Effects of Micronized Bamboo Powder on Growth Performance, Serum Biochemical Indexes, Cecal Chyme Microflora and Metabolism of Broilers Aged 1-22 Days

Abstract

Necrotic enteritis is common in broilers, which makes negative effects on growth performance. Adding insoluble fiber to diet of broilers has been reported to improve intestinal health and promote growth performance. Bamboo powder is a cheap raw material with rich insoluble fiber. This study aims to explore the effects of feeding micronized bamboo powder (MBP) on growth performance, serum biochemical indexes, intestinal microflora, and metabolism of broilers. A total of 1440 1-day-old ephedra chickens were randomly divided into three groups considering gender and body weight: (1) Group D: feeding with basal diet without antibiotics; (2) Group E: feeding with basal diet supplemented with 5% rice bran (RB); (3) Group F: feeding with basal diet supplemented with 1% MBP. Each group involved 8 replicates, with 60 chickens per replicate. After feeding for 22 days, various indexes were detected. For the growth performance, the weight gain and feed consumption ratio (G: F) of Group F supplemented with MBP is 0.57 ± 0.04, which is significantly higher than that of E group supplemented with RB (0.52 ± 0.01, P < 0.05). For the serum biochemical indexes, the glutathione peroxidase activity in Group F is significantly higher than that of in Group D, while the malondialdehyde content is significantly lower than that of in Group D and Group E (P < 0.05 for all). The fresh cecal chyme is taken for determination. In Group F, the α diversity index Faith_pd is significantly lower in Group F than that of in Group D. The microorganism species in cecal chyme of Group F and Group E are also different. The metabolic pathways of Group F differ from those of Group D and Group E, mainly manifested in fatty acid metabolism, amino acid metabolism and intestinal immune IgA production. Adding 1% MBP to broiler diet can enhance the anti-oxidant capacity, improve chyme microflora, regulate the metabolism pathways responsible for intestinal fatty acids, amino acids, and immunity. 

Introduction

With the rapid development of animal husbandry, the reduced resource and rising cost of feed have become the critical factors for limiting its green and lasting development in the future. The exploration of unconventional feed resources is urgently needed (Makkar, 2018). Under the background of “Prohibiting the addition of growth-promoting antibiotics in feed” in China, adopting appropriate fiber-based nutrition is one of the most effective alternatives to improve animal intestinal health and growth performance (Jiménez-Moreno et al., 2016; Shang et al., 2021). However, the effects are different for various fibers in broiler feed (Jiménez-Moreno et al., 2009; Jiménez-Moreno et al., 2019). Therefore, it is very important to find suitable source of fibers.

Bamboo is one of the renewable natural resources with the fastest growth rate and highest yield. The bamboo resources are abundant with wide distribution (He et al., 2014; Lancefield et al., 2017). When pandas fed with whole bamboo, the apparent digestibility of crude protein and crude fiber is 33.8% and 31.8% (Sims et al., 2007). The content of insoluble dietary fiber (IDF) is 62.54% ~ 89.79% in bamboo powder (Felisberto et al., 2017). Further, the bamboo powder is rich in leaf flavonoids and polysaccharides, which is conductive to regulating the immunity and antioxidant capacity of animals (Ge et al., 2020). Bamboo shoot shell fibers exhibit strong cholesterol adsorption activity and prebiotic potential, which can promote the growth of lactic acid bacteria and increase the fermentability of substrates (Wu et al., 2020). It can also improve the disorder of fat metabolism in mice with hyperlipidemia (Luo et al., 2017). Thus, it is expected to become a source of starch and fiber in feed. At present, bamboo-based fiber materials have been added to pig feed and sheep feed (Okano et al., 2009; Oguri et al., 2013), but there has been no report on broiler feed.

In traditional opinions, adding fiber to broiler feed may dilute nutrition, thus making negative effects on feed digestibility and growth performance (Janssen and Carré, 1985). However, existing research show that, moderate content of IDF can lower the moisture content of litter (Kheravii et al., 2017), reduce fat deposition and increase the growth rate (Nassar et al., 2019), and stimulate the development of chicken stomach, thus improving the nutrient utilization rate and promoting the growth of chicken (Donadelli et al., 2019). Similar results can be obtained by supplementing an appropriate level of structural IDF raw materials to the low-fiber diet of broilers (Jiménez-Moreno et al., 2016).

