The Efficacy of Dietary Dead Cell Lactobacillus ingluviei C37 on Carcass Characteristics, Meat Quality and Gut Health in Broilers Subjected to Heat Stress
Main Article Content
Abstract
Heat stress (HS) is a serious problem affecting the worldwide poultry industry, especially in hot and humid countries like Thailand. The aim of this work was to evaluate the efficacy of dead cell L. ingluviei C37 (DC-LIC37) on carcass characteristics, meat quality and gut heath (gut morphology and cecal microbial population) in broilers under heat stress. Three hundred and sixty male broilers Ross 308 (1-d-old) were allocated into 6 groups with 6 replications each in a completely randomized design (CRD). 1) the control group was raised under thermoneutral zone conditions at 21 ± 1°C (TNZ) and received basal diets (control). In contrast, the 15-day-old groups 2-6 were exposed to chronic HS at 32 ± 1°C for 5 h daily, until the end of the experiment and received one of the following 5 diets: 2) the negative control group received basal diet without any supplementation (NC); 3) the positive control group received basal diet + Zinc bacitracin 0.05 g/kg diet (PC); 4-6) the treatment groups received basal diet + DC-LIC37 at levels 1 × 107, 1 × 108, and 1 × 109 CFU/kg diet, respectively. The results revealed that DC-LIC37 can improve live, carcass, breast, liver, spleen, and heart weight in the HS condition. In addition, feeding DC-LIC37 in broilers subjected to HS can also mitigate the negative effect on lipid oxidation (decreased TBARS), activate the antioxidant activity (increased DPPH) in the thigh meat, and improve gut morphology and cecal microbial population in HS groups. The results indicated that DC-LIC37 supplementation at level of 1×109 CFU/kg diet has the potential to improve carcass characteristics, meat quality and gut health in broilers under HS.
Article Details

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
King Mongkut's Agricultural Journal
References
Adams, C. A. (2010). The probiotic paradox: Live and dead cells are biological response modifiers. Nutrition Research Reviews. 23(1), 37–46.
Ahmed, E., Abdelrahman, M., & Gahreeb, K. (2019). Effect of probiotic on growth performance, carcass traits, and clinical health parameters of broilers reared under heat stress in upper Egypt. SVU-International Journal of Veterinary Sciences. 2(2), 27–44.
Akbarian, A., et al. (2016). Association between heat stress and oxidative stress in poultry; mitochondrial dysfunction and dietary interventions with phytochemicals. Journal of Animal Science and Biotechnology. 7(1), 1–14.
Azad, M. A. K., Kikusato, M., Sudo, S., Amo, T., & Toyomizu, M. (2010). Time course of ROS production in skeletal muscle mitochondria from chronic heat-exposed broiler chicken. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology. 157(3), 266–271. https://doi.org/10.1016/j.cbpa.2010.07.011
Cao, C., Chowdhury, V. S., Cline, M. A., & Gilbert, E. R. (2021). The microbiota-gut-brain axis during heat stress in chickens: A review. Frontiers in Physiology. 12(October), 1-12. https://doi.org/10.3389/fphys.2021.752265
Cramer, T. A., et al. (2018). Effects of probiotic (Bacillus subtilis) supplementation on meat quality characteristics of breast muscle from broilers exposed to chronic heat stress. Poultry Science. 97(9), 3358–3368. https://doi.org/10.3382/ps/pey176
Danladi, Y., Loh, T. C., Foo, H. L., Akit, H., & Tamrin, N. A. (2022). Effects of probiotics and paraprobiotics as replacements for antibiotics on growth performance, carcass characteristics, small intestine histomorphology, immune status and hepatic growth gene expression in broiler chickens. Animals. 12(197), 1-18.
Fanning, S., et al. (2012). Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences of the United States of America. 109(6), 2108–2113. https://doi.org/10.1073/pnas.1115621109
Humam, A. M., Loh, T. C., Foo, H. L., & Samsudin, A. A. (2019). Effects of feeding different postbiotics produced by Lactobacillus plantarum on growth performance, carcass yield, intestinal morphology, gut microbiota composition, immune status, and growth gene expression in broilers under heat stress. Animals. 9(644), 1-20.
