Dietary sodium butyrate improves female broiler breeder performance and offspring immune function by enhancing maternal intestinal barrier and microbiota.
Dietary sodium butyrate improves female broiler breeder performance and offspring immune function by enhancing maternal intestinal barrier and microbiota.pdf
broiler breeder; gut microbiota; offspring; reproductive performance; sodium butyrate; Antioxidants; Butyric Acid; Sodium, Dietary; Sodium Chloride, Dietary; Animals; Female; Chickens/physiology; Diet/veterinary; Animal Feed/analysis; Immunity; Dietary Supplements/analysis; Microbiota; Animal Science and Zoology; General Medicine
Abstract :
[en] This study aimed to investigate the effects of dietary sodium butyrate (SB) supplementation on the reproductive performance of female broiler breeders under intensive rearing conditions and to analyze antioxidant capacity, immune function, and intestinal barrier function of the female breeders and their offspring. A total of 96,000 40-wk-old Ross308 female broiler breeders were divided into the control (CON) and SB groups, each with 6 replicates of 8,000 birds. Each house with similar production performance characteristics was considered a replicate. The experiment lasted for 20 wk, whereupon sampling took place. Results showed that SB improved the egg production performance, egg quality of broiler breeders, and hatchability (P < 0.05). Maternal supplementation with SB substantially increased serum immunoglobulin A levels in broiler breeders and offspring (both P = 0.04) and offspring immunoglobulin G (P < 0.001). The levels of interleukin-1β (P < 0.001) and interleukin-4 (P = 0.03) in the offspring were downregulated, while the total superoxide dismutase in the offspring and the eggs increased (P < 0.05). The serum biochemical components in breeders and offspring were altered by SB, as evidenced by the reduction in triglycerides, total cholesterol, and high- and low-density lipoproteins (P < 0.05). The intestinal morphology of broiler breeders and offspring also improved by the SB with the decreasing the jejunal crypt depth (P = 0.04) and increasing villus height in offspring (P = 0.03). Maternal jejunal and ileal intestinal barrier-related genes were also shown to be significantly affected by SB. Furthermore, SB altered the microbial diversity in maternal cecal contents, thus increasing the abundance of Lachnospiraceae (P = 0.004) and Ruminococcaceae (P = 0.03). Dietary SB enhanced the reproductive performance and egg quality of broiler breeders and improved the antioxidant capacity and immune function of broiler breeders and offspring, with the benefits potentially arising from the regulation of the maternal intestinal barrier and gut microbiota by SB.
Disciplines :
Agriculture & agronomy
Author, co-author :
Xiao, Chuanpi ; Université de Liège - ULiège > TERRA Research Centre
Zhang, Li; Key Laboratory of Efficient Utilization of Non-grain Feed Resources, Department of Animal Science, Shandong Agricultural University, Taian, Shandong, China
Zhang, Bo; Adisseo Life Science Products (Shanghai) Co. Ltd., Shanghai, China
Kong, Linglian; Key Laboratory of Efficient Utilization of Non-grain Feed Resources, Department of Animal Science, Shandong Agricultural University, Taian, Shandong, China
Pan, Xue; Key Laboratory of Efficient Utilization of Non-grain Feed Resources, Department of Animal Science, Shandong Agricultural University, Taian, Shandong, China
Goossens, Tim; Adisseo France, Hoogveld, Dendermonde, Belgium
Song, Zhigang; Key Laboratory of Efficient Utilization of Non-grain Feed Resources, Department of Animal Science, Shandong Agricultural University, Taian, Shandong, China. Electronic address: zhigangs@sdau.edu.cn
Language :
English
Title :
Dietary sodium butyrate improves female broiler breeder performance and offspring immune function by enhancing maternal intestinal barrier and microbiota.
Abd El-Hack, M.E., Alagawany, M., Mahrose, K.M., Arif, M., Saeed, M., Arain, M.A., Soomro, R.N., Siyal, F.A., Fazlani, S.A., Fowler, J., Productive performance, egg quality, hematological parameters and serum chemistry of laying hens fed diets supplemented with certain fat-soluble vitamins, individually or combined, during summer season. Anim. Nutr. 5 (2019), 49–55.
