Improvement of Performance, Blood Profiles, Gut Health, and Immune Response of Broilers Supplemented with Chitosan, Bacillus subtilis, or Their Combination

I. Agusetyaningsih, S. Kismiati, I. Mangisah, E. Widiastuti, H. I. Wahyuni, T. Yudiarti, T. A. Sartono, S. Sugiharto

Abstract

The study aimed to investigate the effect of supplementing chitosan, Bacillus subtilis or blends of both on broiler growth performance, immune response, biochemical variables, and intestinal ecology of broiler chickens. Two hundred and eighty day-old chicks were distributed into 4 experimental groups, including T0 (control, basal feed), T1 (basal feed + chitosan 0.1% feed), T2 (basal feed + B. subtilis 0.01% feed), and T3 (basal feed + chitosan 0.1% feed + B. subtilis 0.01% feed). Variables measurements and sample collection were conducted on day 35. The T3 did not differ from T0 and T1, but they consumed less (p≤0.05) feed than T2 chickens. Feed conversion ratio (FCR) was lower (p≤0.05) in T1 and T3 compared to T0 and T2 groups. Leukocyte counts in T2 and T3 were higher (p≤0.05) than those in T0. The T1, T2, and T3 had higher (p≤0.05) lymphocyte counts than T0. The T3 had lower (p≤0.05) low-density lipoprotein (LDL) levels than the T0 group. The T2 had higher (p≤0.05) levels of total protein and globulin than T3 and T0. Compared to T0 and T3, serum albumin levels were greater (p≤0.05) in T1 and T2. The T3 had higher (p≤0.05) duodenal villi height than that in the other groups. The T2 and T3 chicks had higher (p≤0.05) Newcastle disease titer than T0 and T1. Compared to T2 and T3, T0 and T1 showed a worse (p≤0.05) microscopic structure of jejunum. The T2 and T3 showed lower (p≤0.05) lesion score in bursa of fabricius than that in the other groups. In conclusion, the blends of chitosan and B. subtilis resulted in improved FCR, higher leukocyte and lymphocyte counts, lower LDL, higher duodenal villi height, higher Newcastle disease titer, better microscopic structure of jejunum, and lower lesion score in bursa of fabricius of broiler chickens.

