Effect of the inclusion of Ganoderma spp. on gut morphometry and growth performance of broiler chickens

ABSTRACT

We conducted an experiment to evaluate the effect of different inclusion rates and routes of administration of Ganoderma spp. on growth performance and gut morphology in broilers. We randomly assigned 320 one-day-old male broilers (Ross 308) to eight treatments with the same basal diet. Performance parameters were food intake (FI), body weight gain (BWG), and feed conversion ratio (FCR). Treatments were a basal diet (NC) with 55 ppm of bacitracin methylene disalicylate BMC (PC), basal diet with Ganoderma at 50 ppm, 100 ppm, and 150 ppm in drinking water (WG50, WG100, WG150), and feed (FG50, FG100, FG150). Body weight gain was higher for FG150 compared with NC. Treatment FG150 and PC had the best indicators of intestinal morphometry, showing significant differences on villi height to crypt depth ratio compared with other treatments. Ganoderma supplementation may be an alternative for the replacement of growth-promoting antibiotics because it offers comparable results to those generated by bacitracin methylene disalicylate (BDM).

Keywords:
broiler; Ganoderma spp.; intestinal morphology; performance

1. Introduction

The global poultry industry is one of the fastest growing markets, with the potential to become the main source of animal proteins (Carvalho et al., 2021), as a result of the increasing demand of a growing world population for food. While the use of antibiotic-based growth promoters has significantly improved performance in global poultry production over the past 50 years (Gadde et al., 2017), there have been growing concerns about the side effects of prophylactic use of these drugs, such as the pro-apoptotic, pro-inflammatory, genotoxic effect (Gallo et al., 2017; Di Cerbo et al., 2018; Pacelli et al., 2020), the emergence of antibiotic-resistant forms of microorganisms, and the possibility of generating residues in the products of treated birds (Fard et al., 2014; Gadde et al., 2017).

This situation has motivated the development of alternative dietary strategies in poultry to improve growth performance and metabolic and health status (Lee et al., 2014). Research suggests that mushrooms can help improving the health and performance of poultry.

The basidiocarps, mycelia, and spores belonging to the genus Ganoderma spp., P. Karst., contain a variety of bioactive compounds, which mainly include triterpenoids, polysaccharides, nucleotides, sterols, steroids, fatty acids, proteins, and trace elements such as aluminum, arsenic, barium cadmium, calcium, cobalt, copper, iron, magnesium, mercury, plumbum, potassium, selenium, vanadium, and zinc (Liu et al., 2015).

Despite the several trials with broilers (Guo et al., 2004; Willis et al., 2007; Giannenas et al., 2010; Giannenas et al., 2011; Kavyani et al., 2012; Hines et al., 2013; Shang et al., 2014; Abro et al., 2016; Fanhani et al., 2016) and laying hens (Willis et al., 2008; Willis et al., 2009; Hwang et al., 2012; Lee et al., 2015; Wang et al., 2015), studies remain scarce and involve fungal species other than Ganoderma. In addition, until now the use of mushroom polysaccharides as growth promoters in poultry has been quite limited, and inclusion rates are not clearly defined, which limits the use and integration of fungi in nutritional plans on an industrial scale. Further studies are needed to investigate the effects of these fungi to improve production performance in chickens and to illuminate the possible modes of action and methods of administration (Khan et al., 2019). Therefore, this study aimed to evaluate the best administration route and the effect of the dietary supplementation of biomass of Ganoderma spp. on growth performance and gut morphometry of broiler chicks.

2. Material and Methods

2.1. Experimental design, diets, and management

The experiment was conducted in Bogotá D.C., Colombia (04°38'13" S, 74°05'16" W, 2554 m altitude). Research was approved by the Institutional Committee on Animal Use (protocol number 023-2021). A total of 320 one-day-old male broiler chickens (Ross 308) were randomly assigned to eight treatments of four replicates (10 chickens each). Birds were housed in batteries, kept in a strictly isolated room, with a controlled environment (relative humidity and light), where the ambient temperature was gradually reduced from 33 to 25 °C from day 1 to day 21. Feed and water were provided ad libitum throughout the experiment.