Alhaj, H.W., Li, Z., Shan, T., Dai, P., Zhu, P., Li, Y., Alsiddig, M.A., Abdelghani, E., Li, C., Effects of dietary sodium butyrate on reproduction in adult breeder roosters. Anim. Reprod. Sci. 196 (2018), 111–119.
Allam-Ndoul, B., Castonguay-Paradis, S., Veilleux, A., Gut microbiota and intestinal trans-epithelial permeability. Int. J. Mol. Sci., 21, 2020, 6402.
Alva-Murillo, N., Medina-Estrada, I., Báez-Magaña, M., Ochoa-Zarzosa, A., López-Meza, J.E., The activation of the TLR2/p38 pathway by sodium butyrate in bovine mammary epithelial cells is involved in the reduction of Staphylococcus aureus internalization. Mol. Immunol. 68 (2015), 445–455.
Alves-Bezerra, M., Cohen, D.E., Triglyceride metabolism in the liver. Compr. Physiol. 8 (2017), 1–8.
Amevor, F.K., Cui, Z., Ning, Z., Shu, G., Du, X., Jin, N., Deng, X., Xu, D., Tian, Y., Zhang, Y., Li, D., Wang, Y., Du, X., Zhao, X., Dietary quercetin and vitamin E supplementation modulates the reproductive performance and antioxidant capacity of aged male breeder chickens. Poult. Sci., 101, 2022, 101851.
Berger, K., Burleigh, S., Lindahl, M., Bhattacharya, A., Patil, P., Stålbrand, H., Nordberg Karlsson, E., Hållenius, F., Nyman, M., Adlercreutz, P., Xylooligosaccharides increase Bifidobacteria and Lachnospiraceae in mice on a high-fat diet, with a concomitant increase in short-chain fatty acids, especially butyric acid. J. Agric. Food Chem. 69 (2021), 3617–3625.
Berghof, T., Parmentier, H., Lammers, A., Transgenerational epigenetic effects on innate immunity in broilers: an underestimated field to be explored?. Poult. Sci. 92 (2013), 2904–2913.
Bindari, Y.R., Gerber, P.F., Centennial review: Factors affecting the chicken gastrointestinal microbial composition and their association with gut health and productive performance. Poult. Sci., 101, 2021, 101612.
Bortoluzzi, C., Pedroso, A.A., Mallo, J.J., Puyalto, M., Kim, W.K., Applegate, T.J., Sodium butyrate improved performance while modulating the cecal microb iota and regulating the expression of intestinal immune-related genes of broiler chickens. Poult. Sci. 96 (2017), 3981–3993.
Dang, G., Wu, W., Zhang, H., Everaert, N., A new paradigm for a new simple chemical: butyrate, and immune regulation. Food Funct. 12 (2021), 12181–12193.
Di Tommaso, N., Gasbarrini, A., Ponziani, F.R., Intestinal barrier in human health and disease. Int. J. Environ. Res. Public Health, 18, 2021, 12836.
Estaki, M., Pither, J., Baumeister, P., Little, J.P., Gill, S.K., Ghosh, S., Ahmadi-Vand, Z., Marsden, K.R., Gibson, D.L., Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions. Microbiome, 4, 2016, 42.
Fan, H., Lv, Z., Gan, L., Guo, Y., Transcriptomics-related mechanisms of supplementing laying broiler breeder hens with dietary daidzein to improve the immune function and growth performance of offspring. J. Agric. Food Chem. 66 (2018), 2049–2060.
Fellows, R., Denizot, J., Stellato, C., Cuomo, A., Jain, P., Stoyanova, E., Balázsi, S., Hajnády, Z., Liebert, A., Kazakevych, J., Blackburn, H., Corrêa, R.O., Fachi, J.L., Sato, F.T., Ribeiro, W.R., Ferreira, C.M., Perée, H., Spagnuolo, M., Mattiuz, R., Matolcsi, C., Guedes, J., Clark, J., Veldhoen, M., Bonaldi, T., Vinolo, M.A.R., Varga-Weisz, P., Microbiota derived short chain fatty acids promote histone crotonylation in the colon through histone deacetylases. Nat. Commun., 9, 2018, 105.