The processing technology and fiber resource can also change the chemical composition and nutritional composition of fibers (Donadelli et al., 2019). Micronization can change the particle size distribution and functional characteristics of IDF in rice bran (RB), thus affecting the digestibility of raw materials. The micronized RB show high water-holding capacity, swelling capacity, high phenol extraction rate and oxidation resistance (Zhao et al., 2018). The bionic digestion experiment performed on wheat show that the in-vitro digestibility of both dry matter and crude protein is increased with decreased grain size (Bao et al., 2017). The decreased grain size can improve total energy, dry matter, total fiber and IDF apparent ileal digestibility. There are also significant interactions between grain size and fiber source, thus affecting the digestibility of hindgut fiber (Zhao et al., 2019). The fiber resource can also make effects. Compared with the fiber extracted from bamboo shoot shell, the feed bamboo powder made from bamboo stems contains a certain amount of lignin. Ultra-micronization can increase the content of soluble fiber components, reduce the lignin level, and improve the water holding capacity and fat adsorption of raw materials (Speroni et al., 2020).

The previous studies of our group found that, the D90 of micronized bamboo powder (MBP) has been lower than that of conventional bamboo powder. MBP exhibited more obvious growth promoting effects in weaning piglets. In this study, MBP has been added to broiler diet and fed for 22 days. Then, we explore the effects of MBP on growth performance, serum nutrition physiology and anti-oxidation, digestive organ index, cecal chyme volatile fatty acids, cecal chyme microflora structure and metabolic changes of broilers. We hope the results of this study can provide data and information for the applications of MBP in broiler diet.

Discussion Materials And Methods

Discussion Results And Analysis

Discussion

Supplementary of fibers in broiler diets can make beneficial effects on the growth performance, serological indexes and intestinal microbia, etc. For the growth performance, adding an appropriate amount of IDF in broiler diets can decrease the moisture content of the bedding (Kheravii et al., 2017), stimulate the development of chicken stomach (Donadelli et al., 2019), reduce fat deposition (Nassar et al., 2019), lower the pH of muscle stomach, improve nutrient digestibility (Jiménez-Moreno et al., 2019) and utilization rate (Nassar et al., 2019), so as to promote the growth of chicken (Donadelli et al., 2019). Adding 1% ~ 1.5% IDF-based cassava pulp modified fiber to broiler diets can reduce abdominal fat deposition, enhance muscle and stomach function and improve nutrient digestibility (Okrathok and Khempaka, 2020). Adding 3% ~ 6% insoluble fiber to wheat basal diet can improve the growth performance of broilers (Shirzadegan and Taheri, 2017). Similar results can be obtained by adding an appropriate level of structural IDF (Jiménez-Moreno et al., 2016). During the maturation and degeneration of lymphoid organs, adding IDF or mixture of IDF and SDF can promote the development of immune system of young birds and chickens (Hussein et al., 2017). However, the digestibility of organic matter and energy was decreased significantly when the level of fibers increased significantly (Röhe et al., 2020). Adding 3% ~ 6% insoluble fiber such as alfalfa meal, RB and sawdust in diet had no significant effect on slaughter performance of broilers (Shirzadegan and Taheri, 2017). In our study, adding 1% of MBP to broiler diet can improve the G: F and ADG, while it has no significant effect on ADFI, mortality, and most organ indexes. The results indicated that adding MBP to broiler diet was conductive to improving the growth performance of broilers, and the level of 1% was feasible. The dosage could be further tested and optimized from the aspects of organ development and slaughter performance.

In addition, the fiber from different sources also made different effects (Jiménez-Moreno et al., 2016). Jiménez-Moreno et al. (2019) showed that the addition of oat hulls was better than rice husks and sunflower hulls in improving muscle stomach weight, reducing muscle stomach pH and improving nutrient digestibility (Jiménez-Moreno et al., 2019). Our study indicated that the effects of adding MBP in broiler diet were better than that of RB, which may be related to the varied physical and chemical properties between the two fibers.