All animals were fed the same basal diet formulated with the tested corn, vitamins, and minerals to meet the requirements of broilers from 11 to 21 d of age, according to Rostagno et al. (2011) (Table 1). The treatments were basal diet without additives (negative control; NC); basal diet with 55 ppm of Bacitracin methylene disalicylate (positive control; PC); and six diets supplemented with Ganoderma fungal biomass at 50 ppm, 100 ppm, and 150 ppm in drinking water (WG50, WG100, WG150) and in feed (FG50, FG100, FG150). The supplements were administered over 21 days.

Table 1
Ingredients and nutrient specifications of experimental diets applied in starter and finisher periods

Ingredient (%)	Pre-starter diet (1–7 d)	Starter diet (8–21 d)
Corn (7.88%)	58.9	54.9
Soybean meal (45%)	23	29
Whole soy	12	10
Soybean oil	2	2.2
Dicalcium phosphate	1.76	1.64
Calcium carbonate	1	0.97
DL-Methionine	0.34	0.35
Salt	0.35	0.3
L-Lysine HCl	0.39	0.27
L-Threonine	0.17	0.1
Choline HCl	0.09	0.09
Mineral premix	0.1	0.1
Vitamin premix	0.05	0.05

2.2. Sampling and measurements

Performance parameters feed intake (FI), body weight gain (BWG) and feed conversion ratio (FCR) were evaluated weekly. On day 21 of age, all birds were slaughtered, and intestinal samples of 2 cm were taken immediately from the jejunum to evaluate the villus height, crypt depth, and villus height:crypt depth ratio (VH:CD). The samples were flushed with saline and fixed in buffered formalin (pH 7.0). The fixed intestinal samples embedded in paraffin were sectioned in 5.0 μm, stained with hematoxylin-eosin, and examined by light microscope (Nikon Eclipse E400) in 4 X. Villus height was measured from the tip of the villus to the villus-crypt junction according to Uni et al. (2003), and crypt depth was measured from the base upward to the region of transition between the crypt and villus (Uni et al., 1998). All measures were taken in micrometers (μm).

2.3. Statistical analysis

Statistical analysis was performed using SAS software (Statistical Analysis System, version 9.4). Data regarding parameters of growth performance (FI, BWG, and FCR) at the third week and intestinal morphology were expressed as mean ± standard deviation. Statistical differences between treatments were assessed by One-Way Analysis of Variance (ANOVA) followed by Tukey's multiple comparison test. A P<0.05 was considered significant. Normality of the residuals and homogeneity of variances were assessed by the Shapiro–Wilk Test and Barlett's test, respectively. The proposed mathematical model was as follows:

(1) $$Y_{ij}=\mu +T_i+e_{ij},$$

in which Y_ij = value observed for the response variable Y in treatment i and its repetition j, μ = overall mean of all observations, T_i = treatment effect (WG50, WG100, WG150, FG50, FG100, FG150), and e_ij = experimental error associated with the observed value Y_ij.

3. Results

The PC group showed the lowest cumulative FI (827.3 g per bird) and FCR (1.01) compared with the other experimental groups (P<0.05) (Table 2). At 21 days of age, the FG150 group showed the best BW compared with the NC (P<0.05), but there was no difference between the Ganoderma and PC groups. Villi height and depth and VH:CD were similar in FG150 and PC, and these groups showed an increase (P<0.05) in villi dimension compared with the other groups (Table 3).

