Investigating the Effect of Different Levels of Butyric Acid Glycerides and Clove Oil on Growth Performance, Blood Parameters and Tibia Bone Characteristics of Broiler Chickens

پژوهشهای علوم دامی ایران

Article 7, Volume 16, Issue 3 - Serial Number 59, September 2024, Pages 415-432   

Document Type: Research Articles

DOI: 10.22067/ijasr.2024.84978.1178

Authors

Seyyedeh azam khatami^* ; Mir Daryoush Shakouri; Nemat Hedayat Evrigh

Department of Animal Science, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

Abstract

Introduction: Today, livestock and poultry health in the advanced production system is the main challenge affecting human health and the global economy. For years, antibiotics have been widely used as growth promoters to stabilize the microbial population of the digestive tract and improve performance. However, scientific evidence suggests that the massive use of these compounds has led to increased problem of antibiotic resistance and presence of antibiotics residues in feed and compromises human and animal health. Hence, there is a growing need to find effective alternatives to control infectious diseases and limit the spread of resistant bacteria.
Organic acids are an alternative to antibiotics in poultry diets. These are improving the immune system of broilers by acidifying the gastrointestinal tract and improving the intestinal microflora. Coating of organic acids prevents their dissociation and digestion in the stomach so that the biological effect of organic acids reaches the distal parts of the gastrointestinal tract and is effective in intestinal microflora and mucosal morphology. Also, Essential oils are volatile oil compounds that are produced as secondary metabolites by plants. Essential oils extracted from plants have anti-bacterial, anti-viral, anti-fungal, antioxidant activities as well as immune-modulating effects, reducing blood fat and stimulating the digestive system of poultry. Organic acids can complete the effect of essential oils through synergism antibacterial and bactericidal activities. Therefore, the present study was designed to investigate the effect of different levels of butyric acid glycerides and clove oil on growth performance, blood parameters and tibia bone characteristics of broiler chickens.
 
Material and Methods: A total of 300 male and female broilers (Ross 308) with a completely randomized design with a 2 × 3 factorial arrangement, two levels of butyric acid glycerides (0 and 0.2 %) and three levels of clove oil (0, 500 and 1000 mg/kg) were used. Each of the six dietary treatments was fed to five replicate pens of 10 birds each from 0 to 42 days of age. Body weight gain, feed intake, feed conversion ratio, weights of immune organs, plasma lipids and physical and mineral characteristics of the tibia were recorded. The collected data were analyzed using SAS software (2003) and using the general linear model (GLM) procedure. The equation of the statistical model of the experiment was according to the relation Yijk = µ + Ai + Bj + (AB)ij + eijk, where Yijk represents the numerical value of each observation, µ is the population mean, Ai is the effect of butyric acid glycerides (0 and 0.2%), Bj was the effect of clove oil (0, 500 and 1000 mg/kg), ij (AB) was the interaction effect of butyric acid glycerides and clove oil, and eijk was the experimental error.
Results and Discussion: The results showed that the addition of 0.2% butyric acid glycerides in the diet of broiler chickens reduced feed intake, body weight and daily weight gain compared to the control group (P<0.05). Addition of 1000 mg/kg of clove oil in the diet reduced feed intake, body weight, daily weight gain and european production index compared to the control group (P<0.05). Body weight, feed efecioncy, european efficiency factor and feed conversion ratio of broiler chickens were affected by the interaction effect of butyric acid glycerides and clove oil (P<0.05). The addition of different levels of clove oil with and without butyric acid glycerides in the broiler diet reduced cholesterol and LDL concentration compared to the control group (P<0.05). But the concentration of triglyceride, HDL and VLDL were not affected by the experimental treatments. The interaction effect of clove oil and butyric acid glycerides did not affect the weight of bursa of fabricius, thymus and spleen of broiler chickens. The amount of calcium, phosphorus and ash of tibia bone was significantly affected by butyric acid glycerides. Also, the length of the tibia of broiler chickens was affected by the clove oil and the interaction effect of butyric acid glycerides and clove oil (p<0.05).
Conclusion: In general, no synergistic effect was observed between butyric acid glycerides and clove oil on growth performance of chickens. Although the use of 0.2% butyric acid glycerides and 1000 mg/kg clove oil led to a decrease in the weight gain of chickens by reducing feed intake, but the addition of butyric acid glycerides caused an increase in the concentration of phosphorus, calcium and ash in the tibia bone of broiler chickens.