Dietary IDF can affect the serological parameters of broilers. MBP contains 0.94% ~13.4% of polysaccharide, 1.75%~16.89% of starch, 1.31%~2.03% of crude protein, and 62.54% ~ 89.79% of IDF (Felisberto et al., 2017). It was rich in bamboo leaf flavonoids and polysaccharides, which can regulate the immunity and anti-oxidant capacity of animals (Ge et al., 2020). Bamboo shoot shell fiber had strong cholesterol adsorption activity and prebiotic potential, which can be used as a prebiotic to promote the growth of lactic acid bacteria and increase the fermentability of substrates (Wu et al., 2020). For the mice with hyperlipidemia, it improved the disorder of fat metabolism, reduced the contents of serum cholesterol, triglyceride, low-density lipoprotein cholesterol, and increased the content of high-density lipoprotein cholesterol (Luo et al., 2017). Our study indicated that the addition of MBP regulated the serum biochemical indexes. Compared with RB, the MDA and serum glucose were significantly decreased in broilers fed with MBP. Further, the serum urea nitrogen also tended to be decreased. Chicken can be applied as biological model of growth and development (Vainio and Imhof, 1995; Hillier LaDeana, 2004). The addition of 1.0% IDF-based cassava modified fiber in broiler diet can lower serum cholesterol (Okrathok and Khempaka, 2020). It is consisted with the results obtained in our study. The addition of fibers from different source can significantly reduce the serum glucose, triglyceride, and total cholesterol in broilers, while significantly increasing the serum glutathione peroxidase activity. The fibers of RB and MBP are mainly made of IDF, indicating that IDF-based fiber material is helpful to improve serum glucose and lipid metabolism of broilers.

The intestinal microbial community has been very important to the host (Ji et al., 2019), which may affect the intestinal function through its metabolites of SCFAs (Clausen and Mortensen, 1995), thus making effects on the nutrition, immunity and physiological states of the host (Ussar et al., 2016; Imhann et al., 2018; Rubio, 2019). As we all know, cecum can digest some carbohydrates which cannot be digested by small intestine, including cellulose, starch and polysaccharide (Clench and Mathias, 1995). Cecal SCFAs were produced by intestinal microorganisms through the fermentation of undigested carbohydrates (Den Besten et al., 2013; Li, 2018). Awad et al.(2016) found that the variations of fermentation products may be related to the density of microflora (Awad et al., 2016). The highest diversity and abundance of microbial flora has been observed in cecum (Gong et al., 2007; Choi et al., 2014; Liao et al., 2020). After exploring different parts of intestines, it was also found that SCFAs were the most abundant in the cecum (Liao et al., 2020). The difference of SCFAs between small intestine and cecum may be related to the intestinal transportation, intestinal pH and microbial composition (Macfarlane and Macfarlane, 2012). Therefore, our study has also focused on SCFAs in the cecum of broilers.

Previous studies have revealed that the SCFAs can significantly affect the intestinal health, which is closely related the microbials in the intestine. Acetic acid inhibited gastric cell apoptosis and promoted mucin production (Liu et al., 2017), while butyric acid provided energy, maintained the integrity of intestinal epithelial cells and stimulated the growth of intestinal tract (Sun and O'Riordan, 2013). It was found that cecal infusion of butyrate stimulated the proliferation of jejunum and ileum cells in piglets (Kien et al., 2007). Butyrate in cecum may be sent back to the small intestine through reverse peristalsis, thus promoting the development of the small intestine. Lactic acid bacteria was positively correlated to acetate in ileum (Liao et al., 2020), which can improve intestinal health by producing some certain SCFAs (He et al., 2019; Zhai et al., 2019). Salmonella was negatively correlated with SCFAs including acetic acid, butyric acid and isovaleric acid (Liao et al., 2020), indicating that cecal SCFAs may inhibit the growth and invasion of salmonella (Lawhon et al., 2002).

SCFAs can be changed with the diet. Furthermore, when the level of cellulose was increased, SCFAs decreased significantly (Röhe et al., 2020). In addition, it was found that adding a small amount of fiber in diet of weaned piglets tended to increase the VFA in feces. The amount of lactic acid bacteria and total VFA in feces would be increased significantly under poor sanitary conditions (Mu et al., 2017). In our study, adding 1% MBP had no significant effect on the composition of SCFAs in cecal chyme of broilers (including acetic acid, butyric acid, propionic acid, isobutyric acid, isovaleric acid, valeric acid, etc.), while the levels were increased. It may also be related to the supplementary dosage and culture environment. Further study should be performed to explore whether MBP can promote intestinal health and growth by regulating fermentation and producing SCAFs.