Jahromi, M. F., et al. (2016). Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. International Journal of Biometeorology. 60(7), 1099–1110. https://doi.org/10.1007/s00484-015-1103-x
Kers, J. G., et al. (2018). Host and environmental factors affecting the intestinal microbiota in chickens. Frontiers in Microbiology, 9(2), 1–14. https://doi.org/10.3389/fmicb.2018.00235
Kim, H. W., Yan, F. F., Hu, J. Y., Cheng, H. W., & Kim, Y. H. B. (2016). Effects of probiotics feeding on meat quality of chicken breast during postmortem storage. Poultry Science. 95(6), 1457–1464. https://doi.org/10.3382/ps/pew055
Konstantinov, S. R., et al. (2008). S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proceedings of the National Academy of Sciences of the United States of America. 105(49), 19474–19479. https://doi.org/10.1073/pnas.0810305105
Lara, L. J., & Rostagno, M. H. (2013). Impact of heat stress on poultry production. Animals. 3(2), 356–369. https://doi.org/10.3390/ani3020356
Liu, Z., et al. (2017). Characterization and bioactivities of the exopolysaccharide from a probiotic strain of Lactobacillus plantarum WLPL04. Journal of Dairy Science. 100(9), 6895–6905. https://doi.org/10.3168/jds.2016-11944
Metzler-Zebeli, B. U., et al. (2019). Feed restriction modifies intestinal microbiota-host mucosal networking in chickens divergent in residual feed intake. American Society for Microbiology. 4(1). https://doi.org/10.1128/msystems.00261-18
Mohammed, A. A., Jacobs, J. A., Murugesan, G. R., & Cheng, H. W. (2018). Animal well-being and behavior: Effect of dietary synbiotic supplement on behavioral patterns and growth performance of broiler chickens reared under heat stress. Poultry Science. 97(4), 1101–1108. https://doi.org/10.3382/ps/pex421
Mujahid, A., Akiba, Y., & Toyomizu, M. (2007). Acute heat stress induces oxidative stress and decreases adaptation in young white leghorn cockerels by downregulation of avian uncoupling protein. Poultry Science. 86(2), 364–371. https://doi.org/10.1093/ps/86.2.364
Navidshad, B., Liang, J. B., & Jahromi, M. F. (2012). Correlation coefficients between different methods of expressing bacterial quantification using real time PCR. International Journal of Molecular Sciences. 13(2), 2119–2132. https://doi.org/10.3390/ijms13022119
Nguyen, P. T., et al. (2020). Exopolysaccharide production by lactic acid bacteria: The manipulation of environmental stresses for industrial applications. AIMS Microbiology. 6(4), 451–469. https://doi.org/10.3934/MICROBIOL.2020027
NRC. 1994. Nutrient requirements of poultry. 9thEdition. National Academy Press, Washington D.C
Odore, R., et al. (2015). Cytotoxic effects of oxytetracycline residues in the bones of broiler chickens following therapeutic oral administration of a water formulation. Poultry Science. 94(8), 1979–1985. https://doi.org/10.3382/ps/pev141
Piqué, N., Berlanga, M., & Miñana-Galbis, D. (2019). Health benefits of heat-killed (Tyndallized) probiotics: An overview. International Journal of Molecular Sciences. 20(10), 1–30. https://doi.org/10.3390/ijms20102534
Quinteiro-Filho, W. M., et al. (2012). Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathology. 41(5), 421–427. https://doi.org/10.1080/03079457.2012.709315
Quinteiro-Filho, W. M., et al. (2010). Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poultry Science. 89(9), 1905–1914. https://doi.org/10.3382/ps.2010-00812
Rahimi, S., & Khaksefidi, A. (2006). A comparison between the effects of a probiotic (Bioplus 2B) and an antibiotic (virginiamycin) on the performance of broiler chickens under heat stress condition. Iranian Journal of Veterinary Research. 7(3), 23–28.
