In ovo sodium butyrate administration differentially impacts growth performance, intestinal barrier function, immune response, and gut microbiota characteristics in low and high hatch-weight broilers. - 2024
In ovo sodium butyrate administration differentially impacts growth performance, intestinal barrier function, immune response, and gut microbiota characteristics in low and high hatch-weight broilers.
Akram, Muhammad Zeeshan; Everaert, Nadia; Dunisławska, Aleksandra
2024 • In Journal of Animal Science and Biotechnology, 15 (1), p. 165
Broiler production; Flock uniformity; Gut health; In ovo stimulation; Microbiome; Biotechnology; Food Science; Biochemistry; Animal Science and Zoology
Abstract :
[en] [en] BACKGROUND: Hatch weight (HW) affects broiler growth and low HW (LHW) often leads to suboptimal performance. Sodium butyrate (SB) has been shown to promote growth through enhanced intestinal health. This study investigated how broilers with different HW responded to in ovo SB injection and whether SB could enhance gut health and performance in LHW chicks. Ross 308 broiler eggs were injected on incubation d 12 with physiological saline (control) or SB at 0.1% (SB1), 0.3% (SB3), or 0.5% (SB5). Post-hatch, male chicks from each treatment were categorized as high HW (HHW) or LHW and assigned to 8 groups in a 4 × 2 factorial design. Production parameters were recorded periodically. Intestinal weight, length, and gene expression related to gut barrier function and immune response were examined on d 14 and 42. Cecal microbiota dynamics and predicted functionality were analyzed using 16S rRNA gene sequencing.
RESULTS: SB treatments did not affect hatchability. HHW-control group exhibited consistently better weight gain and FCR than LHW-control group. SB dose-dependently influenced performance and gut health in both HW categories, with greater effects in LHW broilers at 0.3%. LHW-SB3 group attained highest body weight on d 42, exceeding controls but not significantly differing from HHW-SB3 group. LHW-SB3 group showed upregulation of gut-barrier genes CLDN1 in ileum, TJP1 in jejunum and anti-inflammatory cytokine IL-10 in both jejunum and ileum on d 14. Additionally, LHW-SB3 group upregulated mucin-producing MUC6 gene in ileum, while HHW-SB5 group increased pro-inflammatory IL-12p40 cytokine in caecum on d 42. LHW-SB3 group demonstrated shorter relative intestinal lengths, while HHW-SB5 had longer lengths. HHW-control group had higher bacterial diversity and growth-promoting bacteria while LHW-control group harbored the potential pathogen Helicobacter. SB reshaped gut microbiota biodiversity, composition, and predicted metabolic pathways in both HW categories. The LHW-SB3 group exhibited highest alpha diversity on d 14 and most beneficial bacteria at all timepoints. HHW-SB5 group presented increased pathogenic Escherichia-Shigella and Campylobacter on d 42.
CONCLUSIONS: HW significantly affects subsequent performance and SB has differential effects based on HW. LHW chicks benefited more from 0.3% SB, showing improvements in growth, intestinal development, health, and gut microbiota characteristics.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Akram, Muhammad Zeeshan ; Université de Liège - ULiège > TERRA Research Centre ; Department of Biosystems, Nutrition and Animal-Microbiota Ecosystems Laboratory, KU Leuven, Heverlee, 3001, Belgium
Everaert, Nadia; Department of Biosystems, Nutrition and Animal-Microbiota Ecosystems Laboratory, KU Leuven, Heverlee, 3001, Belgium
Dunisławska, Aleksandra; Department of Animal Biotechnology and Genetics, Faculty of Animal Breeding and Biology, Bydgoszcz University of Science and Technology, Bydgoszcz, 85-084, Poland. aleksandra.dunislawska@pbs.edu.pl
Language :
English
Title :
In ovo sodium butyrate administration differentially impacts growth performance, intestinal barrier function, immune response, and gut microbiota characteristics in low and high hatch-weight broilers.