Dietary composition is an important factor affecting intestinal bacteria (Liao et al., 2020). The microbial abundance and diversity in feces could be improved by increasing the levels of dietary fibers, which were indicated by Chao and Shannon indexes (Jiang et al., 2019). Mu et al. (2017) found that alfalfa diet can increase the diversity of intestinal flora in piglets (Mu et al., 2017). The cecal microbial diversity was rich in birds (Liao et al., 2020). Our study revealed that the addition of MBP significantly reduced the evolution diversity index Faith_pd of cecal chyme microorganism, and tended to reduce the richness index Chao1. The decrease of diversity index is conductive to reducing the nutrient consumption of microbial flora, thus improving the growth performance.

The composition of microflora was complex in gastrointestinal tract of chicken (about 10⁷-10¹¹ CFU/g), among which Firmicutes were the most abundant, followed by Proteobacteria and Bacteroidetes (Apajalahti et al., 2004; Sergeant et al., 2014; Xiao et al., 2017). During the growth stage of broilers, the dominant flora in cecum were thick-walled bacteria such as Faecalibacterium, Ruminococcus and Lachnospiraceae, while the dominant flora in cecum were Bacteroidetes in the later growth stage. Studies have found that Ruminococcus was the main microflora that produced SCFAs in the intestine (Li et al., 2018), which was positively correlated with the production of butyric acid (Liao et al., 2020). Trichinella can promote intestinal development and health by degrading plant fiber and producing SCFAs (Biddle et al., 2013). Bacteroidetes can degrade complex carbohydrates by fermenting glucose to synthesize butyric acid as energy of epithelial cells (Macy and Probst, 1979), and the abundance of Bacteroidetes in cecum was positively correlated with butyric acid concentration (Liao et al., 2020).

The source and structure of dietary fibers can affect the regulation of intestinal flora in broilers. Adding inulin (contained mainly SDF) to broiler diet made greater effects on microflora, however, its effects on weight gain was less than that of inulin and bran combination group (Li et al., 2018). Adding 2% lignocellulose can reduce Clostridium, without affecting the amount of Bifidobacterium, Bacteroides, Bacillus and Lactobacillus (Kheravii et al., 2017). It has been found that amorphous cellulose with IDF as the main component can change the composition of microflora at the level of Bacteroidea in the chyme, especially Alistipes (De Maesschalck et al., 2019). However, when the level of cellulose increased significantly, Shigella chymotryi decreased significantly (Röhe et al., 2020). In this study, the addition of MBP tended to increase the richness ratio of Firmicutes and Flavonifractor in cecal chyme of broilers, while the addition of RB decreased the ratio of Firmicutes and increase the ratio of Bacteroides, the abundance ratio of Festuca and Bacteroides was also increased. Further results indicated that the addition of MBP made great effects on cecal chyme flora of broilers, in which the abundance of Muribaculum and Veillonellaceae were significantly reduced, and the abundance of Collinsella was significantly increased. It indicated that MBP can not only regulate the richness and diversity of microflora, but also affecting their composition.

Similar results can be obtained by typical chromatogram analysis and metabolic component cluster analysis on the cecal chyme of broilers. The addition of MBP and RB can both affect the total ionic strength and component clustering of cecal chyme metabolites in broilers. It indicated that the addition of IDF can change the specie and concentration of metabolites, thus affecting the cecal chyme metabolism. It was also confirmed by the further analysis of metabolic pathways. Compared with the control, the differential metabolic pathways after the addition of MBP were mainly fatty acid metabolism, amino acid metabolism and intestinal immune IgA production. In addition, the effects of adding different IDF on metabolic pathways also varied. The differences between adding MBP and RB were mainly pathways responsible for amino acid metabolism and fatty acid metabolism.

Fibers play the role of prebiotics in cecal digestion of animals, promoting the selection of healthy intestinal microflora (Kheravii et al., 2017; Donadelli et al., 2019). It is still necessary to further explore the mechanism on the effects of adding MBP in broiler diet. The analysis of differential metabolic pathway confirmed the effects of MBP. Further study can be focused on the fatty acid metabolism, amino acid metabolism and intestinal immune IgA production.