Table 2
Effect of different levels of Ganoderma spp. inclusion on growth performance of broilers over the period of 0-21 days; data are shown as SEM

	Body weight				Feed intake			Accumulated	Feed conversion ratio
Treatment/age (d)	1	7	14	21	7	14	21	21	7	14	21
NC	46.3	158.6a	411	826.03b	125.8	280.8a	571.3a	977.8a	0.793	0.989a	1.18a
PC	45.7	154.7ab	408	831.4ab	114.6	239.7b	473.0b	827.3b	0.741	0.869b	1.01b
WG50	46.2	154.0ab	412	850.84ab	119.4	270.4a	568.0a	957.7a	0.776	0.962a	1.13a
FG50	46.2	158.7a	422	868.25ab	118.6	278.6a	584.4a	981.6a	0.748	0.947a	1.13a
WG100	46.2	155.8ab	419	855.8ab	123.1	276.7a	573.6a	973.4a	0.791	0.955a	1.11a
FG100	46.2	158.3a	409	856.91ab	117.2	272.1a	585.4a	967.2a	0.74	0.952a	1.14a
WG150	46.2	153.0b	411	834.14ab	121.4	273.3a	576.1a	970.7a	0.794	0.960a	1.17a
FG150	46.2	151.6b	412	875.71a	120.5	277.7a	587.9a	986.1a	0.795	0.966a	1.12a
SEM	0.28	1.66	5.73	14.4	2.51	5.23	9.23	13.9	0.016	0.02	0.04

• NC - negative control; PC - positive control; WG50 - 50 ppm mushroom in water; FG50 - 50 ppm mushroom in feed; WG100 - 100 ppm mushroom in water; FG100 - 100 ppm mushroom in feed; WG150 - 150 ppm mushroom in water; FG150 - 150 ppm mushroom in feed; SEM - standard error of the mean.
• a-b - Mean values with different letters within a column differ significantly (P<0.05).

Table 3
Effect of different inclusion levels of Ganoderma spp. on intestinal morphology of broilers at day 21; data are shown as SEM

Parameter (μm)	Villi height	Villi depth	Height + depth	VH:CD
NC	916.84b	125.58bc	996.24bc	11.77ab
PC	1082.03a	148.56a	1171.05a	12.44a
WG50	804.64d	110.60bc	1171.05a	8.39c
FG50	917.05bc	123.99bc	1006.62bc	10.42b
WG100	796.52cd	110.07bc	895.37c	8.25c
FG100	938.56b	123.08bc	1024.24b	11.28ab
WG150	938.64b	108.7c	1051.12b	8.59c
FG150	1082.21a	131.94ab	1169.14a	12.63a
SEM	3.25	4.74	26.33	0.42

• NC - negative control; PC - positive control; WG50 - 50 ppm mushroom in water; FG50 - 50 ppm mushroom in feed; WG100 - 100 ppm mushroom in water; FG100 - 100 ppm mushroom in feed; WG150 - 150 ppm mushroom in water; FG150 - 150 ppm mushroom in feed; SEM - standard error of the mean.
• a,b,c,d - Different letters within a column indicate significant difference (P<0.05).

These results show that the effect of the fungal extract at the inclusion rate of 150 ppm on the intestinal villus was similar compared with the antibiotic. However, the other treatments with and without different inclusion rates of biomass did not show the same behavior.

4. Discussion

Our results confirm that the diet supplementation with Ganoderma spp. at an inclusion rate of 150 ppm had a positive effect on villi morphometry and had the highest BWG and BW at 21 days of age. In a healthy gut, a greater intestinal absorption surface is expected to allow a more efficient use of nutrients and, consequently, better productive performance. The best response due to supplementation with 150 ppm of Ganoderma fungal biomass could be explained by the existence of polysaccharides (β-glucans) and triterpenoids, compounds that modulate the effect on the intestinal microbiota especially on Bifidobacterium populations (Chou et al., 2013), a beneficial bacterium with functional effects to the intestine. In addition, the presence of sugars and indigestible crude fiber and low fat play a beneficial role in the digestive tract of chickens, increasing the growth of this type of beneficial bacteria (Sundu et al., 2006).