Gabbianelli, R., Bordoni, L., Morano, S., Calleja-Agius, J., Lalor, J.G., Nutri-epigenetics and gut microbiota: how birth care, bonding and breastfeeding can influence and be influenced?. Int. J. Mol. Sci., 21, 2020, 5032.
Ghanim, M.B., isihak, f.a., Influence of sodium butyrate on provoke of immune response in vaccinated broilers with avian influenza (H9N2) vaccines. Egypt. J. Vet. Sci. 53 (2022), 381–389.
Gommers, L.M.M., van der Wijst, J., Bos, C., Janssen, L.A.M., Bindels, R.J.M., de Baaij, J.H.F., Hoenderop, J.G.J., Colonic expression of calcium transporter TRPV6 is regulated by dietary sodium butyrate. Pflug. Arch.: Eur. J. Physiol. 474 (2022), 293–302.
Gong, H., Wu, M., Lang, W., Yang, M., Wang, J., Wang, Y., Zhang, Y., Zheng, X., Effects of laying breeder hens dietary β-carotene, curcumin, allicin, and sodium butyrate supplementation on the growth performance, immunity, and jejunum morphology of their offspring chicks. Poult. Sci. 99 (2020), 151–162.
Guilloteau, P., Martin, L., Eeckhaut, V., Ducatelle, R., Zabielski, R., Van Immerseel, F., From the gut to the peripheral tissues: the multiple effects of butyrate. Nutr. Res. Rev. 23 (2010), 366–384.
Huang, P., Zhang, Y., Xiao, K., Jiang, F., Wang, H., Tang, D., Liu, D., Liu, B., Liu, Y., He, X., Liu, H., Liu, X., Qing, Z., Liu, C., Huang, J., Ren, Y., Yun, L., Yin, L., Lin, Q., Zeng, C., Su, X., Yuan, J., Lin, L., Hu, N., Cao, H., Huang, S., Guo, Y., Fan, W., Zeng, J., The chicken gut metagenome and the modulatory effects of plant-derived benzylisoquinoline alkaloids. Microbiome, 6, 2018, 211.
Iqbal, J., Khan, S.H., Mukhtar, N., Ahmed, T., Pasha, R.A., Effects of egg size (weight) and age on hatching performance and chick quality of broiler breeder. J. Appl. Anim. Res. 44 (2016), 54–64.
Jazi, V., Foroozandeh, A.D., Toghyani, M., Dastar, B., Rezaie Koochaksaraie, R., Toghyani, M., Effects of Pediococcus acidilactici, mannan-oligosaccharide, butyric acid and their combination on growth performance and intestinal health in young broiler chickens challenged with Salmonella Typhimurium. Poult. Sci. 97 (2018), 2034–2043.
Kim, H.S., Whon, T.W., Sung, H., Jeong, Y.S., Jung, E.S., Shin, N.R., Hyun, D.W., Kim, P.S., Lee, J.Y., Lee, C.H., Bae, J.W., Longitudinal evaluation of fecal microbiota transplantation for ameliorating calf diarrhea and improving growth performance. Nat. Commun., 12, 2021, 161.
Kim, Y.J., Youk, S., Song, C.S., Effectiveness of administering a mixture of actic acid bacteria to control salmonella ser. Enteritidis infections in broilers. Animals (Basel), 12, 2022, 374.
Ki-Moon, P., Yan-Hua, J., Kyun-Taek, L., Won-Ik, L., Sung-Woo, N., Yung-Keun, H., Influence of Epimedium koreanum on the performance of laying hens, egg quality, and fat-soluble vitamin and cholesterol contents in the yolk. J. Med. Plants Res. 4 (2010), 1971–1976.