The Minister of Science (Poland) financially supported article publication charges under the program \"Regional Initiative of Excellence\" (RID/SP/0017/2024/01). Muhammad Zeeshan Akram has received funding from the European Union\u2019s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie Grant Agreement No. 955374.
A.H. Nawaz K. Amoah Q.Y. Leng J.H. Zheng W.L. Zhang L. Zhang Poultry response to heat stress: its physiological, metabolic, and genetic implications on meat production and quality including strategies to improve broiler production in a warming world Front Vet Sci 2021 8 699081 10.3389/fvets.2021.699081 34368284 8342923
R. Lundberg C. Scharch D. Sandvang The link between broiler flock heterogeneity and cecal microbiome composition Anim Microbiome 2021 3 54 1:CAS:528:DC%2BB38XhtlCqtL%2FL 10.1186/s42523-021-00110-7 34332648 8325257
M.Z. Akram E.A. Sureda L. Comer M. Corion N. Everaert Assessing the impact of hatching system and body weight on the growth performance, caecal short-chain fatty acids, and microbiota composition and functionality in broilers Anim Microbiome 2024 6 41 1:CAS:528:DC%2BB2cXhs1ajtbvF 10.1186/s42523-024-00331-6 39049129 11271025
Jacobs L. Road to better welfare - welfare of broiler chickens during transportation, doctoral thesis. Merelbeke: Ghent University, Faculty of Veterinary Medicine; 2016. http://hdl.handle.net/1854/LU-8502274.
Y.P. Chen X. Chen H. Zhang Y.M. Zhou Effects of dietary concentrations of methionine on growth performance and oxidative status of broiler chickens with different hatching weight Br Poult Sci 2013 54 4 531 537 1:CAS:528:DC%2BC3sXpvFSnsbg%3D 10.1080/00071668.2013.809402 23906221
P.M. Singh S.S. Nagra Effect of day-old chick weight and gender on the performance of commercial broiler Indian J Anim Sci 2006 76 12 1043 1046
X. Zhang M. Akhtar Y. Chen Z. Ma Y. Liang D. Shi et al. Chicken Jejunal microbiota improves growth performance by mitigating intestinal inflammation Microbiome 2022 10 107 1:CAS:528:DC%2BB38XitVGgsL%2FJ 10.1186/s40168-022-01299-8 35836252 9284917
Akram MZ, Sureda EA, Corion M, Comer L, Everaert N. Linking gastrointestinal tract structure, function, and gene expression signatures to growth variability in broilers: a novel interpretation for flock uniformity. Poult Sci. 2024;103(10):104158. https://doi.org/10.1016/j.psj.2024.104158.
W. Wu Z. Xiao W. An Y. Dong B. Zhang Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers PLoS ONE 2018 13 5 e0197762 1:CAS:528:DC%2BC1cXhvVGgu7%2FL 10.1371/journal.pone.0197762 29795613 5967726
A. Sikandar H. Zaneb M. Younus S. Masood A. Aslam F. Khattak et al. Effect of sodium butyrate on performance, immune status, microarchitecture of small intestinal mucosa and lymphoid organs in broiler chickens Asian-Australasian J Anim Sci 2017 30 5 690 699 1:CAS:528:DC%2BC1MXnvFGgsg%3D%3D 10.5713/ajas.16.0824
S.N. Qaisrani M.M. van Krimpen R.P. Kwakkel M.W.A. Verstegen W.H. Hendriks Diet structure, butyric acid, and fermentable carbohydrates influence growth performance, gut morphology, and cecal fermentation characteristics in broilers Poult Sci 2015 94 9 2152 64 1:CAS:528:DC%2BC2sXhvFGhtrvM 10.3382/ps/pev003 26175052 4988549
Sunkara LT, Achanta M, Schreiber NB, Bommineni YR, Dai G, Jiang W, et al. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLoS ONE. 2011;6(11):e27225. https://doi.org/10.1371/journal.pone.0027225.
