Effect of γ-Aminobutyric Acid-producing Lactobacillus Strain on Laying Performance, Egg Quality and Serum Enzyme Activity in Hy-Line Brown Hens under Heat Stress

  • Zhu, Y.Z. (College of Animal Science, Anhui Science and Technology University) ;
  • Cheng, J.L. (Jiangsu Unison Biotechnology Development Co., Ltd.) ;
  • Ren, M. (College of Animal Science, Anhui Science and Technology University) ;
  • Yin, L. (College of Animal Science, Anhui Science and Technology University) ;
  • Piao, X.S. (Ministry of Agriculture Feed Industry Centre, China Agricultural Univeristy)
  • Received : 2015.02.11
  • Accepted : 2015.04.25
  • Published : 2015.07.01


Heat-stress remains a costly issue for animal production, especially for poultry as they lack sweat glands, and alleviating heat-stress is necessary for ensuring animal production in hot environment. A high ${\gamma}$-aminobutyric acid (GABA)-producer Lactobacillus strain was used to investigate the effect of dietary GABA-producer on laying performance and egg quality in heat-stressed Hy-line brown hens. Hy-Line brown hens (n = 1,164) at 280 days of age were randomly divided into 4 groups based on the amount of freeze-dried GABA-producer added to the basal diet as follows: i) 0 mg/kg, ii) 25 mg/kg, iii) 50 mg/kg, and iv) 100 mg/kg. All hens were subjected to heat-stress treatment through maintaining the temperature and the relative humidity at $28.83{\pm}3.85^{\circ}C$ and 37% to 53.9%, respectively. During the experiment, laying rate, egg weight and feed intake of hens were recorded daily. At the 30th and 60th day after the start of the experiment, biochemical parameters, enzyme activity and immune activity in serum were measured. Egg production, average egg weight, average daily feed intake, feed conversion ratio and percentage of speckled egg, soft shell egg and misshaped egg were significantly improved (p<0.05) by the increasing supplementation of the dietary GABA-producer. Shape index, eggshell thickness, strength and weight were increased linearly with increasing GABA-producer supplementation. The level of calcium, phosphorus, glucose, total protein and albumin in serum of the hens fed GABA-producing strain supplemented diet was significantly higher (p<0.05) than that of the hens fed the basal diet, whereas cholesterol level was decreased. Compared with the basal diet, GABA-producer strain supplementation increased serum level of glutathione peroxidase (p = 0.009) and superoxide dismutase. In conclusion, GABA-producer played an important role in alleviating heat-stress, the isolated GABA-producer strain might be a potential natural and safe probiotic to use to improve laying performance and egg quality in heat-stressed hens.


  1. Al-Harthi, M. A. 2014. The effect of natural and synthetic antioxidants on performance, egg quality and blood constituents of laying hens grown under high ambient temperature. Italian J. Anim. Sci. 13:444-449.
  2. Attia, Y. A., R. A. Hassan, and E. M. A. Qota. 2009. Recovery from adverse effects of heat stress on slow-growing chicks in the tropics 1: Effect of ascorbic acid and different levels of betaine. Trop. Anim. Health Prod. 41:807-818.
  3. Attia, Y. A., B. M. Bohmer, and D. A. Roth-Maier. 2006. Responses of broiler chicks raised under constant relatively high ambient temperature to enzymes, amino acid supplementations, or a high-nutrient diet. Archiv. Geflugelk. 70:80-91.
  4. Attia, Y. A, R. A. Hassan, A. E. Tag El-Din, and B. M. Abou-Shehema. 2011. Effect of ascorbic acid or increasing metabolizable energy level with or without supplementation of some essential amino acids on productive and physiological traits of slow-growing chicks exposed to chronic heat stress. J Anim. Physiol. Anim. Nutr. 95:744-755.
  5. Belay, T. and R. G. Teeter. 1993. Broiler water balance and thermobalance during thermoneutral and high ambient temperature exposure. Poult. Sci. 72:116-124.
  6. Baydas, G., E. Sonkaya, M. Tuzcu, A. Yasar, and E. Donder. 2005. Novel role for gabapentin in neuroprotection of central nervous system in streptozotocine-induced diabetic rats. Acta Pharmacol. Sin. 26:417-422.
  7. Bloemhof, S., A. Kause, E. F. Knol, J. A. M. Van Arendonk, and I. Misztal. 2012. Heat stress effects on farrowing rate in sows: Genetic parameter estimation using within-line and crossbred models. J. Anim. Sci. 90:2109-2119.
