Comparative influence of dietary probiotic, yoghurt, and sodium butyrate on growth performance, intestinal microbiota, blood hematology, and immune response of meat-type chickens

  • M. N. Makled
  • K. F. M. AbouelezzEmail author
  • A. E. G. Gad-Elkareem
  • A. M. Sayed
Regular Articles


This study was conducted to assess the effects of early dietary supplementation with probiotic, yoghurt, and sodium butyrate (SB) on the growth performance, intestinal microbiota, blood hematology, and immune response of broiler chickens. A total of 180 1-day-old SASSO broiler chicks, housed in 12 equal floor pen replicates each of 15 chicks, were assigned randomly to four feeding treatments (three replicates/treatment, n = 45): T1. Basal diet (BD) (control), T2. BD incorporated 1 g of a commercial probiotic per kilogram, T3. BD mixed with 5 g of fresh yoghurt per kilogram, and T4. BD incorporated 0.6 g SB/kg. The experimental birds received the dietary treatments from 1 to 21 days of age. The dietary supplementation (g/kg) with commercial probiotic, yoghurt, and SB during the first 21 days of age did not affect broiler’s growth performance variables at day 42, relative weight of immunity organs, blood hematological indices, or the ileal and cecal bacterial counts at day 42, but increased the serum IgG levels and reduced the cecal aerobes at day 21. The probiotic and yoghurt treatments increased the serum content of antibody titer against Newcastle disease virus and decreased the counts of ileal aerobes and E. coli at day 21, whereas the SB treatment increased the ileal lactobacilli count at day 21. In conclusion, the tested feed additives displayed beneficial impacts on broilers’ gut microbiota at day 21 and serum IgG at day 42, but did not affect the growth performance or blood hematological indices at 42 days of age.


Growth promoters Antibiotic alternatives Immune response Gut microflora Broiler chickens 


Funding information

This work was funded by the Faculty of Agriculture, Assiut University, Assiut, 71526, Egypt.