Kong, L., Wang, Z., Xiao, C., Zhu, Q., Song, Z., Glycerol monolaurate attenuated immunological stress and intestinal mucosal injury by regulating the gut microbiota and activating AMPK/Nrf2 signaling pathway in lipopolysaccharide-challenged broilers. Anim. Nutr. 10 (2022), 347–359.
Lan, R.X., Li, S.Q., Zhao, Z., An, L.L., Sodium butyrate as an effective feed additive to improve growth performance and gastrointestinal development in broilers. Vet. Med. Sci. 6 (2020), 491–499.
Liu, J., Bayir, H., Cosby, D., Cox, N., Williams, S., Fowler, J., Evaluation of encapsulated sodium butyrate on growth performance, energy digestibility, gut development, and Salmonella colonization in broilers. Poult. Sci. 96 (2017), 3638–3644.
Luu, M., Pautz, S., Kohl, V., Singh, R., Romero, R., Lucas, S., Hofmann, J., Raifer, H., Vachharajani, N., Carrascosa, L.C., Lamp, B., Nist, A., Stiewe, T., Shaul, Y., Adhikary, T., Zaiss, M.M., Lauth, M., Steinhoff, U., Visekruna, A., The short-chain fatty acid pentanoate suppresses autoimmunity by modulating the metabolic-epigenetic crosstalk in lymphocytes. Nat. Commun., 10, 2019, 760.
Ma, X., Zhou, Z., Zhang, X., Fan, M., Hong, Y., Feng, Y., Dong, Q., Diao, H., Wang, G., Sodium butyrate modulates gut microbiota and immune response in colorectal cancer liver metastatic mice. Cell Biol. Toxicol. 36 (2020), 509–515.
Magdy, O.S., Moussa, I.M., Hussein, H.A., El-Hariri, M.D., Ghareeb, A., Hemeg, H.A., Al-Maary, K.S., Mubarak, A.S., Alwarhi, W.K., Eljakee, J.K., Kabli, S.A., Genetic diversity of Salmonella enterica recovered from chickens farms and its potential transmission to human. J. Infect. Public Health 13 (2020), 571–576.
Maina, A.N., Thanabalan, A., Gasarabwe, J., Mohammadigheisar, M., Schulze, H., Kiarie, E.G., Enzymatically treated yeast bolstered growth performance of broiler chicks from young broiler breeders linked to improved indices of intestinal function, integrity, and immunity. Poult. Sci., 101, 2022, 102175.
Nabi, F., Arain, M.A., Rajput, N., Alagawany, M., Soomro, J., Umer, M., Soomro, F., Wang, Z., Ye, R., Liu, J., Health benefits of carotenoids and potential application in poultry in dustry: a review. J. Anim. Physiol. Animnutr. 104 (2020), 1809–1818.
Naghizadeh, M., Klaver, L., Schönherz, A.A., Rani, S., Dalgaard, T.S., Engberg, R.M., Impact of dietary sodium butyrate and salinomycin on performance and I ntestinal microbiota in a broiler gut leakage model. Animals, 12, 2022, 111.
Peng, L., He, Z., Chen, W., Holzman, I.R., Lin, J., Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr. Res. 61 (2007), 37–41.
Schoeler, M., Caesar, R., Dietary lipids, gut microbiota and lipid metabolism. Rev. Endocr. Metab. Dis. 20 (2019), 461–472.
Shen, Y., Fan, X., Zhang, L., Wang, Y., Li, C., Lu, J., Zha, B., Wu, Y., Chen, X., Zhou, J., Jia, W., Thresholds of glycemia and the outcomes of COVID-19 complicated with diabetes: a retrospective exploratory study using continuous glucose monitoring. Diabetes Care 44 (2021), 976–982.
Shi, N., Li, N., Duan, X., Niu, H., Interaction between the gut microbiome and mucosal immune system. Military Med. Res., 4, 2017, 14.
Song, B., Li, H., Wu, Y., Zhen, W., Wang, Z., Xia, Z., Guo, Y., Effect of microencapsulated sodium butyrate dietary supplementation on growth performance and intestinal barrier function of broiler chickens infected with necrotic enteritis. Anim. Feed Sci. Tech. 232 (2017), 6–15.