  8. Chan, H. O. and H. O. Suk. 2004. Effects of germinated brown rice extracts with enhanced levels of GABA on cancer cell proliferation and apoptosis. J. Med. Food 7:19-23.
  9. Chen, Z., J. Tang, Y. Q. Sun, and J. Xie. 2013. Protective effect of $\gamma$-aminobutyric acid on antioxidation function in intestinal mucosa of Wenchang chicken induced by heat stress. J. Anim. Plant Sci. 23:1634-1641.
  10. Cho, Y. R., J. Y. Chang, and H. C. Chang. 2007. Production of $\gamma$-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 17:104-109.
  11. Dai, S. F., F. Gao, W. H. Zhang, S. X. Song, X. L. Xu, and G. H. Zhou. 2011. Effects of dietary glutamine and gammaaminobutyric acid on performance, carcass characteristics and serum parameters in broilers under circular heat stress. Anim. Feed Sci. Technol. 168:51-60.
  12. Feng, Y., X. J. Yang, Y. B. Wang, W. L. Li, Y. Liu, R. Q. Yin, and J. H. Yao. 2012. Effects of immune stress on performance parameters, intestinal enzyme activity and mRNA expression of intestinal transporters in broiler chicken. Asian Australas. J. Anim. Sci. 25:701-707.
  13. Fox, D. G. and T. P. Tylutki. 1998. Accounting for the effects of environment on the nutrient requirements of dairy cattle. J. Dairy Sci. 81:3085-3095.
  14. Freeman, B. A. and J. D. Crapo. 1982. Biology of disease: Free radicals and tissue injury. Lab. Invest. 47:412-426.
  15. Hodges, R. D. 1969. pH and mineral ion levels in the blood of the laying hen (Gallus domesticus) in relation to egg shell formation. Comp. Biochem. Physiol. 28:1243-1257.
  16. Huang, H. L., W. J. Zhao, X. T. Zou, H. Li, M. Zhang, and X. Y. Dong. 2011. Effect of $\gamma$-aminobutyric acid on incubation, immunity and antioxidant activity in pigeon. Chin J. Vet. Sci. 9:1327-1331.
  17. Kim, S. H., B. H. Shin, Y. H. Kim, S. W. Nam, and S. J. Jeon. 2007. Cloning and expression of a full-length glutamate decarboxylase gene from Lactobacillus brevis BH2. Biotechnol. Bioprocess Eng. 12:707-712.
  18. Kirunda, D. F. K., S. E. Scheideler, and S. R. Mckee. 2001. The efficacy of vitamin E (DL-$\alpha$-tocopheryl acetate) supplementation in hen diets to alleviate egg quality deterioration associated with high temperature exposure. Poult. Sci. 80:1378-1383.
  19. Komatsuzaki, N., J. Shima, S. Kawamoto, H. Monose, and T. Kimura. 2005. Production of $\gamma$-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 22:497-504.
  20. Karamouz, H., J. G. Ghalehkandi, H. Z. A. Nazhad, Y. E. Nezhad, and N. M. Sis. 2011. Effect of different levels of zinc oxide supplement on mucosal sucrase enzyme activity in small intestine of male broiler chicks. Int. J. Anim. Vet. Adv. 3:54-57.
  21. Larbier, Z. M., A. M. Chagneau, and P. A. Geraert. 1993. Influence of ambient temperature on true digestibility of protein and amino acids of rapeseed and soybean meals in broilers. Poult. Sci. 72:289-295.
  22. Li, H., D. Gao, Y. Cao, and H. Xu. 2008. A high $\gamma$-aminobutyric acid-producing Lactobacillus brevis isolated from Chinese traditional paocai. Ann. Microbiol. 58:649-653.
  23. Li, H. X., T. Qiu, G. D. Huang, and Y. S. Cao. 2010. Production of gamma-aminobutyric acid by Lactobacillus brevis NCL912 using fed-batch fermentation. Microb. Cell Fact. 9:85.
  24. Liong, M.T. and N. P. Shah. 2005. Bile salt deconjugation ability, bile salt hydrolase activity and cholesterol co-precipitation ability of lactobacilli strains. Int. Dairy J. 15:391-398.
  25. Mashaly, M. M., G. L. Hendricks 3rd, M. A. Kalama, A. E. Gehad, A. O. Abbas, and P. H. Patterson. 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult. Sci. 83:889-894.
