Efficacy of Lactobacillus plantarum 1582-Fermented Chive (Allium schoenoprasum) as a Natural Antibiotic Against Eimeria acervulina in Broiler Chicken
Abstract
This study evaluated the efficacy of chive (Allium schoenoprasum) fermented by Lactobacillus plantarum 1582 (FC) as an antibiotic alternative in controlling Eimeria acervulina infection in broiler chickens. A total of 250 J-Dabaco male chickens were divided into five treatment groups, each with five replicates (cages) of 10 chickens: PC - positive control, NC - negative control, FC1 - supplemented with 1% FC, FC3 - supplemented with 3% FC, and antibiotic treatment (AB). Chickens in the NC, FC1, FC3, and AB groups were experimentally infected with E. acervulina at 14 days of age and monitored until day 42. Assessed variables included growth performance (body weight gain (BWG), feed intake (FI), feed conversion ratio (FCR), survival rate (SR), production efficiency index (PEI), serum immunoglobulins (IgA, IgM, IgG), ileal mRNA expression of tight junction (ZO-1, Claudin-2) and immune-related genes (IL-4, TNF-α, IFN-γ), fecal oocyst counts, and intestinal lesion scores. The results showed that both FC3 and FC1 groups improved BWG, FI, FCR, SR, and PEI, with the FC3 group showing the best performance, equivalent to the AB group. Additionally, FC contributed to preserving the integrity of the intestinal epithelium by enhancing tight junction protein expression (ZO-1, Claudin-2) and reducing inflammatory responses (IFN-γ, TNF-α), as well as reinforcing the intestinal barrier by improving villus morphology and reducing intestinal mucosal damage scores. Moreover, a significant reduction in Eimeria oocyst counts in the excretion demonstrated effective parasite control. These findings suggest that FC, especially at 3% concentration, can be an effective alternative to antibiotics in broiler farming for controlling coccidiosis and improving the safety and sustainability of production.
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References
Abou-Jaoudeh, C., Andary, J., & Abou-Khalil, R. (2024). Antibiotic residues in poultry products and bacterial resistance: A review in developing countries. Journal of Infection and Public Health, 17(12), 102592. https://doi.org/10.1016/j.jiph.2024.102592
Ahmad, R., Yu, Y. H., Hua, K. F., Chen, W. J., Zaborski, D., Dybus, A., Hsiao, F.S., & Cheng, Y. H. (2024). Management and control of coccidiosis in poultry: A review. Animal Bioscience, 37(1), 1-15. https://doi.org/10.5713/ab.23.0189
Ahmed, S. T., Mun, H. S., Islam, M. M., Ko, S. Y., & Yang, C. J. (2016). Effects of dietary natural and fermented herb combination on growth performance, carcass traits, and meat quality in grower-finisher pigs. Meat Science, 122, 7-15. https://doi.org/10.1016/j.meatsci.2016.07.016
Ayana, G. U., & Kamutambuko, R. (2024). Probiotics in disease management for sustainable poultry production. Advanced Gut & Microbiome Research, 2024, 4326438. https://doi.org/10.1155/2024/4326438
Bacanli, M., & Başaran, N. (2019). Importance of antibiotic residues in animal food. Food and Chemical Toxicology, 125, 462-466. https://doi.org/10.1016/j.fct.2019.01.033
Britez, J. D., Rodriguez, A. E., Di Ciaccio, L., Marugán-Hernandez, V., & Tomazic, M. L. (2023). What do we know about surface proteins of chicken parasites Eimeria? Life, 13(6), 1295. https://doi.org/10.3390/life13061295
Celi, P., Cowieson, A., Fru-Nji, F., Steinert, R., Kluenter, A.-M., & Verlhac, V. (2017). Gastrointestinal functionality in animal nutrition and health: New opportunities for sustainable animal production. Animal Feed Science and Technology, 234(11), 88-100. https://doi.org/10.1016/j.anifeedsci.2017.09.012