Keywords

Butyric acid glycerides; Broilers; Clove oil; Tibia bone

References

1. Abu Isha, A. A., Abd El-Hamid, A. E., Ziena, H. M., & Ahmed, H. A. (2018). Effect of spearmint (Mentha spicata) on productive and physiological parameters of broiler chicks. Egyptian Poultry Science Journal, 38(3), 815-829. http://dx.doi.org/10.21608/EPSJ.2018.17106.
2. Adewole, D. I., Oladokun, S., & Santin, E. (2021). Effect of organic acids–essential oils blend and oat fiber combination on broiler chicken growth performance, blood parameters, and intestinal health. Animal Nutrition, 7(4), 1039-1051. http://dx.doi.org/10.1016/j.aninu.2021.02.001
3. Adil, S., Banday, T., Bhat, G. A., Mir, M. S., & Rehman, M. (2010). Effect of dietary supplementation of organic acids on performance, intestinal histomorphology, and serum biochemistry of broiler chicken. Veterinary Medicine International, http://dx.doi.org/10.4061/2010/479485
4. Aghazadeh, A. M., & TahaYazdi, M. (2012). Effect of butyric acid supplementation and whole wheat inclusion on the performance and carcass traits of broilers. South African Journal of Animal Science, 42(3), 241-248. http://dx.doi.org/10.4314/sajas.v42i3.5
5. Amiri Andi, M., & Mansouri, H. (2018). Effect of different levels of dietary protected butyric acid on growth performance, blood metabolites and minerals of tibiainbroiler chicken. Research on Animal Production, 8(18), 10-19. (In Persian). http://dx.doi.org/10.29252/rap.8.18.10
6. Antongiovanni, M., Buccioni, A., Petacchi, F., Leeson, S., Minieri, S., Martini, A., & Cecchi, R. (2007). Butyric acid glycerides in the diet of broiler chickens: Effects on gut histology and carcass composition. Italian Journal of Animal Science, 6(1), 19-25. http://dx.doi.org/10.4081/ijas.2007.19
7. Aviagen. (2019). Ross 308 Broiler Nutrition Specifications. Aviagen Ltd, Newbridge, UK.
8. Azadegan Mehr, M., Hassanabadi, A., Nassiri Moghaddam, H., & Kermanshah, H. (2014). Supplementation of clove essential oils and probiotic on blood components, lymphoid organs and immune response in broiler chickens. Research Opinions in Animal and Veterinary Sciences, 4(4), 218-223.
9. Biggs, P., & Parsons, C. M. (2008). The effects of several organic acids on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. Poultry Science, 87(12), 2581-2589. http://dx.doi.org/org/10.3382/ps.2008-00080
10. Bortoluzzi, C., Pedroso, A. A., Mallo, J. J., Puyalto, M., Kim, W. K., & Applegate, T. J. (2017). Sodium butyrate improved performance while modulating the cecal microbiota and regulating the expression of intestinal immune-related genes of broiler chickens. Poultry Science,96(11), 3981-3993. http://dx.doi.org/10.3382/ps/pex218
11. Bouhaddouda, N., Aouadi, S., & Labiod, R. (2016). Evaluation of chemical composition and biological activities of essential oil and methanolic extract of Origanum vulgare L. ssp. glandulosum (DESF.) Ietswaart from Algeria. International Journal of Pharmacognosy and Phytochemical Research,8(1), 104-112. http://dx.doi.org/10.26502/jppr.0003
12. Brenes, A., & Roura, E. (2010). Essential oils in poultry nutrition: Main effects and modes of action. Animal Feed Science and Technology, 158(1-2), 1-14. http://dx.doi.org/1016/j.anifeedsci.2010.03.007
13. Caspary, W. F. (1992). Physiology and pathophysiology of intestinal absorption. The American journal of clinical nutrition, 55(1), 299-308. http://dx.doi.org/10.1093/ajcn/55.1.299s
14. Casteleyn, C., Doom, M., Lambrechts, E., Van Den Broeck, W., Simoens, P., & Cornillie, P. (2010). Locations of gut-associated lymphoid tissue in the 3-month-old chicken: A review. Avian Pathology, 39(3), 143-150. http://dx.doi.org/10.1080/03079451003786105