Conclusion

Bamboo powder is a kind of abundant fiber resource. Under the background of forbidding sub-therapeutic antibiotics in China, fiber may be used as a prebiotic to assist animal cecal digestion and promote the formation of healthy intestinal microflora. This study reveals that adding 1% MBP in antibiotic-free basal diet of broilers improved growth performance, serum nutritional and physiological indexes and antioxidant indexes. It plays a regulatory role in the abundance and composition of cecal chyme microflora, as well as the differential metabolic pathways.

Declarations

Funding

This work was supported by the key Research Program of Sichuan Province (NO.2021YFN0106) and the Research Start-up Foundation of Leshan Normal University (No. RC202004).

Conflicts of interest 

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work. All results were strictly in accordance with the experimental data.

Ethics approval

All animal care and handling were approved by the Ethics Committee for Animal Experimentation, science and technology department, Leshan Normal University, Sichuan, China. The protocols were supported by the regulations for animal experiments established by the Ministry of Science and Technology in China (2014). 

Consent to participate

We declare that all authors confirm the content in the paper and participate in the relevant research work.

Consent for publication

We declare that all authors agree to submit the manuscript and pay for the publication if it is accepted.

Availability of data and material

The datasets used or analysed during the current study are available from the corresponding author on reasonable request.

Code availability 

The software SPSS25.0, QIIME2(2019.4), and Greengenes database in the current study were open to researchers around the world. 

Author contributions 

Fawen Dai initiated the idea, finished the experiment design. Fawen Dai, Tao Lin, Lumin Cheng and Jian Wang conducted the animal trial and Laboratory index determination. Lin Tao and Fawen Dai prepared the initial manuscript in English. Jianjun Zuo and Dingyuan Feng made the final revision. All authors read and approved the final manuscript.