Ceylan, A., Saçaklı, P., Özgenç Çınar, Ö., Ramay, M. S., Ahsan, U., Harijaona, J. A., Bayraktaroğlu, A. G., Manghebati, F., & Calik, A. (2025). Effect of supplemental dietary phytogenic blends on growth performance, jejunal histomorphometry, and jejunal immunity of broiler chickens. Archives Animal Breeding, 68, 13-26. https://doi.org/10.5194/aab-68-13-2025
Charen, E., & Harbord, N. (2020). Toxicity of herbs, vitamins, and supplements. Advances in Chronic Kidney Disease, 27(1), 67-71. https://doi.org/10.1053/j.ackd.2019.08.003
Conway, D. P., & McKenzie, M. E. (2007). Poultry coccidiosis: Diagnostic and testing procedures. John Wiley & Sons. https://doi.org/10.1002/9780470344620
Dalloul, R. A., & Lillehoj, H. S. (2006). Poultry coccidiosis: Recent advancements in control measures and vaccine development. Journal of Eukaryotic Microbiology, 5, 143-163. https://doi.org/10.1111/j.1550-7408.2006.00153.x
Fatemi, A., Razavi, S. M., Asasi, K., & Goudarzi, M. T. (2015). Effects of Artemisia annua extracts on sporulation of Eimeria oocysts. Parasitology Research, 114, 1207-1211. https://doi.org/10.1007/s00436-014-4304-z
Galli, G. M., Petrolli, T. G., Aniecevski, E., Santo, A. D., Leite, F., Griss, L. G., Dazuk, V., Boiago, M. M., Dos Santos, H. V., Simões, C., Wagner, R., Bissacotti, B. F., Schentiger, M. R., & Da Silva, A. S. (2021). Phytogenic blend protective effects against microbes but affects health and production in broilers. Microbial Pathogenesis, 152, 104590. https://doi.org/10.1016/j.micpath.2020.104590
Ghaniei, A., Ghafouri, A., Sadr, S., & Hassanbeigi, N. (2023). Investigating the preventive effect of herbal medicine (Allium sativum, Artemisia annua, and Quercus infectoria) against coccidiosis in broiler chickens. Journal of World’s Poultry Research, 13(1), 96-102. https://doi.org/10.36380/jwpr.2023.10
Hai, P. V., Phuong, H. T. A, Hung, P. H. S, Na, T. T., Lai, N. H., Khuong, N. D. T., Liem, T. N., & Hoa, N. X. (2024). Lactobacillus strains from native chicken excretion for the fermentation of purple onion (Allium cepa L.) as an antibiotic alternative against Salmonella spp. in chickens. Open Veterinary Journal, 14, 3525-3538. https://doi.org/10.5455/OVJ.2024.v14.i12.35
Hai, P. V., & Hoa, N. X. (2020). Effect of Allium schoenoprasum extract on immune status against Newcastle virus and growth performance of broiler chicken. Electronic Journal of Agricultural Science and Technology – Hue University of Agriculture and Forestry, 4, 2058-2064.
Hai, P. V., Dung, H. Y., Liem, T. N., Khuong, N. D. T., Hung, P. H. S., & Hoa, N. X. (2020). The dietary supplement efficiency of essential oil of chive (Allium macrostemon) on the productivity and health performance of broilers. Can Tho University Journal of Science, 12(3), 1-6. https://doi.org/10.22144/ctu.jen.2020.018
Halder, N., Sunder, J., De, A. K., Bhattacharya, D., & Joardar, S. N. (2024). Probiotics in poultry: A comprehensive review. The Journal of Basic and Applied Zoology, 85, 23. https://doi.org/10.1186/s41936-024-00379-5
Hirakawa, R., Nurjanah, S., Furukawa, K., Murai, A., Kikusato, M., Nochi, T., & Toyomizu, M. (2020). Heat stress causes immune abnormalities via massive damage to effect proliferation and differentiation of lymphocytes in broiler chickens. Frontiers in Veterinary Science, 7, Article 46. https://doi.org/10.3389/fvets.2020.00046
Ho, D. T., Pham, H. H. S., Aota, W., Matsubayashi, M., Tsuji, N., & Hatabu, T. (2021). Reduction of macrophages by carrageenan decreases oocyst output and modifies local immune reaction in chick cecum with Eimeria tenella. Research in Veterinary Science, 139, 59-66. https://doi.org/10.1016/j.rvsc.2021.07.003
Ignatova, M., Sredkova, V., & Marasheva, V. (2009). Effect of dietary inclusion of probiotic on chickens performance and some blood indices. Journal of Basic and Applied Health Science, 25, 1079-1085.