The gut mucosal architecture was influenced by mushroom intake, improving the villus height and depth, with a significant increase in villus. According to Giannenas et al. (2011), the structure of the intestinal mucosa can reveal information on gut health. The effects on intestinal villus height and depth in FG150 and PC are consistent with those reported by Fard et al. (2014), who found a significant increase in villus height and crypt depth in jejunum in birds fed 1% (1239 and 187 μm) and 2% (1223 and 209 μm) of P. ostreatus fungal extracts. Giannenas et al. (2011) reported an increase in villus height in duodenum, jejunum, and ileum by effect of feed supplementation with 1 and 2% of A. bisporus in turkeys. In contrast, the same authors also reported no effect of intestinal villus by feed supplementation with A. bisporus in broilers under the same experimental conditions as turkeys (Giannenas et al., 2010). In addition, no effects were reported on body weight, daily gain, daily feed intake, and feed conversion ratio when broilers were supplemented or not with G. lucidum for 35 days (Chen and Yu, 2020).

A strong correlation between increased villus height with high absorptive efficiency and gut health has been reported (Shamoto and Yamauchi, 2000; Giannenas et al., 2010; Abuajamieh et al., 2020). Cook and Bird (1973) and Schneeman (1982) reported shorter villus and deeper crypts when the counts of pathogenic bacteria increased in the gastrointestinal tract.

In contrast with results of the current study, in which treatment FG150 had the best indicators of growth performance, Willis et al. (2013) found that the Pleurotus mushroom (5%) produced the highest average BWG compared with G. lucidum (5 and 10%) and C. inensis (10%). Similar results were reported in laying hens with the supplementation of 0.1 or 2% of Ganoderma mushroom, (Ogbe et al., 2009). Giannenas et al. (2010) found that 2% of dried A. bisporus mushroom in broiler chicken feed increased body weight and improved FCR at 42 days of age. In our study, mushroom supplementation also resulted in a better growth performance. However, the feed conversion was better in PC group. Bacitracin methylene disalicylate reduced intake, and there was a direct association between FI and FCR.

Limited evidence exists on the mechanisms through which Ganoderma exerts growth-promoting activities. However, it is well known that their polysaccharides enhance feed efficiency of broilers (Khan et al., 2019). Although the effect on the intestinal microbiota was not evaluated in this study, other studies reported more efficient use of dietary nutrients and increased proliferation of epithelial cells at the intestinal level as the results of reduction in the intestinal pathogens, coupled with increased intestinal absorptive area (Topping, 1996; Józefiak et al., 2007), which promotes both feed digestibility and animal performance (Rehman et al., 2006; Rehman et al., 2007a,b).

From a nutritional point of view, Ganoderma is a source of crude protein (16.79%) and carbohydrates (63.27%). Glucose accounted for 11% and metals 10.2% of dry mass (K, Mg, and Ca are the major trace components) that can positively affect the performance parameters (Bao et al., 2001; Ogbe et al., 2008; Ogbe and Obeka, 2013; Willis et al., 2013); however, currently there is little information about the effects of this mushrooms on performance parameters in broilers.

There is not enough information in the literature to determine which is the best route of administration of mushrooms as supplements in poultry feed. As demonstrated in the present study, the best route of administration was the supplementation of fungi in the feed because of the best growth performance and the best intestinal morphometry obtained. The differential effect observed between water and feed administration may be due to a possible dilution effect of Ganoderma when supplemented in drinking water, which could reduce the concentration of polysaccharides and triterpenoids. Additionally, it is not ruled out that these bioactive compounds will be degraded in drinking water, decreasing their action potential. However, it is necessary to perform more tests to determine this.

5. Conclusions

The results presented in this paper suggest that Ganoderma spp. may be able to improve both growth performance and gut morphometry of broiler chickens. The diet supplemented with inclusion rates of FG150 significantly improved body weight and weight gain at day 21 of broilers. Besides, we determined that feed is the best route of administration. Thus, Ganoderma spp. can be included in the diets of broilers at commercially relevant rates with beneficial effects on their performance. The greater area of intestinal absorption observed with inclusion doses of 150 ppm in feed was associated with better growth performance, showing that Ganoderma spp., can have a growth-promoting effect comparable to that produced by the antibiotic Bacitracin methylene disalicylate (BMD). This research showed promising results for the supplementation of Ganoderma in poultry feed. However, there are still unresolved aspects as the mechanism of action and the type of microbiota that proliferate in the intestine after Ganoderma administration, such as the immunostimulant effect on broilers.

