysaccharide extracts might increase the activity of intestinal microflora and fermentation end-products such as volatile fatty acids (VFA) and increased proliferation of GIT [ 38]. According to Muthusamy et al. [ 47], the polysaccharides, especially ß-glucan substances, extracted from mushrooms had significant immune stimulatory functions in broiler chickens. A significant higher antibody response against Newcastle disease and infectious bursal disease was noted in Flammulina velutipes mushroom stalk waste fed broiler chickens and concluded that feeding. Velutipes stalk waste at a 2% level can be an effective way of improving the immunity in broilers Mahfuz et al. [ 19]. According to Abou-Zeid et al. [ 18], Pleurotus ostreatus mushrooms could be safely used in broiler feeding as natural feed additives at 2 g kg ^-1 diet with superior effects on their immune response.

3.3. Effects on Broiler Performance

Most findings highlighted the positive growth performances of broilers supplemented with various forms of mushrooms. Polysaccharide extracts of two mushrooms ( Lentinus edodes and Tremella fuciformis) inclusion prompted the growth performance, feed intake and feed conversion ratio of broiler chickens compared to the control group, but were not significantly different from those fed with antibiotic treatment group (20 mg kg ^-1, virginiamycin (VRG) [ 38]. Giannenas et al. [ 37] have also found increased performance of broiler chickens fed with 10 and 20 g kg ^-1 of an edible Agaricus bisporus. In a study with Japanese quails, Asadi- Dizaji et al. [ 32] found that supplementation with mushroom ( Agaricus. bisporus) at 2% significantly increased (p<0.05) weight gain and feed intake compared to the control. The possible mechanisms regarding mushrooms include changes in the intestinal microbiota, increased nutrient digestibility, increased feed intake and absorption, enhanced nitrogen absorption, improved immune response, and antioxidant activity [ 48]. In another study conducted to evaluate the feeding of four medicinal mushrooms via fungus myceliated grain (FMG), reduced performance was observed in broiler chickens fed Reishi ( Ganoderma lucidum) and Oyster ( Pleurotus ostreatus) FMG supplemented diets compared with those fed diets supplemented with Lentinus edodes FMG [ 20]. Dietary inclusion of five levels (0, 0.5, 1.0, 1.5, and 2.0 g kg ^-1 of diet) of edible mushroom powder ( Agaricus bisporus) positively affected broiler weight gain and feed conversion ratio [ 49]. According to Abou-Zeid et al. [ 18], Pleurotus ostreatus mushrooms could be safely used in broiler feeding as natural feed additives at 2g kg ^-1 diet with superior effects on their productive performance.

An increase in daily body weight gain of broilers fed with Agaricus bisporus mushroom was also noted by Guimarães et al. [ 50]. Daneshmand et al. [ 51] however found negative effects following administration of oyster mushroom powder (2 g kg ^-1) in male broiler chickens. It has also been documented that dried P. ostreatus (oyster mushroom) waste at 1% negatively affected body weight gain and feed conversion ratio of broiler chickens should be added (a feed additive for broiler chickens, which might be due to the high fibre contents in the mushroom additive) [ 52]. Replacement of Pleurotus ostreatus-colonized substrate in standard diet (100-200g kg ^-1) of broiler chickens has been found to be effective for improving body weight, feed intake and feed conversion ratio [ 53]. It has been reported that the improved growth and feed utilization efficiency of birds supplemented with natural materials is due to their appetite and digestion stimulating properties [ 54-56]. No significant differences were observed in daily body weight gain, feed intake, and feed conversion ratio when F. velutipes mushroom stalk waste was incorporated at 1 and 2% in broiler rations [ 19]. In another experiment, Agaricus bisporus mushroom powder and flavophospholipol inclusion, as individual factors, produced positive effect on weight gain and feed conversion ratio of broiler chickens [ 50]. The observed variation between results on broilers growth performance could be attributed to the difference in the type of mushroom species used, forms offered (powder, extracts, leftover, etc.), supplement dose, and may partly be due to the difference in the type of broiler breeds under investigation.

3.4. Effects on Laying Performance and Egg Quality Traits

Unlike broiler chickens, studies are limited regarding the effects of feeding different forms of mushrooms on laying performance and egg quality parameters. Hwang et al. [ 57] reported that dietary supplementation with shiitake ( Lentinula edodes) mushroom powder up to 0.5% positively affects egg production, egg quality, and fatty acid composition of eggs. It was observed that feeding F. velutipes mycelium had no adverse effects on egg production percentage, feed intake, and feed conversion ratio in laying hens, but the egg weight was found greater (p < 0.05) in the 1% and 3% mushroom-fed groups than the control diets [ 32].