References

Abdul-Rahman, D. I., M. F. Hassan, , W. F. Khalil, , E. A. Ahmed, & F. M. Youssef. 2023. Application of chitosan and omega-3 supplementation on blood constituents, immunity, and antioxidant enzymes in broiler chicks. J. Adv. Vet. Res. 13:1063-1069. https://doi.org/10.1016/j.rvsc.2021.04.009
Abudabos, A. M., M. R. Aljumaah, M. M. Alkhulaifi, A. Alabdullatif, , G. M. Suliman, & A. R. A. Sulaiman. 2020. Comparative effects of Bacillus subtilis and Bacillus licheniformis on live performance, blood metabolites and intestinal features in broiler inoculated with Salmonella infection during the finisher phase. Microb. Pathog. 139:103870. https://doi.org/10.1016/j.micpath.2019.103870
Abudabos, A. M., H. A. A. Alhouri, M. A. Alhidary, A. A. Nassan, & A. A. Swelum. 2019. Ameliorative effect of Bacillus subtilis, Saccharomyces boulardii, oregano, and calcium montmorillonite on growth, intestinal histology, and blood metabolites on Salmonella infected broiler chicken. Environ. Sci. Pollut. Res. Int. 26:16274–16278. https://doi.org/10.1007/s11356-019-05105-1
Agusetyaningsih, I., E. Widiastuti, H.I. Wahyuni, R. Murwani, T. A. Sartono, & S. Sugiharto. 2022. Effect of encapsulated Cosmos caudatus leaf extract on the physiological conditions, immune competency, and antioxidative status of broilers at high stocking density. Ann. Anim. Sci. 22:653-662. https://doi.org/10.2478/aoas-2021-0043
Ahmad, S. S., K. Ahmad, E. J. Lee, Y. H. Lee, & I. Choi. 2020. Implications of insulin-like growth factor-1 in skeletal muscle and various diseases. Cells 9:1773. https://doi.org/10.3390/cells9081773
Alabi, O. J., J. W. Ng’Ambi, & E. E. Mbajiorgu. 2020. Aqueous extract of Moringa (Moringa oleifera) leaf (AEMOL) on the growth, sensory and histology parameters of broiler chickens. Appl. Ecol. Environ. Res. 18:6753-6764. https://doi.org/10.15666/aeer/1805_67536764
Ayman, U., L. Akter, R. Islam, S. Bhakta, M. A. Rahman, M. R. Islam, & Z. Haque. 2022. Dietary chitosan oligosaccharides improves health status in broilers for safe poultry meat production. Ann. Agric. Sci. 67:90-98. https://doi.org/10.1016/j.aoas.2022.05.003
Bilal, M., W. Si, F. Barbe, E. Chevaux, O. Sienkiewicz, & X. Zhao. 2021. Effects of novel probiotic strains of Bacillus pumilus and Bacillus subtilis on production, gut health, and immunity of broiler chickens raised under suboptimal conditions. Poult. Sci. 100:100871. https://doi.org/10.1016/j.psj.2020.11.048
Burtis, C. A. & E. R. Aswood. 1999. Tietz Textbook of Clinical Chemistry. 3rd ed. Philadelphia. WB. Saunders Company.
Chang, Qingqing, L. Yiqi, & L. Ruixia. 2020. Chitosan oligosaccharide as an effective feed additive to maintain growth performance, meat quality, muscle glycolytic metabolism, and oxidative status in yellow-feather broilers under heat stress. Poult. Sci. 99:4824-4831. https://doi.org/10.1016/j.psj.2020.06.071
Duan, Y., K. Gong, S. Xu, F. Zhang, X. Meng, & J. Han. 2022. Regulation of cholesterol homeostasis in health and diseases from mechanism to targeted theraupetics. Signal Transduuct. Target Ther. 7:265. https://doi.org/10.1038/s41392-022-01125-5
Dong, Y., R. Li, Y. Liu, L. Ma, J. Zha, Q. Qiao, & B. Wu. 2020. Benefit of dietary supplementation with Bacillus subtilis BYS2 on growth performance, immune response, and disease resistance of broilers. Probiotics Antimicrob. Proteins 12:1385-1397. https://doi.org/10.1007/s12602-020-09643-w
Egorov, I. A., T. A. Egorova, E. A. Yildirim, K. A. Kalitkina, L. A. Illina, & V. G. Flrolov. 2022. Effect of chitosan complexes on the bacterial community of cecum and productivity of broiler chickens. In The 2nd International Conference “Sport and Healthy Lifestyle Culture tn The XXI Century”. BIO Web Conference. 48 03007. https://doi.org/10.1051/bioconf/20224803007