Compliance with ethical standards

The care and use of experiment birds were performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. This study has been approved by the council of Poultry Production Department, Faculty of Agriculture, Assiut University.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdelqader, A. and Al-Fataftah, A., 2016. Effect of dietary butyric acid on performance, intestinal morphology, microflora composition and intestinal recovery of heat-stressed broilers, Livestock Science, 183, 78–83.CrossRefGoogle Scholar
  2. Abouelezz, K., Abou-Hadied, M., Yuan, J., Elokil, A., Wang, G., Wang, S., Wang, J. and Bian, G., 2019. Nutritional impacts of dietary oregano and Enviva essential oils on the performance, gut microbiota and blood biochemicals of growing ducks, Animal, 1–7.
  3. Adolfsson, O., Meydani S.N. and Russell, R.M., 2004. Yoghurt and gut function, American Journal of Clinical Nutrition, 80, 245–256.CrossRefGoogle Scholar
  4. Ahsan, U., Cengiz, O., Raza, I., Kuter, E., Chacher, M.F.A., Iqbal, Z., Umar, S. and Cakir, S., 2016. Sodium butyrate in chicken nutrition: the dynamics of performance, gut microbiota, gut morphology, and immunity, World’s Poultry Science Journal, 72, 265–275.CrossRefGoogle Scholar
  5. Attia, Y.A., Abd El-Hamid, A.E., Ellakany, H.F., Bovera, F., Al-Harthi, M.A. and Ghazaly, S.A., 2013. Growing and laying performance of Japanese quail fed diet supplemented with different concentrations of acetic acid, Italian Journal of Animal Science, 12, 2. Scholar
  6. Attia, Y.A., Abd Al-Hamid, A.E., Allakany, H.F., Al-Harthi, M.A. and Mohamed, N.A., 2016. Necessity of continuing of supplementation of non-nutritive feed additive during day 21-42 of age following three weeks of feeding aflatoxin to broiler chickens, Journal of Applied Animal Research, 44, 87–98.CrossRefGoogle Scholar
  7. Bai, S., Wu, A., Ding, X., Lei, Y., Bai, J., Zhang, K. and Chio, J., 2013. Effects of probiotic supplemented diets on growth performance and intestinal immune characteristics of broiler chickens, Poultry Science, 92, 663–670.CrossRefGoogle Scholar
  8. Bajagai, Y.S., 2017. Impact of Bacillus amyloliquefaciens probiotic strain H57 on the intestinal microbiota and broiler performance, PhD thesis, University of Queensland, Australia.Google Scholar
  9. Bohoua, G.L., 2008. Effect of palm wine yeasts and yogurt probiotics on the growth performance of broilers, Livestock Research for Rural Development, 20, 47.Google Scholar
  10. Boostani, A., Fard, M.H.R., Ashayerizadeh, A. and Aminafshar, M., 2013. Growth performance, carcass yield and intestinal microflora populations of broilers fed diets containing thepax and yogurt, Brazilian Journal of Poultry Science, 15, 1–6.CrossRefGoogle Scholar
  11. Cao, G.T., Zeng, X.F., Chen, A.G., Zhou, L., Zhang, L., Xiao, Y.P. and Yang, C.M., 2013. Effects of a probiotic, Enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88, Poultry Science, 92, 2949–2955.CrossRefGoogle Scholar
  12. Chamba, F., Puyalto, M., Ortiz, A., Torrealba, H., Mallo, J.J. and Riboty, R., 2014. Effect of partially protected sodium butyrate on performance, digestive organs, intestinal villi and E. coli development in broilers chickens, International Journal of Poultry Science, 13, 390–396.CrossRefGoogle Scholar
  13. Chawla, S., Katoch, S., Sharma, K. and Sharma, V., 2013. Biological response of broiler supplemented with varying dose of direct fed microbial, Veterinary World, 6, 521–524.CrossRefGoogle Scholar
  14. Czerwiński, J,, Højberg, O., Smulikowska, S., Engberg, R.M. and Mieczkowska, A., 2012. Effects of sodium butyrate and salinomycin upon intestinal microbiota, mucosal morphology and performance of broiler chickens, Archives of Animal Nutrition, 66, 102–16.CrossRefGoogle Scholar
  15. Duncan, D.B., 1955. Multiple range and multiple F-Tests, Biometrics, 11, 1–42.CrossRefGoogle Scholar
  16. Eshak, M.G., Elmenawey, M.A., Atta, A., Gharib, H.B., Shalaby, B. and Awaad, M.H.H., 2016. The efficacy of Na-butyrate encapsulated in palm fat on performance of broilers infected with necrotic enteritis with gene expression analysis, Veterinary World, 9, 450–7.CrossRefGoogle Scholar