References

1. Apajalahti, J., A. Kettunen, and H. Graham. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poultry Science Journal 2004;60(2):223–232.
2. Awad, W., F. Dublecz, C. Hess, K. Dublecz, B. Khayal, J. Aschenbach, et al. Campylobacter jejuni colonization promotes the translocation of Escherichia coli to extra-intestinal organs and disturbs the short-chain fatty acids profiles in the chicken gut. Poultry science 2016;95(10):2259–2265.
3. Bao, K., K. Wang, X. Wang, T. Zhang, H. Liu, and G. Li. Effects of dietary manganese supplementation on nutrient digestibility and production performance in male sika deer (Cervus Nippon). Animal science journal = Nihon chikusan Gakkaiho 2017;88(3):463–467.
4. Biddle, A., L. Stewart, J. Blanchard, and S. Leschine. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 2013;5(3):627–640.
5. Callahan, B. J., P. J. McMurdie, M. J. Rosen, A. W. Han, A. J. A. Johnson, and S. P. Holmes. DADA2: high-resolution sample inference from Illumina amplicon data. Nature methods 2016;13(7):581–583.
6. Choi, J., G. Kim, and C. Cha. Spatial heterogeneity and stability of bacterial community in the gastrointestinal tracts of broiler chickens. Poultry science 2014; 93(8):1942–1950.
7. Clausen, M. R., and P. Mortensen. Kinetic studies on colonocyte metabolism of short chain fatty acids and glucose in ulcerative colitis. Gut 1995;37(5):684–689.
8. Clench, M. H., and J. R. Mathias. The avian cecum: a review. The Wilson Bulletin 1995;93–121.
9. De Maesschalck, C., V. Eeckhaut, L. Maertens, L. De Lange, L. Marchal, G. Daube, et al. Amorphous cellulose feed supplement alters the broiler caecal microbiome. Poultry science 2019;98(9):3811–3817.
10. Den Besten, G., K. Van Eunen, A. K. Groen, K. Venema, D.-J. Reijngoud, and B. M. Bakker. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of lipid research 2013;54(9):2325–2340.
11. Donadelli, R. A., D. A. Stone, C. G. Aldrich, and R. S. Beyer. Effect of fiber source and particle size on chick performance and nutrient utilization. Poultry science 2019;98(11):5820–5830.
12. Felisberto, M. H. F., P. S. E. Miyake, A. L. Beraldo, and M. Clerici. Young bamboo culm: Potential food as source of fiber and starch. Food research international (Ottawa, Ont.) 2017;101:96–102.
13. Ge, Q., H. Li, P. Wu, R. Sha, Z. Xiao, J. Dai, et al. Investigation of physicochemical properties and antioxidant activity of ultrafine bamboo leaf powder prepared by ball milling. Journal of Food Processing and Preservation 2020;44(7):e14506.
14. Gong, J., W. Si, R. J. Forster, R. Huang, H. Yu, Y. Yin, et al. 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS microbiology ecology 2007;59(1):147–157.
15. He, M. X., J. L. Wang, H. Qin, Z. X. Shui, Q. L. Zhu, B. Wu, et al. Bamboo: a new source of carbohydrate for biorefinery. Carbohydrate polymers 2014;111:645–654.
16. He, T., Y. H. Zhu, J. Yu, B. Xia, X. Liu, G. Y. Yang, et al. Lactobacillus johnsonii L531 reduces pathogen load and helps maintain short-chain fatty acid levels in the intestines of pigs challenged with Salmonella enterica Infantis. Veterinary Microbiology 2019.
17. Hillier LaDeana, W. International chicken genome sequencing consortium. Nature 2004; 432:695–716.
18. Hussein, S. M., J. S. Yokhana, and T. L. Frankel. Supplementing the feeds of layer pullets, at different ages with two different fiber sources improves immune function. Poultry science 2017;96(8):2718–2727.
19. Imhann, F., A. Vich Vila, M. J. Bonder, J. Fu, D. Gevers, M. C. Visschedijk, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut 2018;67(1):108–119.
20. Janssen, W., and B. Carré. Influence of fibre on digestibility of poultry feeds. In: 19. Nutrition conference for feed manufacturers 1985.
21. Ji, J., C. L. Luo, X. Zou, X. H. Lv, Y. B. Xu, D. M. Shu, et al. Association of host genetics with intestinal microbial relevant to body weight in a chicken F2 resource population. Poultry science 2019;98(9):4084–4093.
22. Jiang, X., N. Lu, Y. Xue, S. Liu, H. Lei, W. Tu, et al. Crude fiber modulates the fecal microbiome and steroid hormones in pregnant Meishan sows. General and comparative endocrinology 2019;277:141–147.
23. Jiménez-Moreno, E., A. de Coca-Sinova, J. González-Alvarado, and G. Mateos. Inclusion of insoluble fiber sources in mash or pellet diets for young broilers. 1. Effects on growth performance and water intake. Poultry science 2016; 95(1):41–52.
24. Jiménez-Moreno, E., J. González-Alvarado, A. D. Coca-Sinova, R. Lázaro, and G. G. Mateos. Effects of source of fibre on the development and pH of the gastrointestinal tract of broilers. Animal Feed Science & Technology 2009;154(1–2):93–101.
25. Jiménez-Moreno, E., J. M. González-Alvarado, A. de Coca-Sinova, R. P. Lázaro, L. Cámara, and G. G. Mateos. Insoluble fiber sources in mash or pellets diets for young broilers. 2. Effects on gastrointestinal tract development and nutrient digestibility1. Poultry science 2019;98(6):2531–2547.
26. Kheravii, S., R. A. Swick, M. Choct, and S.-B. Wu. Dietary sugarcane bagasse and coarse particle size of corn are beneficial to performance and gizzard development in broilers fed normal and high sodium diets. Poultry science 2017;96(11):4006–4016.
27. Kien, C. L., R. Blauwiekel, J. Y. Bunn, T. L. Jetton, and E. Al. Cecal Infusion of Butyrate Increases Intestinal Cell Proliferation in Piglets. Journal of Nutrition 2007;137(4):916–922.
28. Lancefield, C. S., I. Panovic, P. J. Deuss, K. Barta, and N. J. Westwood. Pre-treatment of lignocellulosic feedstocks using biorenewable alcohols: towards complete biomass valorisation. Green Chemistry 2017;19
29. Lawhon, S. D., R. Maurer, M. Suyemoto, and C. Altier. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Molecular Microbiology 2002;46(5)
30. Li, Y., T. Liu, C. Yan, R. Xie, Z. Guo, S. Wang, et al. Diammonium glycyrrhizinate protects against nonalcoholic fatty liver disease in mice through modulation of gut microbiota and restoration of intestinal barrier. Molecular pharmaceutics 2018;15(9):3860–3870.
31. Liao, X., Y. Shao, G. Sun, Y. Yang, L. Zhang, Y. Guo, et al. The relationship among gut microbiota, short-chain fatty acids, and intestinal morphology of growing and healthy broilers. Poultry science 2020;99(11):5883–5895.