Acknowledgments

The authors thank Catalina Torres for her support at the Laboratorio de Patología Aviar of the Universidad Nacional de Colombia. The fungal biomass of Ganoderma was provided by the Bioinnco company (Biotechnology of mushroom products company, Medellin, Colombia).

References

• Abro, R.; Changezi, G. A.; Abro, S. H.; Yasmin, A.; Leghari, R. A.; Rizwana, H. and Lochi, G. M. 2016. Carcass and digestibility patterns fed different levels of mushroom (Pleurotus ostreatus) in the diet of broiler. Science International 28:2985-2988.
• Abuajamieh, M.; Abdelqader, A.; Irshaid, R.; Hayajneh, F. M. F.; Al-Khaza'leh, J. M. and Al-Fataftah, A. R. 2020. Effects of organic zinc on the performance and gut integrity of broilers under heat stress conditions. Archives Animal Breeding 63:125-135. https://doi.org/10.5194/aab-63-125-2020
  » https://doi.org/10.5194/aab-63-125-2020
• Bao, X. F.; Fang, J. and Li, X. 2001. Structural characterization and immunomodulating activity of a complex glucan from spores of Ganoderma lucidum Bioscience, Biotechnology, and Biochemistry 65:2384-2391. https://doi.org/10.1271/bbb.65.2384
  » https://doi.org/10.1271/bbb.65.2384
• Carvalho, N. M.; Oliveira, D. L.; Dib Saleh, M. A.; Pintado, M. E. and Madureira, A. R. 2021. Importance of gastrointestinal in vitro models for the poultry industry and feed formulations. Animal Feed Science and Technology 271:114730. https://doi.org/10.1016/j.anifeedsci.2020.114730
  » https://doi.org/10.1016/j.anifeedsci.2020.114730
• Chen, H. W. and Yu, Y. H. 2020. Effect of Ganoderma lucidum extract on growth performance, fecal microbiota, and bursal transcriptome of broilers. Animal Feed Science and Technology 267:114551. https://doi.org/10.1016/j.anifeedsci.2020.114551
  » https://doi.org/10.1016/j.anifeedsci.2020.114551
• Chou, W. T.; Sheih, I. C. and Fang, T. J. 2013. The applications of polysaccharides from various mushroom wastes as prebiotics in different systems. Journal of Food Science 78:M1041-M1048. https://doi.org/10.1111/1750-3841.12160
  » https://doi.org/10.1111/1750-3841.12160
• Cook, R. H. and Bird, F. H. 1973. Duodenal villus area and epithelial cellular migration in conventional and germ-free chicks. Poultry Science 2:2276-2280. https://doi.org/10.3382/ps.0522276
  » https://doi.org/10.3382/ps.0522276
• Di Cerbo, A.; Scarano, A.; Pezzuto, F.; Guidetti, G.; Canello, S.; Pinetti, D.; Genovese, F. and Corsi, L. 2018. Oxytetracycline-protein complex: the dark side of pet food. The Open Public Health Journal 11:162-169. https://doi.org/10.2174/1874944501811010162
  » https://doi.org/10.2174/1874944501811010162
• Fanhani, J. C.; Murakami, A. E.; Guerra, A. F. Q. G.; Nascimento, G. R.; Pedroso, R. B. and Alves, M. C. F. 2016. Effect of Agaricus blazei in the diet of broiler chickens on immunity, serum parameters and antioxidant activity. Semina: Ciências Agrárias 37:2235-2246. https://doi.org/10.5433/1679-0359.2016v37n4p2235
  » https://doi.org/10.5433/1679-0359.2016v37n4p2235
• Fard, S. H.; Toghyani, M. and Tabeidian, S. A. 2014. Effect of oyster mushroom wastes on performance, immune responses and intestinal morphology of broiler chickens. International Journal of Recycling of Organic Waste in Agriculture 3:141-146. https://doi.org/10.1007/s40093-014-0076-9
  » https://doi.org/10.1007/s40093-014-0076-9