  26. Miyazawa, T., T. Kawabata, K. Okazaki, T. Suzuki, D. Imai, T. Hamamoto, S. Matsumura, and T. Miyagawa. 2012. Oral administration of $\gamma$-aminobutyric acid affects heat production in a hot environment in resting humans. J. Physiol. Anthropol. 31:3.
  27. Nguyen, T. D. T., J. H. Kang, and M. S. Lee. 2007. Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int. J. Food Microbiol. 113:358-361.
  28. Nesamvuni, E., R. Lekalakala, D. Norris, and J. W. Ngambi. 2012. Effects of climate change on dairy cattle, South Africa. Afr. J. Agric. Res. 7:3867-3872.
  29. National Research Council. 1994. Nutrient Requirements of Poultry, 9th rev. edn. National Academy Press, Washington, DC, USA.
  30. Ole Miaron, J. O. and R. J. Christopherson. 1992. Effect of prolonged thermal exposure on heat production, reticular motility, rumen-fluid and -particulate passage-rate constants, and apparent digestibility in steers. Can. J. Anim. Sci. 72:809-819.
  31. Ooi, L. and M. Liong. 2010. Cholesterol-lowering effects of probiotics and prebiotics: A review of in vivo and in vitro findings. Int. J. Mol. Sci. 11:2499-2522.
  32. Puthpongsiriporn, U., S. E. Scheideler, J. L. Sell, and M. M. Beck. 2001. Effects of vitamin E and C supplementation on performance, in vitro lymphocyte proliferation, and antioxidant status of laying hens during heat stress. Poult. Sci. 80:1190-1200.
  33. Quinteiro-Filho, W. M., M. V. Rodrigues, A. Ribeiro, V. Ferrazde-Paula, M. L. Pinheiro, L. R. M. Sa, A. J. P. Ferreira, and J. Palermo-Neto. 2012. Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chicken: Role of acute hypothalamic-pituitary-adrenal axis activation. J. Anim. Sci. 90:1986-1994.
  34. Rhoads, M. L., R. P. Rhoads, M. J. VanBaale, R. J. Collier, S. R. Sanders, W. J. Weber, B. A. Crooker, and L. H. Baumgard. 2009. Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production, metabolism, and aspects of circulating somatotropin. J. Dairy Sci. 92:1986-1997.
  35. Sanderson, I. R. and Y. P. He. 1994. Nucleotide uptake and metabolism by intestinal epithelial cells. J. Nutr. 124:131S-137S.
  36. SAS. 2004. SAS/STAT User's Guide Statistics, Version 9.1. SAS Inst., Inc., Cary, NC, USA.
  37. Slater, T. F. 1984. Free-radical mechanisms in tissue injury. Biochem. J. 222:1-15.
  38. Sliwowska, J. H., H. J. Billings, R. L. Goodman, and M. N. Lehman. 2006. Immunocytochemical colocalization of GABA-B receptor subunits in gonadotropin-releasing hormone neurons of the sheep. Neuroscience 141:311-319.
  39. Tajalli, S., H. Jonaidi, M. Abbasnejad, and D. M. Denbow. 2006. Interaction between nociceptin/orphanin FQ (N/OFQ) and GABA in response to feeding. Physiol. Behav. 89:410-413.
  40. Viveros, A., A. Brenes, I. Arija, and C. Centeno. 2002. Effects of microbial phytase supplementation on mineral utilization and serum enzyme activities in broiler chicks fed different levels of phosphorus. Poult. Sci. 81:1172-1183.
  41. Watanabe, M., K. Maemura, K. Kanbara, T. Tamayama, and H. Hayasaki,, 2002. GABA and GABA receptors in the central nervous system and other organs. Int. Rev. Cytol. 213:1-47.
  42. Wei, X. J., J. Wu, Y. D. Ni, L. Z. Lu, and R. Q. Zhao. 2011. Antioxidant effect of a phytoestrogen equol on cultured muscle cells of embryonic broilers. In Vitro Cell. Dev. Biol. 47:735-741.
  43. Williams, A. J., C. C. Bautista, R. W. Chen, J. R. Dave, X. Lu, F. C. Tortella, and J. A. Hartings. 2006. Evaluation of gabapentin and ethosuximide for treatment of acute nonconvulsive seizures following ischemic brain injury in rats. J. Pharmacol. Exp. Ther. 318:947-955.
  44. Zhang, M., X. T. Zou, H. Li, X. Y. Dong, and W. J. Zhao. 2012. Effect of dietary gamma-aminobutyric acid on laying performance, egg quality, immune activity and endocrine hormone in heat-stressed Roman hens. Anim. Sci. J. 83:141-147.

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