Renaudeau, D., et al. (2012). Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal. 6(5), 707–728. https://doi.org/10.1017/S1751731111002448
ROSS. 2019. Nutritional specifications. An Aviagen Brand.
Rostagno, M. H. (2020). Effects of heat stress on the gut health of poultry. Journal of Animal Science. 98(4), 1–9. https://doi.org/10.1093/jas/skaa090
Shazali, N., Foo, H. L., Loh, T. C., Choe, D. W., & Abdul Rahim, R. (2014). Prevalence of antibiotic resistance in lactic acid bacteria isolated from the faeces of broiler chicken in Malaysia. Gut Pathogens. 6(1). https://doi.org/10.1186/1757-4749-6-1
Sirisopapong, M., Okratok, S., Pukkung, C., & Khempaka, S. (2021). kān sœ̄m læk tōbāsinlat ʻinkalūwiʻi sī sām sip čhet chūai lot
khwāmkhrīat thāng phūmkhumkan læ phœ̄m kān sadǣngʻō̜k khō̜ng yīn thī kīeokhō̜ng kap khwām khængrǣng khō̜ng lamsai nai kai nư̄athī thūk kratun dūai laipōphōlīsǣkkhārai [Lactobacillus ingluviei C37 supplementation alleviates immunological stress and improves intestinal barrier gene expression in lipopolysaccharide challenged broiler chickens]. Khon Kaen Agriculture Journal. 42(2), 929.
Sohail, M. U., et al. (2013). Effect of supplementation of mannan oligosaccharide and probiotic on growth performance, relative weights of viscera, and population of selected intestinal bacteria in cyclic heat-stressed broilers. Journal of Applied Poultry Research. 22(3), 485–491. https://doi.org/10.3382/japr.2012-00682
Sugiharto, S., Yudiarti, T., Isroli, I., Widiastuti, E., & Kusumanti, E. (2017). Dietary supplementation of probiotics in poultry exposed to heat stress - A review. Annals of Animal Science. 17(3), 591–604. https://doi.org/10.1515/aoas-2016-0062
Tsukagoshi, M., et al. (2020). Lactobacillus ingluviei C37 from chicken inhibits inflammation in LPS-stimulated mouse macrophages. Animal Science Journal. 91(1), 1–7. https://doi.org/10.1111/asj.13436
Van Boeckel, T. P., et al. (2015). Global trends in antimicrobial use in food animals. Proceedings of the National Academy of Sciences of the United States of America. 112(18), 5649–5654. https://doi.org/10.1073/pnas.1503141112
Weng, K., et al. (2022). Fiber characteristics and meat quality of different muscular tissues from slow - and fast-growing broilers. Poultry Science. 101(1), 1–8. https://doi.org/10.1016/j.psj.2021.101537
Wu, Z., Pan, D., Guo, Y., Sun, Y., & Zeng, X. (2015). Peptidoglycan diversity and anti-inflammatory capacity in Lactobacillus strains. Carbohydrate Polymers. 128, 130–137. https://doi.org/10.1016/j.carbpol.2015.04.026
Zaboli, G., Huang, X., Feng, X., & Ahn, D. U. (2019). How can heat stress affect chicken meat quality? - A review. Poultry Science. 98(3), 1551–1556. https://doi.org/10.3382/ps/pey399
Zeferino, C. P. et al. (2016). Carcass and meat quality traits of chickens fed diets concurrently supplemented with vitamin C and E under constant heat stress. The Animal consortium. 10(1), 163–171. http://doi.org/10.1017/S1751731115001998
Zhu, C., et al. (2020). Effect of heat-inactivated compound probiotics on growth performance, plasma biochemical indices, and cecal microbiome in Yellow-Feathered broilers. Frontiers in Microbiology. 11(October), 1–16. https://doi.org/10.3389/fmicb.2020.585623