Xu J, Chen X, Yu S, Su Y, Zhu W. Effects of early intervention with sodium butyrate on gut microbiota and the expression of inflammatory cytokines in neonatal piglets. PLoS ONE. 2016;11(9):e0162461. https://doi.org/10.1371/journal.pone.0162461.
C.L. Fang H. Sun J. Wu H.H. Niu J. Feng Effects of sodium butyrate on growth performance, haematological and immunological characteristics of weanling piglets J Anim Physiol Anim Nutr 2014 98 4 680 685 1:CAS:528:DC%2BC2cXhtFajtL%2FL 10.1111/jpn.12122
Zhang Q, Zhang K, Wang J, Bai S, Zeng Q, Peng H, et al. Effects of coated sodium butyrate on performance, egg quality, nutrient digestibility, and intestinal health of laying hens. Poult Sci. 2022;101(9):102020. https://doi.org/10.1016/j.psj.2022.102020.
S.S. Elnesr M. Alagawany H.A.M. Elwan M.A. Fathi M.R. Farag Effect of sodium butyrate on intestinal health of poultry-a review Ann Anim Sci 2020 20 1 29 41 1:CAS:528:DC%2BB3cXitlGmsLs%3D 10.2478/aoas-2019-0077
C.A. Ficagna G.M. Galli E. Zatti B.M. Sponchiado B.G. Cecere G.L. Deolindo et al. Butyric acid glycerides in the diet of broilers to replace conventional growth promoters: effects on performance, metabolism, and intestinal health Arch Anim Nutr 2022 76 191 204 1:CAS:528:DC%2BB3sXit1Kjsbs%3D 10.1080/1745039X.2022.2162796 36688467
J.E. De Oliveira Z. Uni P.R. Ferket Important metabolic pathways in poultry embryos prior to hatch Worlds Poult Sci J 2008 64 4 488 99 10.1017/S0043933908000160
M.A. Schilling R. Katani S. Memari M. Cavanaugh J. Buza J. Radzio-Basu et al. Transcriptional innate immune response of the developing chicken embryo to newcastle disease virus infection Front Genet 2018 9 61 1:CAS:528:DC%2BC1cXit1egsLrO 10.3389/fgene.2018.00061 29535762 5835104
F.T. Akinyemi J. Ding H. Zhou K. Xu C. He C. Han et al. Dynamic distribution of gut microbiota during embryonic development in chicken Poult Sci 2020 99 10 5079 5090 1:CAS:528:DC%2BB3MXhtl2qsLrP 10.1016/j.psj.2020.06.016 32988546 7598139
Wishna-Kadawarage RN, Połtowicz K, Dankowiakowska A, Hickey RM, Siwek M. Prophybiotics for in-ovo stimulation; validation of effects on gut health and production of broiler chickens. Poult Sci. 2024;103(4):103512. https://doi.org/10.1016/j.psj.2024.103512.
A. Dunisławska J. Biesek M. Adamski Growth performance, carcass composition, and qualitative meat features of broiler chickens after galactooligosaccharides and sodium butyrate in ovo administration Poult Sci 2024 103 10 104094 1:CAS:528:DC%2BB2cXhs1yjt7vP 10.1016/j.psj.2024.104094 39096828 11345557
Council of the European Union. Council Regulation (EC) 1099/2009 of 24 September 2009 on the protection of animals at the time of killing. Off J Eur Union. 2009;1–30. https://eur-lex.europa.eu/legal-content/EN/ALL/?uri=celex%3A32009R1099. Assessed 26 Aug 2024.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative pcr and the 2–∆∆ct method. Methods. 2001;25(4):402–8. https://doi.org/10.1006/meth.2001.1262.
Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.
