Milk Kefir as a Natural Probiotic, Individually or in Combination with Organic Acids in Broiler Chickens: Influence on the Immune-Related Gene Expression, Intestinal Morphology, Microbiota Activity, and Serum Biochemistry

Document Type : Original Paper

Authors

1 Department of Biology, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran

2 2Department of Animal Science, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran

3 Department of Animal Science, Qaemshahr Branch, Islamic Azad University, Qaemshahr, Iran

Abstract

The objective of this study was to examine the influence of the addition of milk kefir (MK), as a natural probiotic to drinking water, individually or in combination with organic acids (OA), on the growth performance, intestinal microbial counts and morphology, serum metabolites and immune status in broiler chickens. Two hundred and fifty one-day-old broiler chicks (Ross 308) were randomly distributed into 4 treatment groups including a control group, and the control group with MK (2% of drinking water), OA (350 mL/1000 L of water), or MK+OA. At d 35, Body weight gain, feed intake, and feed conversion ratio were recorded. At the end of the experiment (d 35), five birds per treatment were selected to determine the bacterial population, serum biochemical metabolites, and intestinal morphology. According to the results, water supplemented with MK increased the mRNA levels of IFN-γ and IFN-β at 35 d in the jejunum (P < 0.05). OA supplementation significantly increased the gene expression of IL-6 (P < 0.05). On the other hand, the gene expression of IL-12 increased in broilers fed the control diet (P < 0.05). The broiler chickens that received MK+OA showed an improvement in feed conversion ratio (P < 0.05) compared with OA and control groups. The addition of MK+OA resulted in a higher relative weight of thigh in broiler chickens compared with the MK group (P < 0.05), while the relative weight of spleen was lower in OA and MK treatments compared with the MK+OA group (P < 0.05). The results also indicated that the addition of MK+OA decreased the ileocaecal E. coli population compared to other treatments (P < 0.05). Conversely, the birds that received MK+OA had a higher viable count of ileocaecal lactobacilli (P < 0.05) compared with the OA group. In conclusion, the combination of OA with MK had beneficial effects on the performance, intestinal immune-related genes, and gut microbiota activity of broiler chickens.

Keywords


Adhikari PA & Kim WK. 2017. Overview of prebiotics and probiotics: focus on performance, gut health and immunity–a review. Annals of Animal Science, 17: 949-966. DOI: 10.1515/aoas-2016-0092
Awad W, Ghareeb K, Abdel-Raheem S & Böhm J. 2009. Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poultry Science, 88: 49-56. DOI: 10.3382/ps.2008-00244
Bai S, Wu A, Ding X, Lei Y, Bai J, Zhang K & Chio J. 2013. Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poultry Science, 92: 663-670. DOI: 10.3382/ps.2012-02813
Brisbin JT, Gong J &  Sharif S. 2008. Interactions between commensal bacteria and the gut-associated immune system of the chicken. Animal Health Research Reviews, 9: 101-110. DOI: 10. 1017/S146625230800145X
Chaveerach P, Keuzenkamp DA, Lipman LJA &  Van Knapen F. 2004. Effect of Organic Acids in Drinking Water for Young Broilers on Campylobacter Infection, Volatile Fatty Acid
 