Fathi, M., S. Saeidian, Z. Baghaeifar, & S. Varzandeh. 2023. Chitosan oligosaccharides in the diet of broiler chickens under cold stress had anti-oxidant and anti-inflammatory effects and improved hematological and biochemical indices, cardiac index, and growth performance. Livest. Sci. 276:105338. https://doi.org/10.1016/j.livsci.2023.105338
Govoni, C., D. D. Chiarelli, A. Luciano, M. Ottoboni, S. N. Perpelek, L. Pinotti, & M. C. Rulli. 2021. Global assessment of natural resources for chicken production. Adv. Water Resour. 154:1033987. https://doi.org/10.1016/j.advwatres.2021.103987
Horns, F., C. L. Dekker, & S. R. Quake. 2020. Memory B cell activation, broad anti-influenza antibodies, and bystander activation revealed by single-cell transcriptomics. Cell Rep. 30:905-913. https://doi.org/10.1016/j.celrep.2019.12.063
Huang, X. J., Y. K. Choi, H. S. Im, O. Yarimaga, E. Yoon, & H. S. Kim. 2006. Aspartate aminotransferase (AST/GOT) and alanine aminotransferase (ALT/GPT) detection techniques. Sensors 6:756-782. https://doi.org/10.3390/s6070756
Jayaraman, S., G. Thangavel, H. Kurian, R. Mani, R. Mukkalil, & H. J. P. Chirakkal. 2013. Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poult. Sci. 92:370–374. https://doi.org/10.3382/ps.2012-02528
Jiraphocakul, S., T. W. Sullivan, & K. M. Shahani. 1990. Influence of a dried Bacillus subtilis culture and antibiotics on performance and intestinal microflora in Turkeys. Poult. Sci. 69:1966–1973. https://doi.org/10.3382/ps.0691966
Kaufmann, L., M. Syedbasha, D. Vogt, Y. Hollenstein, J. Hartmann, J. E. Linnik, & A. Egli. 2017. An optimized hemagglutination inhibition (HI) assay to quantify Unfluenza-specific antibody titers. J. Vis. Exp. 130:55833. https://doi.org/10.3791/55833-v
Khan, I., H. Zaneb, S. Masood, S. Ashraf, H. F. Rehman, A. Ullah, & S. Din, S. 2023. Effects of selenium nanoparticles coated with chitosan supplementation on morphometry of immune organs, redox status, and immune response in broiler chicken. J. Appl. Poult. Res. 32:100377. https://doi.org/10.1016/j.japr.2023.100377
Klein, B. G. 2021. Cunningham’s Textbook of Veterinary Physiology, 6th ed. London, UK, Saunders.
Kriaa, A., M. Bourgin, A. Potiron, H. Mkaoouar, A. Jablaoui, P. Gerard, E. Maguin, & M. Rhimi. 2019. Microbial impact on cholesterol and bile acid metabolism: current status and future prospects. J. Lipid. Res. 60:323-332. https://doi.org/10.1194/jlr.R088989
Li, T., R. Na, P. Yu, B. Shi, S. Yan, Y. Zhao, & Y. Xu. 2015. Effects of dietary supplementation of chitosan on immune and antioxidative function in beef cattle. Czech J. Anim. Sci. 60:38–44. https://doi.org/10.17221/7910-CJAS
Li, W., J. Li, N. He, X. Dai, Z. Wang,, Y. Wang, & K. Pan. 2021. Molecular mechanism of enhancing the immune effect of the Newcastle disease virus vaccine in broilers fed with Bacillus cereus PAS38. Food Funct. 12:10903-10916. https://doi.org/10.1039/D1FO01777B
Liu, L., Y. Miao, X. Shi, H. Gao, & Y. Wang. 2020. Phosphorylated chitosan hydrogels inducing osteogenic differentiation of osteoblasts via JNK and p38 signaling pathways. ACS Biomater. Sci. Engineering. 6:1500-1509. https://doi.org/10.1021/acsbiomaterials.9b01374
Lopez-Virella, M. F., P. Stone, S. Ellis, & A. J. Coldwell. 1997. Cholesterol determinations in high density lipoproteins separated by three methods. Clin. Chem. 23:882-884. https://doi.org/10.1093/clinchem/23.5.882
Markowiak-Kopeć, P. & K. Śliżewska. 2020. The effect of probiotics on the production of short-chain fatty acids by human intestinal microbiome. Nutrients 12:1107. https://doi.org/10.3390/nu12041107
Maslennikov, R., V. Ivashkin, I. Efremova, E. Poluektova, & E. Shirokova. 2021. Probiotics in hepatology: An update. World J. Hepatol. 13:1154. https://doi.org/10.4254/wjh.v13.i9.1154