• Gadde, U.; Kim, W. H.; Oh, S. T. and Lillehoj, H. S. 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Animal Health Research Reviews 18:26-45. https://doi.org/10.1017/S1466252316000207
  » https://doi.org/10.1017/S1466252316000207
• Gallo, A.; Landi, R.; Rubino, V.; Di Cerbo, A.; Giovazzino, A.; Palatucci, A. T.; Centenaro, S.; Guidetti, G.; Canello, S.; Cortese, L.; Ruggiero, G; Alessandrini, A. and Terrazzano, G. 2017. Oxytetracycline induces DNA damage and epigenetic changes: a possible risk for human and animal health? PeerJ 5:e3236. https://doi.org/10.7717/peerj.3236
  » https://doi.org/10.7717/peerj.3236
• Giannenas, I.; Pappas, I. S.; Mavridis, S.; Kontopidis, G.; Skoufos, J. and Kyriazakis, I. 2010. Performance and antioxidant status of broiler chickens supplemented with dried mushrooms (Agaricus bisporus) in their diet. Poultry Science 89:303-311. https://doi.org/10.3382/ps.2009-00207
  » https://doi.org/10.3382/ps.2009-00207
• Giannenas, I.; Tsalie, E.; Chronis, E.; Mavridis, S.; Tontis, D. and Kyriazakis, I. 2011. Consumption of Agaricus bisporus mushroom affects the performance, intestinal microbiota composition and morphology, and antioxidant status of turkey poults. Animal Feed Science and Technology 165:218-229. https://doi.org/10.1016/j.anifeedsci.2011.03.002
  » https://doi.org/10.1016/j.anifeedsci.2011.03.002
• Guo, F. C.; Williams, B. A.; Kwakkel, R. P.; Li, H. S.; Li, X. P.; Luo, J. Y.; Li, W. K. and Verstegen, M. W. A. 2004. Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on the cecal microbial ecosystem in broiler chickens. Poultry Science 83:175-182. https://doi.org/10.1093/ps/83.2.175
  » https://doi.org/10.1093/ps/83.2.175
• Hines, V.; Willis, W. L.; Isikhuemhen, O. S.; Ibrahim, S. L.; Anike, F.; Jackson, J.; Hurley, S. L. and Ohiman, E. I. 2013. Effect of incubation time and level of fungus myceliated grain supplemented diet on the growth and health of broiler chickens. International Journal of Poultry Science 12:206-211. https://doi.org/10.3923/ijps.2013.206.211
  » https://doi.org/10.3923/ijps.2013.206.211
• Hwang, J. A.; Hossain, M. E.; Yun, D. H.; Moon, S. T.; Kim, G. M. and Yang, C. J. 2012. Effect of shiitake (Lentinula edodes (Berk.) Pegler) mushroom on laying performance, egg quality, fatty acid composition and cholesterol concentration of eggs in layer chickens. Journal of Medicinal Plants Research 6:146-153.
• Józefiak, D.; Rutkowski, A.; Jensen, B. B. and Engberg, R. M. 2007. Effects of dietary inclusion of triticale, rye and wheat and xylanase supplementation on growth performance of broiler chickens and fermentation in the gastrointestinal tract. Animal Feed Science and Technology 132:79-93. https://doi.org/10.1016/j.anifeedsci.2006.03.011
  » https://doi.org/10.1016/j.anifeedsci.2006.03.011
• Kavyani, A.; Zare Shahne, A.; PorReza, J.; Haji-abadi, J. S. M. A. and Landy, N. 2012. Evaluation of dried powder of mushroom (Agaricus bisporus) as an antibiotic growth promoter substitution on performance, carcass traits and humoral immune responses in broiler chickens. Journal of Medicinal Plants Research 6:94-100.
• Khan, S. H.; Mukhtar, N. and Iqbal, J. 2019. Role of mushroom as dietary supplement on performance of poultry. Journal of Dietary Supplements 16:611-624. https://doi.org/10.1080/19390211.2018.1472707
  » https://doi.org/10.1080/19390211.2018.1472707