Irawan, A., Hidayat, C., Jayanegara, A., & Ratriyanto, A. (2021). Essential oils as growth-promoting additives on performance, nutrient digestibility, cecal microbes, and serum metabolites of broiler chickens: A meta-analysis. Animal Bioscience, 34(9), 1499-1513. https://doi.org/10.5713/ab.20.0668
Jiang, Y., Zeng, Y., Chen, K., Cheng, H., Dai, S., Deng, X., Wang, L., Liao, J., Yang, R., Zhang, L. (2024). Effects of natural extract from medicinal herbs on broilers experimentally infected with Eimeria tenella. Veterinary Parasitology, 327, 110107. https://doi.org/10.1016/j.vetpar.2023.110107
Kim, D. K., Lillehoj, H. S., Lee, S. H., Jang, S. I., Lillehoj, E. P., Bravo, D. (2013). Dietary Curcuma longa enhances resistance against Eimeria maxima and Eimeria tenella infections in chickens. Poultry Science, 92, 2635-2643. https://doi.org/10.3382/ps.2013-03095
Kothari, D., Lee, W.-D., & Kim, S.-K. (2020). Allium flavonols: Health benefits, molecular targets, and bioavailability. Antioxidants, 9(9), 888. https://doi.org/10.3390/antiox9090888
Kumar, S., Garg, R., Moftah, A., Clark, E. L., Macdonald, S. E., Chaudhry, A. S., Sparagano, O., Banerjee, P. S., Kundu, K., Tomley, F. M., & Blake, D. P. (2014). An optimised protocol for molecular identification of Eimeria from chickens. Veterinary Parasitology, 199(1-2), 24-31. https://doi.org/10.1016/j.vetpar.2013.09.026
Khan, M., Anjum, A. A., Nawaz, M., Awan, A. R., & Ali, M. A. (2019). Effect of newly characterized probiotic Lactobacilli on weight gain, immunomodulation and gut microbiota of Campylobacter jejuni challenged broiler chicken. Poultry Veterinary Journal, 39(4), 56-69. https://doi.org/10.29261/pakvetj/2019.051
Layton, C., Bancroft, J. D., & Suvarna, S. K. (2019). Fixation of tissues. In: Suvarna, S. K., Layton, C., & Bancroft, J. D. (Eds.), Bancroft’s theory and practice of histological techniques (pp. 40-63). Elsevier. https://doi.org/10.1016/B978-0-7020-6864-5.00004-9
Li, J. Y., Huang, H. B., Pan, T. X., Wang, N., Shi, C. W., Zhang, H., Zhao, S., Song, X., & Qiao, H. (2022). Sanguinarine induces apoptosis in Eimeria tenella sporozoites via the generation of reactive oxygen species. Poultry Science, 101, 101771. https://doi.org/10.1016/j.psj.2022.101771
Li, H., Kang, Y., Sun, Y., Bian, C., Fan, M., Zhang, H., Zhao, S., Song, X., & Qiao, H. (2025). The role of Lactobacterium plantarum in solid-state fermentation of Astragalus membranaceus for broiler chicken feed. AMB Express, 15, 26. https://doi.org/10.1186/s13568-025-01823-7
Liu, K., Jia, M., & Wong, E. A. (2020). Delayed access to feed affects broiler small intestinal morphology and goblet cell ontogeny. Poultry Science, 99(11), 5275-5285. https://doi.org/10.1016/j.psj.2020.07.040
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Macpherson, A. J., & Uhr, T. (2004). Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Annals of the New York Academy of Sciences, 1029, 36-43. https://doi.org/10.1196/annals.1306.005
Malematja, E., Ng’ambi, J., Chitura, T., Manyelo, G., & Kolobe, D. (2022). Onion meal and onion extracts (Alium cepa L.) as natural growth promoters for use in poultry production: A review. Applied Ecology and Environmental Research, 20, 1097-1109. https://doi.org/10.15666/aeer/2001_383396
Martins, J. M. S., Carvalho, C. M. C., Litz, F., Silveira, M. M., Moraes, C., Silva, M. C. A., Fagundes, N., & Fernandes, E. (2016). Productive and economic performance of broiler chickens subjected to different nutritional plans. Revista Brasileira de Ciência Avícola, 18, 209-216. https://doi.org/10.1590/1806-9061-2015-0037
Memon, F. U., Yang, Y., Soliman, A. M., Lv, F., Rajput, N., Zhang, G., Baig, M. B., Wang, Y., & Si, H. (2021). Dietary supplementation with Piper sarmentosum extract on gut health of chickens infected with Eimeria tenella. Tropical Animal Health Production, 53, 497. https://doi.org/10.1007/s11250-021-02934-6
Mohsin, M., Zhang, Z., & Yin, G. (2022). Effect of probiotics on the performance and intestinal health of broiler chickens infected with Eimeria tenella. Journal of Veterinary Science, 10, 97. https://doi.org/10.1016/j.jvsv.2022.03.007
Mosmann, T. R., & Coffman, R. L. (1989). TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology, 7, 145-173. https://doi.org/10.1146/annurev.immunol.7.1.145
Navidshad, B., Darabighane, B., & Malecky, M. (2018). Garlic: An alternative to antibiotics in poultry production, a review. Iranian Journal of Applied Animal Science, 8, 9-17.