  17. FAO, 2016. Probiotics in animal nutrition – Production, impact and regulation by Yadav S. Bajagai, Athol V. Klieve, Peter J. Dart and Wayne L. Bryden. Editor Harinder P.S. Makkar. FAO Animal Production and Health Paper No. 179.: Food and Agriculture Organization of the United Nations (FAO), Rome, Italy.Google Scholar
  18. Fudge, A.M., 2000. Avian complete blood count. In: Laboratory medicine-avian and exotic pets. (Fudge A. M., Ed.), WB Saunders company, Philadelphia, USA, 9–18.Google Scholar
  19. Goudswaard, J., Noordzij, A. and Vaerman, J.P., 1977. The immunoglobulins of the turkey (Meleagris gallopavo). Isolation and characterization of IgG, IgM and IgA in body fluids, eggs and intraocular tissues, Poultry science, 56, 1847–1851.CrossRefGoogle Scholar
  20. Haque, M.I., Ahmad, N. and Miah, M.A., 2017. Comparative analysis of body weight and serum biochemistry in broilers supplemented with some selected probiotics and antibiotic growth promoters, Journal of Advanced Veterinary and Animal Research, 4, 288–294.CrossRefGoogle Scholar
  21. Hernandez, J., Afandor, G., Ariza-Nieto, C. and Avellaneda, Y., 2013. Evaluation of coated and powder sodium butyrate in diets for broilers reared with reused litter during a commercial production cycle, Journal of Animal Science, 91, 335.Google Scholar
  22. Houndonougbo, M.F., Chrysostome, C.A.A.M. and Zlao Z., 2011. Tchoukoutou residue and yogurt as feed additives in broilers feed, Research opinions in Animal and Veterinary sciences, 1, 597–600.Google Scholar
  23. Kamboh, A., Hang, S., Khan, M. and Zhu, W., 2016. In vivo immunomodulatory effects of plant flavonoids in lipopolysaccharide-challenged broilers, Animal, 10, 1619–1625.CrossRefGoogle Scholar
  24. Landy, N. and Kavyani, A., 2013. Effects of using a multi-strain probiotic on performance, immune responses and cecal microflora composition in broiler chickens reared under cyclic heat stress condition, Iranian Journal of Applied Animal Science, 3, 703–708.Google Scholar
  25. Mahdavi, R. and Torki, M., 2009. Study on usage period of dietary protected butyric acid on performance, carcass characteristics, serum metabolite levels and humoral immune response of broiler chickens, Journal of Animal Veterinary Advances, 8, 1702–1709.Google Scholar
  26. Mahmmod, Z.A., Abdulrazaq, H.S., Salem, A.S., Sideq, R.H., 2014. Effects of supplementation probiotic and dried yogurt powder on growth performance, carcass characteristics, intestinal micro flora and immunity of broiler chickens, Zanco Journal of Pure and Applied Sciences, 26, 35–42.Google Scholar
  27. Mallo, J.J., Puyalto, M. and Rao, R.S.V., 2012. Evaluation of the effect of sodium butyrate addition to broiler diet on energy and protein digestibility productive parameters and size of intestinal villi of animals, Feed and Livestock, 8, 26–30.Google Scholar
  28. Mansoub, N.H., 2011. Comparative effect of butyric acid, probiotic and garlic on performance and serum composition of broilers chickens, American Eurasian Journal of Agricultural and Environmental Sciences, 11, 507–511.Google Scholar
  29. Mashayekhi, H., Mazhari, M. and Esmaeilipour, O., 2018. Eucalyptus leaves powder, antibiotic and probiotic addition to broiler diets: Effect on growth performance, immune response, blood components and carcass traits, Animal, 12, 2049–2055.CrossRefGoogle Scholar
  30. Monoura, P., Rahman, M., Khan, M.F.R., Rahman, M.B. and Rahman, M.M., 2008. Effect of vitamins, minerals and probiotics on production of antibody and live weight gain following vaccination with BCRDV in broiler birds, Bangladesh Journal of Veterinary Medicine, 6, 31–36.CrossRefGoogle Scholar
  31. Mookiah, S., Sieo, C.C., Ramsamy, K., Abdullah, N. and YW, H.O., 2014. Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens, Journal of the Science of Food and Agriculture, 94, 341–348.CrossRefGoogle Scholar