• Lee, S. B.; Im, J.; Kim, S. K.; Kim, Y. C.; Kim, M. J.; Lee, J. S. and Lee, H. G. 2014. Effects of dietary fermented Flammulina velutipes mycelium on performance and egg quality in laying hens. International Journal of Poultry Science 13:637-644. https://doi.org/10.3923/ijps.2014.637.644
  » https://doi.org/10.3923/ijps.2014.637.644
• Lee, T. T.; Ciou, J. Y.; Chen, C. N. and Yu, B. 2015. The effect of Pleurotus eryngii stalk residue dietary supplementation on layer performance, egg traits and oxidative status. Annals of Animal Science 15:447-461. https://doi.org/10.2478/aoas-2014-0070
  » https://doi.org/10.2478/aoas-2014-0070
• Liu, Y. H.; Lin, Y. S.; Lin, K. L.; Lu, Y. L.; Chen, C. H.; Chien, M. Y.; Shang, H. F.; Lin, S. Y. and Hou, W. C. 2015. Effects of hot-water extracts from Ganoderma lucidum residues and solid-state fermentation residues on prebiotic and immune-stimulatory activities in vitro and the powdered residues used as broiler feed additives in vivo. Botanical Studies 56:17. https://doi.org/10.1186/s40529-015-0097-3
  » https://doi.org/10.1186/s40529-015-0097-3
• Ogbe, A. O.; Mgbojikwe, L. O.; Owoade, A. A.; Atawodi, S. E. and Abdu, P. A. 2008. The effect of a wild mushroom (Ganoderma lucidum) supplementation of feed on the immune response of pullet chickens to infectious bursal disease vaccine. Electronic Journal of Environmental, Agricultural and Food Chemistry 7:2844-2855.
• Ogbe, A. O.; Ditse, U.; Echeonwu, I.; Ajodoh, K.; Atawodi, S. E. and Abdu, P. A. 2009. Potential of a wild medicinal mushroom, Ganoderma sp., as feed supplement in chicken diet: effect on performance and health of pullets. International Journal of Poultry Science 8:1052-1057. https://doi.org/10.3923/ijps.2009.1052.1057
  » https://doi.org/10.3923/ijps.2009.1052.1057
• Ogbe, A. O. and Obeka, A. D. 2013. Proximate, mineral and anti-nutrient composition of wild Ganoderma lucidum: implication on its utilization in poultry production. Iranian Journal of Applied Animal Science 3:161-166.
• Pacelli, C.; Di Cerbo, A.; Lecce, L.; Piccoli, C.; Canello, S.; Guidetti, G. and Capitanio, N. 2020. Effect of chicken bone extracts on metabolic and mitochondrial functions of K562 cell line. Pharmaceuticals 13:114. https://doi.org/10.3390/ph13060114
  » https://doi.org/10.3390/ph13060114
• Rehman, H.; Böhm, J. and Zentek, J. 2006. Effects of diets with insulin and sucrose on the microbial fermentation in the gastrointestinal tract of broilers. Proceedings of the Society of Nutrition Physiology 15:155-158.
• Rehman, H.; Rosenkranz, C.; Böhm, J. and Zentek, J. 2007a. Dietary inulin affects the morphology but not the sodium dependent glucose and glutamine transport in the jejunum of broilers. Poultry Science 86:118-122. https://doi.org/10.1093/ps/86.1.118
  » https://doi.org/10.1093/ps/86.1.118
• Rehman, H. U.; Vahjen, W.; Awad, W. A. and Zentek, J. 2007b. Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broilers chickens. Archives of Animal Nutrition 61:319-335. https://doi.org/10.1080/17450390701556817
  » https://doi.org/10.1080/17450390701556817
• Rostagno, H. S.; Albino, L. F. T.; Donzele, J. L.; Gomes, P. C.; Oliveira, R. F.; Lopes, D. C.; Ferreira, A. S.; Barreto, S. L. T. and Euclides, R. F. 2011. Tabelas brasileiras para aves e suínos - Composição de alimentos e exigências nutricionais. 3.ed. Universidade Federal de Viçosa, Viçosa, MG. 252p.