R. Caspi R. Billington I.M. Keseler A. Kothari M. Krummenacker P.E. Midford et al. The MetaCyc database of metabolic pathways and enzymes-a 2019 update Nucleic Acids Res 2020 48 D1 445 453 1:CAS:528:DC%2BB3cXhslWlt77I 10.1093/nar/gkz862
Wen C, Wu P, Chen Y, Wang T, Zhou Y. Methionine improves the performance and breast muscle growth of broilers with lower hatching weight by altering the expression of genes associated with the insulin-like growth factor-I signalling pathway. Br J Nutr. 2014;111(2):201–6. https://doi.org/10.1017/S0007114513002419.
A. Salahi S.G. Adabi M.M. Khabisip A. Anissian R.G. Cooper Effect of in ovo administration of butyric acid into broiler breeder eggs on chicken small intestine pH and morphology Slovak J Anim Sci 2015 48 1 8 15
A. Salahi S.N. Mousavi F. Foroudi M.M. Khabisi M. Norozi Effects of in ovo injection of butyric acid in broiler breeder eggs on hatching parameters, chick quality and performance Glob Vet 2011 7 5 468 477 1:CAS:528:DC%2BC3MXhs1Kht77N
C. Pineda-Quiroga R. Atxaerandio R. Ruiz A. García-Rodríguez Effects of dry whey powder alone or combined with calcium butyrate on productive performance, duodenal morphometry, nutrient digestibility, and ceca bacteria counts of broiler chickens Livest Sci 2017 206 65 70 10.1016/j.livsci.2017.10.001
B. Song H. Li Y. Wu W. Zhen Z. Wang Z. Xia et al. Effect of microencapsulated sodium butyrate dietary supplementation on growth performance and intestinal barrier function of broiler chickens infected with necrotic enteritis Anim Feed Sci Technol 2017 232 6 15 1:CAS:528:DC%2BC2sXht1ylt7fP 10.1016/j.anifeedsci.2017.07.009
S. Adil T. Banday G.A. Bhat M.S. Mir M. Rehman Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and serum biochemistry of broiler chicken Vet Med Int 2010 2010 479485 10.4061/2010/479485 20613998 2896631
Makowski Z, Lipiński K, Mazur-Kuśnirek M. The effects of sodium butyrate, coated sodium butyrate, and butyric acid glycerides on nutrient digestibility, gastrointestinal function, and fecal microbiota in turkeys. Animals. 2022;12(14):1836. https://doi.org/10.3390/ani12141836.
N. Hosseini-Mansoub K. Rahimpour L. Majedi asl M. Ali Mohammad Nezhady S. Lale Zabihi M. Mohammadi Kalhori Effect of different level of butyric acid glycerides on performance and serum composition of broiler chickens World J Zool 2011 6 2 179 82
A. Pascual A. Trocino M. Birolo B. Cardazzo F. Bordignon C. Ballarin et al. Dietary supplementation with sodium butyrate: growth, gut response at different ages, and meat quality of female and male broiler chickens Ital J Anim Sci 2020 19 1 1134 1145 10.1080/1828051X.2020.1824590
S. Smulikowska J. Czerwinski A. Mieczkowska J. Jankowiak The effect of fat-coated organic acid salts and a feed enzyme on growth performance, nutrient utilization, microflora activity, and morphology of the small intestine in broiler chickens J Anim Feed Sci 2009 18 3 478 489 10.22358/jafs/66422/2009
W.H. Zhang Y. Jiang Q.F. Zhu F. Gao S.F. Dai J. Chen et al. Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens Br Poult Sci 2011 52 3 292 301 1:CAS:528:DC%2BC3MXovVensrs%3D 10.1080/00071668.2011.578121 21732874
S. Sengupta J.G. Muir P.R. Gibson Does butyrate protect from colorectal cancer? J Gastroenterol Hepatol 2006 21 1 209 218 1:CAS:528:DC%2BD28XjsFOrt7c%3D 10.1111/j.1440-1746.2006.04213.x 16460475
L. Peng Z.R. Li R.S. Green I.R. Holzmanr J. Lin Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in caco-2 cell monolayers J Nutr 2009 139 9 1619 1625 1:CAS:528:DC%2BD1MXhtlWrt7nM 10.3945/jn.109.104638 19625695 2728689
J.D. Liu B. Lumpkins G. Mathis S.M. Williams J. Fowler Evaluation of encapsulated sodium butyrate with varying releasing times on growth performance and necrotic enteritis mitigation in broilers Poult Sci 2019 98 8 3240 3245 1:CAS:528:DC%2BB3cXps1Skt7o%3D 10.3382/ps/pez049 30789214
Sadurní M, Barroeta AC, Sala R, Sol C, Puyalto M, Castillejos L. Impact of dietary supplementation with sodium butyrate protected by medium-chain fatty acid salts on gut health of broiler chickens. Animals. 2022;12(19):2496. https://doi.org/10.3390/ani12192496.