32. Liu, J., J. Wang, Y. Shi, W. Su, J. Chen, Z. Zhang, et al. Short Chain Fatty Acid Acetate Protects against Ethanol-Induced Acute Gastric Mucosal Lesion in Mice. Biological & Pharmaceutical Bulletin 2017;40(9):1439–1446.
33. Luo, X., Q. Wang, B. Zheng, L. Lin, B. Chen, Y. Zheng, et al. Hydration properties and binding capacities of dietary fibers from bamboo shoot shell and its hypolipidemic effects in mice. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association 2017;109(Pt 2):1003–1009.
34. Macfarlane, G. T., and S. Macfarlane. Bacteria, colonic fermentation, and gastrointestinal health. Journal of AOAC International 2012;95(1):50–60.
35. Macy, J. M., and I. Probst. The biology of gastrointestinal bacteroides. Annual review of microbiology 1979;33:561–594.
36. Makkar, H. P. S. Review: Feed demand landscape and implications of food-not feed strategy for food security and climate change. Animal: an international journal of animal bioscience 2018;12(8):1744–1754.
37. Mu, C., L. Zhang, X. He, H. Smidt, and W. Zhu. Dietary fibres modulate the composition and activity of butyrate-producing bacteria in the large intestine of suckling piglets. Antonie van Leeuwenhoek 2017;110(5):687–696.
38. Nassar, M., S. Lyu, J. Zentek, and G. Brockmann. Dietary fiber content affects growth, body composition, and feed intake and their associations with a major growth locus in growing male chickens of an advanced intercross population. Livestock Science 2019;227:135–142.
39. Oguri, M., K. Okano, H. Ieki, M. Kitagawa, O. Tadokoro, Y. Sano, et al. Feed intake, digestibility, nitrogen utilization, ruminal condition and blood metabolites in wethers fed ground bamboo pellets cultured with white-rot fungus (Ceriporiopsis subvermispora) and mixed with soybean curd residue and soy sauce cake. Animal science journal Nihon chikusan Gakkaiho 2013;84(9):650–655.
40. Okano, K., N. Ohkoshi, A. Nishiyama, T. Usagawa, and M. Kitagawa. Improving the nutritive value of madake bamboo, Phyllostachys bambusoides, for ruminants by culturing with the white-rot fungus Ceriporiopsis subvermispora. Animal Feed Science and Technology 2009;152(3–4):278–285.
41. Okrathok, S., and S. Khempaka. Modified-dietary fiber from cassava pulp reduces abdominal fat and meat cholesterol contents without affecting growth performance of broiler chickens. Journal of Applied Poultry Research 2020;29(1):229–239.
42. Röhe, I., F. Metzger, W. Vahjen, G. Brockmann, and J. Zentek. Effect of feeding different levels of lignocellulose on performance, nutrient digestibility, excreta dry matter, and intestinal microbiota in slow growing broilers. Poultry science 2020;99(10):5018–5026.
43. Rognes, T., T. Flouri, B. Nichols, C. Quince, and F. Mahé. VSEARCH: a versatile open source tool for metagenomics. PeerJ 2016;4:e2584.
44. Rubio, L. A. Possibilities of early life programming in broiler chickens via intestinal microbiota modulation. Poultry science 2019;98(2):695–706.
45. Sergeant, M. J., C. Constantinidou, T. A. Cogan, M. R. Bedford, C. W. Penn, and M. J. Pallen. Extensive microbial and functional diversity within the chicken cecal microbiome. PloS one 2014;9(3):e91941.
46. Shang, Q., H. Liu, D. Wu, S. Mahfuz, and X. Piao. Source of fiber influences growth, immune responses, gut barrier function and microbiota in weaned piglets fed antibiotic-free diets. Animal nutrition (Zhongguo xu mu shou yi xue hui) 2021;7(2):315–325.
47. Shirzadegan, K., and H. Taheri. Insoluble fibers affected the performance, carcass characteristics and serum lipid of broiler chickens fed wheat-based diet. Iranian Journal of Applied Animal Science 2017;7(1):109–117.
48. Sims, J. A., J. L. Parsons, H. A. Bissell, R. S. Sikes, J. R. Ouellette, and B. J. Rude. Determination of bamboo-diet digestibility and fecal output by giant pandas. Ursus 2007;18(1):38–45.
49. Speroni, C. S., A. B. B. Bender, J. Stiebe, C. A. Ballus, P. F. Ávila, R. Goldbeck, et al. Granulometric fractionation and micronization: A process for increasing soluble dietary fiber content and improving technological and functional properties of olive pomace. LWT 2020;130:109526.
50. Sun, Y., and M. X. D. O'Riordan. Regulation of Bacterial Pathogenesis by Intestinal Short-Chain Fatty Acids. Advances in Applied Microbiology 2013;85:93–118.
51. Ussar, S., S. Fujisaka, and C. R. Kahn. Interactions between host genetics and gut microbiome in diabetes and metabolic syndrome. Molecular metabolism 2016;5(9):795–803.
52. Vainio, O., and B. A. Imhof. The immunology and developmental biology of the chicken. Immunology today 1995;16(8):365–370.
53. Wu, W., J. Hu, H. Gao, H. Chen, X. Fang, H. Mu, et al. The potential cholesterol-lowering and prebiotic effects of bamboo shoot dietary fibers and their structural characteristics. Food chemistry 2020;332:127372.
54. Xiao, Y., Y. Xiang, W. Zhou, J. Chen, K. Li, and H. Yang. Microbial community mapping in intestinal tract of broiler chicken. Poultry science 2017;96(5):1387–1393.
55. Zhai, Q., Q. Zhang, F. Tian, J. Zhao, H. Zhang, and W. Chen. The synergistic effect of Lactobacillus plantarum CCFM242 and zinc on ulcerative colitis through modulating intestinal homeostasis. Food & Function 2019;10
56. Zhao, Guanghe, Zhang, Ruifen, Dong, Lihong, Huang, Fei, Tang, and Xiaojun. Particle size of insoluble dietary fiber from rice bran affects its phenolic profile, bioaccessibility and functional properties. Lwt Food Science & Technology 2018.
57. Zhao, J., G. Zhang, W. Dong, Y. Zhang, J. Wang, L. Liu, and S. Zhang. Effects of dietary particle size and fiber source on nutrient digestibility and short chain fatty acid production in cannulated growing pigs. Animal Feed Science and Technology 2019;258:114310.
58. Zhou, X. L., X. F. Kong, G. Q. Lian, F. Blachier, M. M. Geng, and Y. L. Yin. Dietary supplementation with soybean oligosaccharides increases short-chain fatty acids but decreases protein-derived catabolites in the intestinal luminal content of weaned Huanjiang mini-piglets. Nutr Res 2014;34(9):780–788.