Stacchiotti, V., Rezzi, S., Eggersdorfer, M., Galli, F., Metabolic and functional interplay between gut microbiota and fat-soluble vitamins. Crit. Rev. Food Sci. Nutr. 61 (2021), 3211–3232.
Šuligoj, T., Vigsnæs, L.K., Abbeele, P.V.D., Apostolou, A., Karalis, K., Savva, G.M., McConnell, B., Juge, N., Effects of human milk oligosaccharides on the adult gut microbiota and barrier function. Nutrients, 12, 2020, 2808.
Sun, B., Jia, Y., Yang, S., Zhao, N., Hu, Y., Hong, J., Gao, S., Zhao, R., Sodium butyrate protects against high-fat diet-induced oxidative stress in rat liver by promoting expression of nuclear factor E2-related factor 2. Br. J. Nutr. 122 (2019), 400–410.
Sun, C., Tian, X., Lee, Y.S., Gunti, S., Lipsky, A., Herman, S.E., Salem, D., Stetler-Stevenson, M., Yuan, C., Kardava, L., Moir, S., Maric, I., Valdez, J., Soto, S., Marti, G.E., Farooqui, M.Z., Notkins, A.L., Wiestner, A., Aue, G., Partial reconstitution of humoral immunity and fewer infections in patients with chronic lymphocytic leukemia treated with ibrutinib. Blood 126 (2015), 2213–2219.
Swaggerty, C.L., Byrd, 2nd, J.A., Arsenault, R.J., Perry, F., Johnson, C.N., Genovese, K.J., He, H., Kogut, M.H., Piva, A., Grilli, E., A blend of microencapsulated organic acids and botanicals reduces necrotic enteritis via specific signaling pathways in broilers. Poult. Sci., 101, 2022, 101753.
Tan, Z., Halter, B., Liu, D., Gilbert, E.R., Cline, M.A., Dietary flavonoids as modulators of lipid metabolism in poultry. Front. Physiol., 13, 2022, 863860.
Verwoolde, M.B., Arts, J., Jansen, C.A., Parmentier, H.K., Lammers, A., Transgenerational effects of maternal immune activation on specific antibody responses in layer chickens. Front. Vet. Sci., 9, 2022, 832130.
Wang, Y., Wang, G., Li, Y., Zhu, Q., Shen, H., Gao, N., Xiao, J., Structural insights into secretory immunoglobulin A and its interaction with a pneumococcal adhesin. Cell Res. 30 (2020), 602–609.
Wang, Y., Wang, Y., Lin, X., Gou, Z., Fan, Q., Jiang, S., Effects of clostridium butyricum, sodium butyrate, and butyric acid glycerides on the reproductive performance, egg quality, intestinal health, and offspring performance of yellow-feathered breeder hens. Front. Microbiol., 12, 2021, 657542.
Wang, X., Zhang, H., Sapio, R., Yang, J., Wong, J., Zhang, X., Guo, J.Y., Pine, S., Van Remmen, H., Li, H., White, E., Liu, C., Kiledjian, M., Pestov, D.G., Steven Zheng, X.F., SOD1 regulates ribosome biogenesis in KRAS mutant non-small cell lung cancer. Nat. Commun., 12, 2021, 2259.
Wu, Z., Yang, K., Zhang, A., Chang, W., Zheng, A., Chen, Z., Cai, H., Liu, G., Effects of Lactobacillus acidophilus on the growth performance, immune response, and intestinal barrier function of broiler chickens challenged with Escherichia coli O157. Poult. Sci., 100, 2021, 101323.
Zou, X., Ji, J., Qu, H., Wang, J., Shu, D.M., Wang, Y., Liu, T.F., Li, Y., Luo, C.L., Effects of sodium butyrate on intestinal health and gut microbiota composition during intestinal inflammation progression in broilers. Poult. Sci. 98 (2019), 4449–4456.