Ryu, J. H., Kim, C. H., & Yoon, J. H. (2010). Innate immune responses of the airway epithelium. Molecular Cells, 30(3), 173-183. https://doi.org/10.1007/s10059-010-0146-4
Shang, Y., Regassa, A., Kim, J. H., & Kim, W. K. (2015). The effect of dietary fructooligosaccharide supplementation on growth performance, intestinal morphology, and immune responses in broiler chickens challenged with Salmonella enteritidis lipopolysaccharides. Poultry Science, 94(12), 2887-2897. https://doi.org/10.3382/ps/pev275
Sugiharto, S., & Ranjitkar, S. (2019). Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology, and immune responses: A review. Animal Nutrition, 5(1), 1-10. https://doi.org/10.1016/j.aninu.2018.11.001
Teng, P. Y., Fuller, A. L., & Kim, W. K. (2020). Evaluation of nitro compounds as feed additives in diets of Eimeria-challenged broilers in vitro and in vivo. Poultry Science, 99(3), 1320-1325. https://doi.org/10.1016/j.psj.2019.11.026
Trojan, A., Jay, L., Kasprzak, H., Anthony, D., & Trojan, J. (2014). Immunotherapy of malignant tumors using antisense anti-IGF-I approach: Case of glioblastoma. Journal of Cancer Therapy, 5(7), 685-705. https://doi.org/10.4236/jct.2014.57078
Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nature Reviews Immunology, 9, 799-809. https://doi.org/10.1038/nri2653
Wang, X., Xie, H., Liu, F., & Wang, Y. (2017). Production performance, immunity, and heat stress resistance in Jersey cattle fed a concentrate fermented with probiotics in the presence of a Chinese herbal combination. Animal Feed Science and Technology, 228, 59-65. https://doi.org/10.1016/j.anifeedsci.2017.03.015
Wang, Y., Wu, T. R., Cai, S., Welte, T., & Chin, Y. E. (2000). Stat1 as a component of tumor necrosis factor alpha receptor 1-TRADD signaling complex to inhibit NF-kappaB activation. Molecular and Cellular Biology, 20, 4505-4512. https://doi.org/10.1128/MCB.20.13.4505-4512.2000
Wlaźlak, S., Pietrzak, E., Biesek, J., & Dunislawska, A. (2023). Modulation of the immune system of chickens: A key factor in maintaining poultry production—a review. Poultry Science, 102(8), 102785. https://doi.org/10.1016/j.psj.2023.102785
Zhang, X., Zhao, L., Cao, F., Ahmad, H., Wang, G., & Wang, T. (2013). Effects of feeding fermented Ginkgo biloba leaves on small intestinal morphology, absorption, and immunomodulation of early lipopolysaccharide-challenged chicks. Poultry Science, 92(1), 119-130. https://doi.org/10.3382/ps.2012-02645
Zhang, C., Zhao, X. H., Yang, L., Chen, X. Y., Jiang, R. S., Jin, S. H., & Geng, Z. Y. (2017). Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poultry Science, 96(12), 4325–4332. https://doi.org/10.3382/ps/pex245
Zhao, R., Qiu, Z., Bai, X., Xiang, L., Qiao, Y., & Lu, X. (2022). Digestive properties and prebiotic activity of garlic saccharides with different molecular weights obtained by acidolysis. Current Research in Food Science, 5, 2033-2044. https://doi.org/10.1016/j.crfs.2022.10.022
Zhu, X., Tao, L., Liu, H., & Yang, G. (2023). Effects of fermented feed on growth performance, immune organ indices, serum biochemical parameters, cecal odorous compound production, and the microbiota community in broilers. Poultry Science, 102(6), 102629. https://doi.org/10.1016/j.psj.2023.102629
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