  32. Moquet, P.C.A., Onrust, L., Van Immerseel, F., Ducatelle, R., Hendriks, W.H. and Kwakkel, R.P., 2016. Importance of release location on the mode of action of butyrate derivatives in the avian gastrointestinal tract, World's Poultry Science Journal, 72, 61–80.CrossRefGoogle Scholar
  33. Mountzouris, K., Tsitrsikos, P., Palmidi, I., Arvaniti, A., Mohnl, M., Schatzmayr, G. and Fegeros, K., 2010. Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition, Poultry Science, 89, 58–67.CrossRefGoogle Scholar
  34. OIE, 2004. Avian influenza. Manual of diagnostic tests and vaccines for terrestrial animals, Accessed 21 January 2018.
  35. Olnood, C.G., Beski, S.S.M., Choct, M. and Iji, P.A., 2015 . Novel probiotics: Their effects on growth performance, gut development, microbial community and activity of broiler chickens, Animal Nutrition, 1, 184–191.CrossRefGoogle Scholar
  36. Qaisrani, S.N., Van Krimpen, M.M., Kwakkel, R.P., Verstegen, M.W.A. and Hendriks, W.H., 2015. Diet structure, butyric acid, and fermentable carbohydrates influence growth performance, gut morphology, and cecal fermentation characteristics in broilers, Poultry Science, 94, 2152–2164.CrossRefGoogle Scholar
  37. Ravindran, V., 2003. Development of digestive function in neonatal poultry: physiological limitations and potential, Proceedings of the 15th Annual Australian Poultry Science Symposium, Sydney, Australia, 1–7.Google Scholar
  38. Shim, Y., Ingale, S,, Kim, J., Kim, K., Seo, D., Lee, S., Chae, B. and Kwon, I., 2012. A multi-microbe probiotic formulation processed at low and high drying temperatures: effects on growth performance, nutrient retention and caecal microbiology of broilers, British Poultry Science, 53, 482–490.CrossRefGoogle Scholar
  39. Sikandar, A., Zaneb, H., Younus, M., Masood, S., Aslam, A., Khattak, F., Ashraf, S., Yousaf, M.S. and Rehman, H., 2017. Effect of sodium butyrate on performance, immune status, microarchitecture of small intestinal mucosa and lymphoid organs in broiler chickens, Asian-Australasian Journal of Animal Science, 30, 690–699.CrossRefGoogle Scholar
  40. Sunkara, L.T., Achanta, M., Schreiber, N.B., Bommineni, Y.R., Dai, G., Jiang, W., Lamont, S., Lillehoj, H.S., Beker, A., Teeter, R.G. and Zhang, G., 2011. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression, PLoS One 6, e27225. Accessed 21 January 2018.CrossRefGoogle Scholar
  41. Thayer, S.G. and Beard, C.W., 1998. Serologic procedures. In: Swayne, D.E., Ed., A Laboratory Manual for the Isolation and Identification of Avian Pathogens, 4th Edition, American Association of Avian Pathologists, Philadelphia, 256–258.Google Scholar
  42. Van Immerseel, F., Fievez, V., De Buck, J., Pasmans, F., Martel, A., Haesebrouck, F. and Ducatelle, R., 2004. Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella Enteritidis in young chickens, Poultry Science, 83, 69–74.CrossRefGoogle Scholar
  43. Wu, W., Xiao, Z., An, W., Dong, Y. and Zhang, B., 2018. Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PloS one, 13, e0197762. Scholar
  44. Zhang, Z. and Kim, I., 2014. Effects of multistrain probiotics on growth performance, apparent ileal nutrient digestibility, blood characteristics, cecal microbial shedding, and excreta odor contents in broilers, Poultry Science, 93, 364–370.CrossRefGoogle Scholar
  45. Zhang, W.H., Jiang, Y., Zhu, Q.F., Gao, F., Dai, S.F., Chen, J. and Zhou, G.H., 2011. Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens, British Poultry Science, 52, 292–301.CrossRefGoogle Scholar
  46. Zou, Y., Yang, Z.B., Yang, W.R., Jiang, S.Z., Zhang, G.G. and YU, R., 2010. Effects of coated sodium butyrate on the performance and gut morphology of broiler chickens, Poultry Science, 89, 385–385.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Poultry Production, Faculty of AgricultureAssiut UniversityAssiutEgypt
  2. 2.Institute of Animal Science, Guangdong Academy of Agricultural Science, Key Laboratory of Animal Nutrition and Feed Science (South China) of Ministry of Agriculture, State Key Laboratory of Livestock and Poultry Breeding, Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangdong Key Laboratory of Animal Breeding and NutritionGuangzhouChina

Personalised recommendations