Production, Gut Microflora and Histological Cell Changes. Poultry Science, 83: 330-334. DOI: 10.1093/ps/83.3.330
Cho J, Zhang Z &  Kim I. 2013. Effects of single or combined dietary supplementation of β-glucan and kefir on growth performance, blood characteristics and meat quality in broilers. British Poultry Science, 54: 216-221. DOI: 10.1080/ 00071668.2013.777691
Eftekhari A, Rezaeipour V & Abdullahpour R. 2015. Effects of acidified drinking water on performance, carcass, immune response, jejunum morphology, and microbiota activity of broiler chickens fed diets containing graded levels of threonine. Livestock Science, 180: 158-163. DOI: 10.1016/j.livsci.2015.07.010
Fattahi S, Langroudi MP, Samadani AA, Nikbakhsh N, Asouri M & Akhavan-Niaki H. 2017. Application of unique sequence index (USI) barcode to gene expression profiling in gastric adenocarcinoma. Journal of Cell Communication and Signaling, 11: 97-104. DOI: 10.1007/s12079-017-0376-8
Gadde U, Kim W, Oh S & Lillehoj HS. 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: a review. Animal Health Research Reviews, 1: 26-45. DOI: 10.1017/S1466252316000207
Ghareeb K, Awad WA, Soodoi C, Sasgary S, Strasser A & Böhm, J. 2013. Effects of feed contaminant deoxynivalenol on plasma cytokines and mRNA expression of immune genes in the intestine of broiler chickens. PloS One, 8: e71492. DOI: 10.1371/journal.pone.0071492
Haghighi HR, Abdul-Careem MF, Dara RA, Chambers JR &  Sharif S. 2008. Cytokine geneexpression in chicken cecal tonsils following treatment with probiotics and Salmonella infection. Veterinary Microbiology, 126: 225-233. DOI: 10.1016/j.vetmic.2007.06.026
Hashemi SR, Zulkifli I, Davoodi H, Zunita Z & Ebrahimi M. 2012. Growth performance, intestinal microflora, plasma fatty acid profile in broiler chickens fed herbal plant (Euphorbia hirta) and mix of acidifiers. Animal Feed Science and Technology, 178: 167-174. DOI: 10.1016/ j.anifeedsci.2012.09.006
Hedayati M, Manafi M, Yari M & Avara A. 2014. The influence of an Acidifier feed additive on biochemical parameters and immune response of broilers. Annual Research & Review in Biology, 1637-1645. DOI: 10.9734/ARRB/2014/8210
Kandir EH & Yardimci M. 2015. Effects of Kefir on Growth Performance and Carcass Characteristics in Pekin Ducks (Anas platyrhynchos domestica). Journal of Animal Research, 5: 207. DOI: 10.5958/2277-940X.2015.00035.2
Li LL, Hou ZP, Li TJ, Wu GY, Huang RL, Tang ZR, Yang CB, Gong J, Yu H &  Kong XF. 2008. Effects of dietary probiotic supplementation on ileal digestibility of nutrients and growth performance in 1 to 42dayold broilers. Journal of the Science of Food and Agriculture, 88: 35-42. DOI: 10.1002/jsfa.2910
Li Z, Wang W, Liu D & Guo Y. 2018. Effects of Lactobacillus acidophilus on the growth performance and intestinal health of broilers challenged with Clostridium perfringens. Journal of Animal Science and Biotechnology, 9: 25. DOI: 10.1186/s40104-018-0243-3
Magalhães KT, Dragone G, de Melo Pereira GV, Oliveira JM, Domingues L, Teixeira JA, e Silva JBA &  Schwan RF. 2011. Comparative study of the biochemical changes and volatile compound formations during the production of novel whey-based kefir beverages and traditional milk kefir. Food Chemistry, 126: 249-253. DOI: 10.1016/ j.foodchem.2010.11.012
Mountzouris K, Tsitrsikos P, Palamidi I, Arvaniti A, Mohnl M, Schatzmayr G &  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. DOI: 10.3382/ps.2009-00308
Otutumi LK, De Moraes Garcia E, Góis M& Loddi MM. 2012. Variations on the efficacy of probiotics in poultry. Probiotic in Animals. DOI: 10.5772/50058
Palamidi I, Fegeros K, Mohnl M, Abdelrahman W, Schatzmayr G, Theodoropoulos G & Mountzouris K. 2016. Probiotic form effects on growth performance, digestive function, and immune related biomarkers in broilers. Poultry Science, 95: 1598-1608. DOI: 10.3382/ps/pew052
Ragaa NM & Korany RMS. 2016. Studying the effect of formic acid and potassium diformate on performance, immunity and gut health of broiler chickens. Animal Nutrition, 2: 296-302. DOI: 10. 1016/j.aninu.2016.08.003
Rezaeipour V, Barsalani A & Abdullahpour R. 2016. Effects of phytase supplementation on growth performance, jejunum morphology, liver health, and serum metabolites of Japanese quails fed sesame (Sesamum indicum) meal-based diets containing graded levels of protein. Tropical Animal Health and Production, 48: 1141-1146. DOI: 10.1007/s11250-016-1066-x
Roofchaei A, Rezaeipour V, Vatandour S & Zaefarian F. 2019. Influence of dietary carbohydrases, individually or in combination with phytase or an acidifier, on performance, gut morphology and microbial population in broiler chickens fed a wheat-baseddiet. Animal Nutrition, 5: 63-67. DOI: 10.1016/j.aninu.2017.12.001
Sarkar S. 2008. Biotechnological innovations in kefir production: a review. British Food Journal, 110: 283-295. DOI: 10.1108/00070700810858691
SAS, 1999. 'SAS Statistics User’s Guide. Statistical Analytical System, fifth revised ed. SAS Institute Inc, Carry, NC.
Siriken B, Bayram I &  Önol AG. 2003. Effects of probiotics: alone and in a mixture of Biosacc® plus Zinc Bacitracin on the caecal microflora of Japanese quail. Research in Veterinary Science, 75: 9-14. DOI: 10.1016/S0034-5288(03)00036-5
Toghyani M, kazem Mosavi S, Modaresi M & Landy N. 2015. Evaluation of kefir as a potential probiotic on growth performance, serum biochemistry and immune responses in broiler chicks. Animal Nutrition, 1: 305-309. DOI: 10. 1016/j.aninu.2015.11.010
Wang L, Liu C, Chen M, Ya T, Huang W, Gao P & Zhang H. 2015. A novel Lactobacillus plantarum strain P-8 activates beneficial immuneresponse of broiler chickens. International Immuno pharmacology, 29:  901-907. DOI: 10.1016/ j. intimp.2015.07.024
Yenice G, Celebi D, Yörük MA, Uçar Ö, Sağlam Y, Tunc MA & Altun S. 2014. Effect of kefir upon
the performance, intestinal microflora and histopathology of certain organs inlaying hens. Kafkas Univ Vet Fak Derg, 20: 363-370. DOI: 10.9775/kvfd.2013.10173
Yu B, Liu J, Hsiao F & Chiou P. 2008. Evaluation of Lactobacillus reuteri Pg4 strain expressing heterologous β-glucanase as a probiotic in poultry diets based on barley. Animal Feed Science and Technology, 141: 82-91. DOI:
10.1016 /j.anifeedsci.2007.04.010
Zhu K, Xu X, Sun D, Tang J &  Zhang Y. 2014. Effects of drinking water acidification by organic acidifier on growth performance, digestive enzyme activity and caecal bacteria in growing rabbits. Animal Feed Science and Technology, 190: 87-94. DOI: 10.1016/j.anifeedsci. 2014. 01.014