V. Lorén E. Cabré I. Ojanguren E. Domènech E. Pedrosa A. García-Jaraquemada et al. Interleukin-10 enhances the intestinal epithelial barrier in the presence of corticosteroids through p38 MAPK activity in caco-2 monolayers: a possible mechanism for steroid responsiveness in ulcerative colitis PLoS ONE 2015 10 6 e0130921 1:CAS:528:DC%2BC28XntV2gsbw%3D 10.1371/journal.pone.0130921 26090671 4474693
K. Simon G. de Vries Reilingh B. Kemp A. Lammers Development of ileal cytokine and immunoglobulin expression levels in response to early feeding in broilers and layers Poult Sci 2014 93 12 3017 3027 1:CAS:528:DC%2BC28Xhsl2ns7jF 10.3382/ps.2014-04225 25306458
Li MH, Meng JX, Wang W, He M, Zhao ZY, Ma N, et al. Dynamic description of temporal changes of gut microbiota in broilers. Poult Sci. 2022;101(9):102037. https://doi.org/10.1016/j.psj.2022.102037.
G.G. Han E.B. Kim J. Lee J.Y. Lee G. Jin J. Park et al. Relationship between the microbiota in different sections of the gastrointestinal tract, and the body weight of broiler chickens Springerplus 2016 5 911 1:CAS:528:DC%2BC28XhtV2gu7fE 10.1186/s40064-016-2604-8 27386355 4927549
X. Dou Z. Ma D. Yan N. Gao Z. Li Y. Li et al. Sodium butyrate alleviates intestinal injury and microbial flora disturbance induced by lipopolysaccharides in rats Food Funct 2022 13 3 1360 1369 1:CAS:528:DC%2BB38XhtlOrtrw%3D 10.1039/D1FO03183J 35044411
Chen Y, Ni J, Li H. Effect of green tea and mulberry leaf powders on the gut microbiota of chicken. BMC Vet Res. 2019;15:77. https://doi.org/10.1186/s12917-019-1822-z.
Qiu M, Hu J, Peng H, Li B, Xu J, Song X, et al. Research note: the gut microbiota varies with dietary fiber levels in broilers. Poult Sci. 2022;101(7):101922. https://doi.org/10.1016/j.psj.2022.101922.
C.S. Marcolla T. Ju H.L. Lantz B.P. Willing Investigating the cecal microbiota of broilers raised in extensive and intensive production systems Microbiol Spectr 2023 11 5 e02352 02323 1:CAS:528:DC%2BB3sXitlenu7bM 10.1128/spectrum.02352-23 37754552 10581045
Y. Fan T. Ju T. Bhardwaj D.R. Korver B.P. Willing Week-old chicks with high Bacteroides abundance have increased short-chain fatty acids and reduced markers of gut inflammation Microbiol Spectr 2023 11 2 e03616 03622 1:CAS:528:DC%2BB3sXptlOhtrg%3D 10.1128/spectrum.03616-22 36719194 10100795
Zhang B, Lv Z, Li Z, Wang W, Li G, Guo Y. Dietary L-arginine supplementation alleviates the intestinal injury and modulates the gut microbiota in broiler chickens challenged by Clostridium perfringens. Front Microbiol. 2018;9:1716. https://doi.org/10.3389/fmicb.2018.01716.