• Schneeman, B. O. 1982. Pancreatic and digestive function. p.73-83. In: Dietary fiber in health and disease. Vahouny, G. V. and Kritchevsky, D., eds. Plenum Press, New York.
• Shamoto, K. and Yamauchi, K. 2000. Recovery responses of chick intestinal villus morphology to different refeeding procedures. Poultry Science 79:718-723. https://doi.org/10.1093/ps/79.5.718
  » https://doi.org/10.1093/ps/79.5.718
• Shang, H. M.; Song, H.; Jiang, Y. Y.; Ding, G. D.; Xing, Y. L.; Niu, S. L.; Wu, B. and Wang, L. N. 2014. Influence of fermentation concentrate of Hericium caput-medusae (Bull.:Fr.) Pers. on performance, antioxidant status, and meat quality in broilers. Animal Feed Science and Technology 198:166-175. https://doi.org/10.1016/j.anifeedsci.2014.09.011
  » https://doi.org/10.1016/j.anifeedsci.2014.09.011
• Sundu, B.; Kumar, A. and Dingle, J. 2006. Palm kernel meal in broiler diets: effect on chicken performance and health. World's Poultry Science Journal 62:316-325. https://doi.org/10.1079/WPS2005100
  » https://doi.org/10.1079/WPS2005100
• Topping, D. L. 1996. Short-chain fatty acids produced by intestinal bacteria. Asia Pacific Journal of Clinical Nutrition 5:15-19.
• Uni, Z.; Ganot, S. and Sklan, D. 1998. Posthatch development of mucosal function in the broiler small intestine. Poultry Science 77:75-82. https://doi.org/10.1093/ps/77.1.75
  » https://doi.org/10.1093/ps/77.1.75
• Uni, Z.; Smirnov, A. and Sklan, D. 2003. Pre-and posthatch development of goblet cells in the broiler small intestine: effect of delayed access to feed. Poultry Science 82:320-327. https://doi.org/10.1093/ps/82.2.320
  » https://doi.org/10.1093/ps/82.2.320
• Wang, C. L.; Chiang, C. J.; Chao, Y. P.; Yu, B. and Lee, T. T. 2015. Effect of Cordyceps militaris waster mediumon production performance, egg traits and egg yolk cholesterol of laying hens. The Journal of Poultry Science 52:188-196. https://doi.org/10.2141/jpsa.0140191
  » https://doi.org/10.2141/jpsa.0140191
• Willis, W. L.; Isikhuemhen, O. S. and Ibrahim, S. A. 2007. Performance assessment of broiler chickens given mushroom extract alone or in combination with probiotics. Poultry Science 86:1856-1860. https://doi.org/10.1093/ps/86.9.1856
  » https://doi.org/10.1093/ps/86.9.1856
• Willis, W. L.; Goktepe, I.; Isikhuemhen, O. S.; Reed, M.; King, K. and Murray, C. 2008. The effect of mushroom and pokeweed extract on Salmonella, egg production, and weight loss in molting hens. Poultry Science 87:2451-2457. https://doi.org/10.3382/ps.2008-00004
  » https://doi.org/10.3382/ps.2008-00004
• Willis, W. L.; Isikhuemhen, O. S.; Allen, J. W.; Byers, A.; King, K. and Thomas, C. 2009. Utilizing fungus myceliated grain for molt induction and performance in commercial laying hens. Poultry Science 88:2026-2032. https://doi.org/10.3382/ps.2009-00120
  » https://doi.org/10.3382/ps.2009-00120
• Willis, W. L.; Wall, D. C.; Isikhuemhen, O. S.; Jackson, J. N.; Ibrahim, S.; Hurley, S. L. and Anike, F. 2013. Effect of level and type of mushroom on performance, blood parameters and natural coccidiosis infection in floor-reared broilers. The Open Mycology Journal 7:1-6. https://doi.org/10.2174/1874437001307010001
  » https://doi.org/10.2174/1874437001307010001

Publication Dates

• Publication in this collection
  24 Nov 2023
• Date of issue
  2023

History

• Received
  25 Jan 2022
• Accepted
  06 July 2022