Miao, Z., W. Zhao, L. Guo, S. Wang, & J. Zhang. 2020. Effects of dietary supplementation of chitosan on immune function in growing Huoyan geese. Poult. Sci. 99:95-100. https://doi.org/10.3382/ps/pez565
Mohamed, T. M., W. Sun, , G. Z. Bumbie, W. M. Dosoky, Z. Rao, P. Hu, & Z. Tang. 2022. Effect of dietary supplementation of Bacillus subtilis on growth performance, organ weight, digestive enzyme activities, and serum biochemical indices in broiler. Animals 12:1558. https://doi.org/10.3390/ani12121558
Mohan, K., D. K. Rajan, A. R. Ganesan, D. Divya, J. Johansen, & S. Zhang. 2023. Chitin, chitosan and chitooligosaccharides as potential growth promoters and immunostimulants in aquaculture: A comprehensive review. Int. J. Biol. Macromol. 126285. https://doi.org/10.1016/j.ijbiomac.2023.126285
Pickard, J. M., M. Y. Zeng,  R. Caruso, & R. G. Núñez. 2017. Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease. Immunol. Rev. 279:70-89. https://doi.org/10.1111/imr.12567
Qiu, K., C. L. Li, J. Wang, G. H. Qi, J. Gao, H. J. Zhang, & S. G. Wu. 2021. Effects of dietary supplementation with Bacillus subtilis, as an alternative to antibiotics, on growth performance, serum immunity, and intestinal health in broiler chickens. Front. Nutr. 8:786878. https://doi.org/10.3389/fnut.2021.786878
Sugiharto, S., T. Yudiarti, I. Isroli, E. Widiastuti, & F. D. Putra. 2017. Effect of dietary supplementation with Rhizopus oryzae or Chrysonilia crassa on growth performance, blood profile, intestinal microbial population, and carcass traits in broilers exposed to heat stress. Arch. Anim. Breed. 60:347–356. https://doi.org/10.5194/aab-60-347-2017
Stoica, C. & G. Cox. 2021. Old problems and new solutions: Antibiotic alternatives in food animal production. Can. J. Microbiol. 67:427-444. https://doi.org/10.1139/cjm-2020-0601
Wang, Y., Z. Zhong, R. Wang, N. Munawar, L. Zan, & J. Zhu. 2023. Effects of proanthocyanidins and dialdehyde chitosan on the proliferation and differentiation of bovine myoblast for cultured meat production. Int. J. Biol. Macromol. 246:125618. https://doi.org/10.1016/j.ijbiomac.2023.125618
Wasti, S., N. Sah, & B. Mishra. 2020. Impact of heat stress on poultry health and performances, and potential mitigation strategies. Animals 10:1266. https://doi.org/10.3390/ani10081266
Werner, M., D. G. Gabrielson, & G. Eastman. 1981. Ultramicrodeterminations of serum triglycerides by bioluminescent assay. Clin. Chem. 21:268-271. https://doi.org/10.1093/clinchem/27.2.268
Xu, Y., Y. Yu, Y. Shen, Q. Li, J. Lan, Y. Wu, R. Zhang, G. Cao, & C. Yang. 2021. Effects of Bacillus subtilis and Bacillus licheniformis on growth performance, immunity, short chain fatty acid production, antioxidant capacity, and cecal microflora in broilers. Poult. Sci. 100:101358. https://doi.org/10.1016/j.psj.2021.101358
Yang, W. Y., P. E. Chang, Y. T. Chen, P. X. Liao, & Y. Y. Lin. 2023. Taurine-conjugated bile acids are the predominant form in hens and have potential impact in lipid metabolism in the liver. Ital. J. Anim. Sci. 22:1033-1039. https://doi.org/10.1080/1828051X.2023.2263026

Authors

I. Agusetyaningsih
S. Kismiati
I. Mangisah
E. Widiastuti
H. I. Wahyuni
T. Yudiarti
T. A. Sartono
S. Sugiharto
sgh_undip@yahoo.co.id (Primary Contact)
AgusetyaningsihI., KismiatiS., MangisahI., WidiastutiE., WahyuniH. I., YudiartiT., SartonoT. A., & SugihartoS. (2024). Improvement of Performance, Blood Profiles, Gut Health, and Immune Response of Broilers Supplemented with Chitosan, Bacillus subtilis, or Their Combination. Tropical Animal Science Journal, 47(3), 343-353. https://doi.org/10.5398/tasj.2024.47.3.343

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