S. Javed F. Gul K. Javed H. Bokhari Helicobacter pullorum: an emerging zoonotic pathogen Front Microbiol 2017 8 604 10.3389/fmicb.2017.00604 28443081 5385324
T. Fujimoto H. Imaeda K. Takahashi E. Kasumi S. Bamba Y. Fujiyama et al. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn’s disease J Gastroenterol Hepatol 2013 28 4 613 619 1:CAS:528:DC%2BC3sXkvFOgt70%3D 10.1111/jgh.12073 23216550
M. Lopez-Siles S.H. Duncan L.J. Garcia-Gil M. Martinez-Medina Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics ISME J 2017 11 4 841 52 10.1038/ismej.2016.176 28045459 5364359
Anjaria P, Koringa P, Bhavsar P, Soni M, Desai M, Nayak J, et al. Metagenomic analysis reveals the complex microbial landscape of market chicken meat. Indian J Microbiol. 2024. https://doi.org/10.1007/s12088-024-01249-y.
V. Farkas G. Csitári L. Menyhárt N. Such L. Pál F. Husvéth et al. Microbiota composition of mucosa and interactions between the microbes of the different gut segments could be a factor to modulate the growth rate of broiler chickens Animals 2022 12 10 1296 10.3390/ani12101296 35625142 9137591
Song B, He J, Pan X, Kong L, Xiao C, Keerqin C, et al. Dietary extract supplementation improves the growth performance and gut health of broiler chickens with necrotic enteritis. J Anim Sci Biotechnol. 2023;14:113. https://doi.org/10.1186/s40104-023-00916-2.
Zhao W, Huang Y, Cui N, Wang R, Xiao Z, Su X. Glucose oxidase as an alternative to antibiotic growth promoters improves the immunity function, antioxidative status, and cecal microbiota environment in white-feathered broilers. Front Microbiol. 2023;14:1100465. https://doi.org/10.3389/fmicb.2023.1100465.
Narasinakuppe Krishnegowda D, Dhama K, Kumar Mariappan A, Munuswamy P, Iqbal Yatoo M, Tiwari R, et al. Etiology, epidemiology, pathology, and advances in diagnosis, vaccine development, and treatment of Gallibacterium anatis infection in poultry: a review. Vet Q. 2020;40(1):16–34. https://doi.org/10.1080/01652176.2020.1712495.
X. Xu M.J. Rothrock G. Dev Kumar A. Mishra Assessing the risk of seasonal effects of campylobacter contaminated broiler meat prepared in-home in the United States Foods 2023 12 13 2559 10.3390/foods12132559 37444297 10340310
Alberoni D, Gaggìa F, Baffoni L, Modesto MM, Biavati B, Di Gioia D. Bifidobacterium xylocopae sp. nov. and Bifidobacterium aemilianum sp. nov., from the carpenter bee (Xylocopa violacea) digestive tract. Syst Appl Microbiol. 2019;42(2):205–16. https://doi.org/10.1016/j.syapm.2018.11.005.
D.W. Dean T.D. Bidner L.L. Southern Glycine supplementation to low protein, amino acid-supplemented diets supports optimal performance of broiler chicks Poult Sci 2006 85 2 288 296 1:CAS:528:DC%2BD28Xhs1Klurw%3D 10.1093/ps/85.2.288 16523629
M.D. Wheeler K. Ikejema N. Enomoto R.F. Stacklewitz V. Seabra Z. Zhong et al. Glycine: a new anti-inflammatory immunonutrient Cell Mol Life Sci 1999 56 843 856 1:CAS:528:DyaK1MXotVOnurk%3D 10.1007/s000180050030 11212343 11147092