15. Cengiz, S. S., Yesilbag, D., Eren, M., Cetin, I., Meral, Y., & Biricik, H. A. K. A. N. (2016). Effects of volatile oil additives on growth, carcass performances, and calcium and phosphorus concentrations in serum and bone of broilers. Revue de Medecine Veterinaire, 167(7), 230-239.
16. Chambers, E. S., Morrison, D. J., & Frost, G. (2015). Control of appetite and energy intake by SCFA: what are the potential underlying mechanisms?.R Proceedings of the Nutrition Society, 74(3), 328-336. http://dx.doi.org/10.1017/S0029665114001657
17. Chowdhury, S., Mandal, G. P., Patra, A. K., Kumar, P., Samanta, I., Pradhan, S., & Samanta, A. K. (2018). Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Animal Feed Science and Technology, 1 (236), 39-47. http://dx.doi.org/10.1016/J.ANIFEEDSCI.2017.12.003
18. Cortés-Rojas, D. F., de Souza, C. R. F., & Oliveira, W. P. (2014). Clove (Syzygium aromaticum): A precious spice. Asian Pacific Journal of Tropical Biomedicine, 4(2), 90-96. http://dx.doi.org/10.1016/S2221-1691(14)60215-X
19. Daniel, A. N., Sartoretto, S. M., Schmidt, G., Caparroz-Assef, S. M., Bersani-Amado, C. A., & Cuman, R. K. N. (2009). Anti-inflammatory and antinociceptive activities A of eugenol essential oil in experimental animal models. Revista Brasileira de Farmacognosia, 19(1), 212-217. http://dx.doi.org/10.1590/S0102-695X2009000200006
20. Deepa, K., Purushothaman, M. R., Vasanthakumar, P., & Sivakumar, K. (2017). Serum biochemical parameters and meat quality influenced due to supplementation of sodium butyrate in broiler chicken. International Journal of Livestock Research, 7(8), 108-116. http://dx.doi.org/10.5455/IJLR.20170610051212
21. Elbaz, A. M., Ashmawy, E. S., Salama, A. A., Abdel-Moneim, A. M. E., Badri, F. B., & Thabet, H. A. (2022). Effects of garlic and lemon essential oils on performance, digestibility, plasma metabolite, and intestinal health in broilers under environmental heat stress. BMC Veterinary Research, 18(1), 1-12. http://dx.doi.org/10.1186/s12917-022-03530-y.
22. Emami, N. K., Naeini, S. Z., & Ruiz-Feria, C. A. (2013). Growth performance, digestibility, immune response and intestinal morphology of male broilers fed phosphorus deficient diets supplemented with microbial phytase and organic acids. Livestock Science, 157(2-3), 506-513. http://dx.doi.org/10.1016/j.livsci.2013.08.014
23. Esmaeilipour, O., Shivazad, M., Moravej, H., Aminzadeh, S., Rezaian, M., & Van Krimpen, M. M. (2011). Effects of xylanase and citric acid on the performance, nutrient retention, and characteristics of gastrointestinal tract of broilers fed low-phosphorus wheat-based diets. Poultry Science, 90(9), 1975-1982. http://dx.doi.org/10.3382/ps.2010-01264
24. Evangelista, A. G., Corrêa, J. A. F., Pinto, A. C. S. M., & Luciano, F. B. (2022). The impact of essential oils on antibiotic use in animal production regarding antimicrobial resistance–a review. Critical Reviews in Food Science and Nutrition, 62(19), 5267-5283. http://dx.doi.org/10.1080/10408398.2021.1883548
25. Fascina, V. B., Pasquali, G. A. M., Carvalho, F. B., Muro, E. M., Vercese, F., Aoyagi, M. M., & Sartori, J. R. (2017). Effects of phytogenic additives and organic acids, alone or in combination, on the performance, intestinal quality and immune responses of broiler chickens. Brazilian Journal of Poultry Science, 19(3), 497-508. http://dx.doi.org/1590/1806-9061-2016-0422
26. Friedewald, W. T., Levy, R. I., & Fredrickson, D. S. (1972). Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clinical Chemistry, 18(6), 499-502.
27. Furness, J. B., Rivera, L. R., Cho, H. J., Bravo, D. M., & Callaghan, B. (2013). The gut as a sensory organ. Nature Reviews Gastroenterology and Hepatology, 10(12), 729-740. http://dx.doi.org/10.1038/nrgastro.2013.18 .