Tables

Table 1 Composition and nutrition level of the diet in three groups (as-fed basis, g/kg)

*: Premix supplies the following nutrients (per kilogram of diet): vitamin A (retinyl acetate), 10,000 IU; vitamin D3 (cholecalciferol), 2,500 IU; vitamin E (dl-α-tocopheryl acetate), 40 IU; vitamin K3 (menadione sodium bisulfite), 2 mg; vitamin B1 (thiamine), 2 mg; vitamin B2 (riboflavin), 6 mg; vitamin B3 (niacin), 50 mg; vitamin B5(calcium d-pantothenate), 12 mg; vitamin B6 (pyridoxine hydrochloride), 5 mg; vitamin B12 (cyanocobalamin), 0.02 mg; biotin, 0.12 mg; folic acid, 1.5 mg; choline chloride, 600 mg; Mn(MnSO₄∙H₂O), 80 mg; Fe(FeSO₄∙7H₂O), 80 mg; Zn (sulphate and oxide) 60 mg; Cu(CuSO₄∙5H₂O), 8 mg; I (iodide), 1 mg; Se(Na₂SeO₃), 0.3 mg; Co (cobalt), 0.3 mg;NaCl, 3 g; antioxidant, 40 mg. 

Table 2. Effect of dietary fiber on organ indexes of broilers

Note: Different superscript letters indicate significant difference (P < 0.05). Data are presented as Mean ± SD (n=8).