Recently, Karaalp et al. [ 22] evaluated the effects of supplementing apple cider vinegar (ACV) and feed mushroom ( Agaricus bisporus) stalk separately and in combination on performance and certain egg characteristics. Their study found a lack of significant effect of dietary treatments on any performance criteria, and physical external and external egg quality characteristics. Another study by Yoshida et al. [ 58] demonstrated that supplementation of fermented mushroom bed ( Flammulina velutipes) in a laying hen diet (3%) improved egg production and decreased damaged eggs due to broken/ soft shells by one-sixth than the control group, which might be associated with the potentials of mushroom in reducing stress conditions. Hens fed dietary spent mushroom ( Cordyceps militaris) substrate had higher egg weight and feed conversion ratio than non-supplemented group (p<0.05), but hen-day egg production and feed intake were not affected by treatment groups [ 42, 59]. Kim et al. [ 60] also reported a lack of difference in egg production, egg mass, egg weight, feed conversion ratio, feed intake, and most internal and external egg quality parameters, but significantly heavy egg yolks were reported for laying hens fed fermented spent mushroom( Hypsizygus marmoreus) substrate in corn-soy based experimental diet. It has also been observed that the inclusion of the dried edible portions of the fruiting body of Cordyceps militaris mushrooms could be employed as a new feed additive that offers potential benefits for elevating egg mass and producing lower cholesterol eggs [ 39]. The improvement in egg production parameters with phytogenic feed additives may be due to the provision of certain functional compounds that improve digestion and absorption of nutrients in the digestive tract [ 61].

3.5. Effects on Blood Biochemistry

Blood biochemical parameters reflect the health [ 61] of an animal and are vital indicators of the physiological and nutritional status of an organism as well as the quality of feed [ 62]. Dietary supplementation of Flammulina velutipes stalk waste at 1 and 2% level of inclusion resulted in significantly lower total cholesterol and high density lipoprotein cholesterol than the control diets [ 19]. The cholesterol concentration of egg yolk significantly decreased in egg laying chickens supplemented with shiitake (0.5%) compared to the control group (basal diet with no shiitake mushroom) [ 32]. Conversely, Mužić et al. [ 63] reported no effect of Shiitake ( Lentinus edodes) mushroom on the cholesterol content of egg yolk. Daneshmand et al. [ 52] found that inclusion of 2 g kg ^-1 oyster mushroom power significantly reduced the high density lipoprotein concentration than the probiotic treatments in the 42 days intervention time, whereas this level of inclusion did not bring significant change in the other lipid parameters when compared to the control and probiotic treatments. In hens, dietary spent mushroom supplementation decreased total cholesterol, LDL-cholesterol, and triglycerides (P<0.05) in laying hens [ 59]. Shah et al. [ 64] reported the anti-cholesterol property of mushrooms. Other studies also proved that phytogenic feed additives such as garlic, fenugreek, coriander, and garden cress are effective in lowering cholesterol concentration in broiler and layer chickens [ 65-68]. Ming-Yei et al. [ 69] indicated that both enoki mushrooms ( Flammulina velutipes) extract and powder, at 3% level of inclusion, are capable of reducing the level of total cholesterol, triglycerides, low-density lipoprotein cholesterol and high density lipoprotein cholesterol in the serum and liver of the hamsters. In the layer rations, supplementation of Pleurotus eryngii mushrooms resulted in significantly low serum triglycerides and serum cholesterol compared to the control fed group [ 33]. Schneider et al. [ 70] observed that groups that received oyster mushroom soup showed a significant reduction in triacylglycerol concentrations and oxidized low density lipoprotein levels in humans. Addition of edible mushroom ( Agaricus bisporus) powder showed an overall decrease in blood lipid metabolite profiles of broiler chickens fed for a period of 42 days [ 50]. Sogunle et al. [ 27] also suggested that the administration of oyster mushroom in water and feed at 15 ml/liter and 750 ppm, respectively, could be adopted in cockerel chickens’ for improved blood lipid profile. Beta-glucan and its derivatives in medicinal mushrooms had cholesterol lowering effects by reducing the absorption or increasing faecal excretion [ 71]. Feeding mushrooms may also involve suppression of endogenous cholesterol biosynthesis by inhibiting the 3-hydroxy-3- methylglutaryl coenzyme A (HMG-CoA) reductase activity, which is the rate-limiting enzyme of cholesterol biosynthesis [ 72].

3.6. Hazards of fungal feed additives

It has been known for a long time that it is hazardous to eat or use as feed some of the larger fungi species, i.e., mushrooms. This might be due to the fact that several mycotoxins can be produced by hazardous fungi [ 73]. Fortunately, various enzymes produced by mushrooms contribute to an antifungal activity [ 74] and can also act to decrease the toxicity of mycotoxins [ 73]. Previous research works demonstrated positive health and performance upon feeding different forms of mushrooms in both broiler and laying poultry [ 11, 19, 25, 59]. The potential of mushroom-forming fungi for the mitigation of mycotoxin contamination in cereal products has also been reviewed by Savoie et al. [ 74]. The same authors further suggested that through proper storage conditions (including rapid drying and crushing), the risk of mycotoxins in the mushroom can be minimized.