28. Gandomani, V. T., Mahdavi, A. H., Rahmani, H. R., Riasi, A., & Jahanian, E. (2014). Effects of different levels of clove bud (Syzygium aromaticum) on performance, intestinal microbial colonization, jejunal morphology, and immunocompetence of laying hens fed different n-6 to n-3 ratios. Livestock Science, 167(1), 236-248.
    http://dx.doi.org/10.1016/j.livsci.2014.05.006
29. Gheisari, A. A., Heidari, M., Kermanshahi, R. K., Togani, M., & Saraeian, S. (2007). Effect of dietary supplementation of protected organic acids on ileal microflora and protein digestibility in broiler chickens. In Proceedings of the 16th European Symposium on Poultry Nutrition. Strasbourg, France (pp. 519-522).
30. Gopi, M., Karthik, K., Manjunathachar, H. V., Tamilmahan, P., Kesavan, M., Dashprakash, M., Balaraju, B. L., & Purushothaman, M. R. (2014). Essential oils as a feed additive in poultry nutrition. Advances in Animal and Veterinary Sciences, 2(1), 1-7. http://dx.doi.org/10.14737/journal.aavs/2014.2.1.1.7
31. Gordon, R. W., & Roland Sr, D. A. (1998). Influence of supplemental phytase on calcium and phosphorus utilization in laying hens. Poultry Science, 77(2), 290-294. http://dx.doi.org/10.1093/ps/77.2.290
32. Harb, A. A., Bustanji, Y. K., Almasri, I. M., & Abdalla, S. S. (2019). Eugenol reduces LDL cholesterol and hepatic steatosis in hypercholesterolemic rats by modulating TRPV1 receptor. Scientific Reports, 9(1), 1-10. http://dx.doi.org/10.1038/s41598-019-50352-4
33. Hernandez, F., Garcia, V., Madrid, J., Orengo, J., Catalá, P., & Megias, M. D. (2006). Effect of formic acid on performance, digestibility, intestinal histomorphology and plasma metabolite levels of broiler chickens. British Poultry Science, 47(1), 50-56. http://dx.doi.org/10.1080/00071660500475574
34. Hu, Z., & Guo, Y. (2007). Effects of dietary sodium butyrate supplementation on the intestinal morphological structure, absorptive function and gut flora in chickens. Animal Feed Science and Technology, 132(3-4), 240-249. http://dx.doi.org/10.1016/j.anifeedsci.2006.03.017
35. Ibrahim, D., Eldemery, F., Metwally, A. S., Abd-Allah, E. M., Mohamed, D. T., Ismail, T. A., Hamed, T. A., Al Sadik, G.M., Neamat-Allah, A.N., & Abd El-Hamid, M.I. (2022). Dietary eugenol nanoemulsion potentiated performance of broiler chickens: Orchestration of digestive enzymes, intestinal barrier functions and cytokines related gene expression with a consequence of attenuating the severity of E. coli O78 infection. Frontiers in Veterinary Science, 23(9), 1-17. http://dx.doi.org/10.3389/fvets.2022.847580
36. Imran, M., Ahmed, S., Ditta, Y. A., Mehmood, S., Khan, M. I., Gillani, S. S., Rasool, Z., Sohail, M. L., Mushtaq, , & Umar, S. (2018). Effect of microencapsulated butyric acid supplementation on growth performance, ileal digestibility of protein, duodenal morphology and immunity in broilers. Journal of the Hellenic Veterinary Medical Society, 69(3), 1109-1116.
37. Iqbal, H., Rahman, A., Khanum, S., Arshad, M., Badar, I. H., Asif, A. R., Hayat, Z. & Iqbal, M. A. (2021). Effect of essential oil and organic acid on performance, gut health, bacterial count and serological parameters in broiler. Brazilian Journal of Poultry Science, 23(3), 1-10. http://dx.doi.org/10.1590/1806-9061-2021-1443
38. Irani, M., Gharahveysi, S., Zamani, M., & Rahmatian, R. (2011). The effect of butyric acid glycerides on performance and some bone parameters of broiler chickens. African Journal of Biotechnology, 10(59), 12782- http://dx.doi.org/10.5897/AJB11.1148
39. Jouany, J. P., & Morgavi, D. P. (2007). Use of ‘natural’ products as alternatives to antibiotic feed additives in ruminant production. Animal, 1(10), 1443-1466. http://dx.doi.org/10.1017/S1751731107000742
40. Kamal, A. M., & Ragaa, N. M. (2014). Effect of dietary supplementation of organic acids on performance and serum biochemistry of broiler chicken. Nature and Science, 12(2), 38-45. http://dx.doi.org/10.4061/2010/479485
41. Krauze, M., Cendrowska-Pinkosz, M., Matuseviĉius, P., Stępniowska, A., Jurczak, P., & Ognik, K. (2021). The effect of administration of a phytobiotic containing cinnamon oil and citric acid on the metabolism, immunity, and growth performance of broiler chickens. Animals, 11(2), 399. http://dx.doi.org/10.3390/ani11020399
42. Lan, R. X., Li, S. Q., Zhao, Z., & An, L. L. (2020). Sodium butyrate as an effective feed additive to improve growth performance and gastrointestinal development in broilers. Veterinary Medicine and Science, 6(3), 491-499. http://dx.doi.org/10.1002/vms3.250
43. Leeson, S., Namkung, H., Antongiovanni, M., & Lee, E. H. (2005). Effect of butyric acid on the performance and carcass yield of broiler chickens. Poultry science, 84(9), 1418-1422. http://dx.doi.org/10.1093/ps/84.9.1418
44. Mahdavi, R., & Torki, M. (2009). Study on usage period of dietary protected butyric acid on performance. Journal of Animal and Veterinary Advances, 8(9), 1702-1709.
45. Mahrous, H. S., El-Far, A. H., Sadek, K. M., & Abdel-Latif, M. A. (2017). Effects of different levels of clove bud (Syzygium aromaticum) dietary supplementation on immunity, antioxidant status, and performance in broiler chickens. Alexandria Journal for Veterinary Sciences, 54(2): 29-32. http://dx.doi.org/10.5455/ajvs.272231
46. Marcu, A., Vacaru-Opriş, I., Dumitrescu, G., Ciochină, L. P., Marcu, A., Nicula, M., Peţ, I., Dronca, D., Kelciov, B., & Mariş, C. (2013). The influence of genetics on economic efficiency of broiler chicken’s growth. Animal Science and Biotechnologies, 46(2), 339-346.
47. Micciche, A. C., Foley, S. L., Pavlidis, H. O., McIntyre, D. R., & Ricke, S. C. (2018). A review of prebiotics against Salmonella in poultry: current and future potential for microbiome research applications. Frontiers in Veterinary Science, 5(191), 1-11. http://dx.doi.org/10.3389/fvets.2018.00191 
48. Mohammadbagheri, N., & Najafi, R. (2014). 'The effect of citric acid and phytase on performance, blood lipid profile, immune system and some carcass characteristics of broiler chickens. Iranian Journal of Animal Science Research, 6(2), 131-139. (In Persian). http://dx.doi.org/10.22067/ijasr.v6i2.27800
49. Mohammadi, Z., Ghazanfari, S., & Moradi, M. A. (2014). Effect of supplementing clove essential oil to the diet on microflora population, intestinal morphology, blood parameters and performance of broilers. European Poultry Science, 78, 51-59. http://dx.doi.org/10.1399/eps.2014.51
50. Mohammadpour, A. A., Kermanshahi, H., Golian, A., Gholizadeh, M., & Gilani, A. (2014). Evaluation of varying levels of acid-binding capacity of diets formulated with various acidifiers on physical and histological characteristics of leg bones in broiler chickens. Comparative Clinical Pathology, 23(5), 1409-1420. http://dx.doi.org/10.1007/ s00580-013-1798-1
51. Monir, M. M., Hiramatsu, K., Nishimura, K., Takemoto, C., & Watanabe, T. (2014). Distribution of glucagon-like peptide (GLP)-2-immunoreactive cells in the chicken small intestine: antigen retrieval immunohistochemistry. Journal of Veterinary Medical Science, 76(4), 565-568. http://dx.doi.org/10.1292/jvms.13-0513
52. Moquet, P. C. A., Salami, S. A., Onrust, L., Hendriks, W. H., & Kwakkel, R. P. (2018). Butyrate presence in distinct gastrointestinal tract segments modifies differentially digestive processes and amino acid bioavailability in young broiler chickens. Poultry Science, 97(1), 167-176. http://dx.doi.org/10.3382/ps/pex279
53. Moustafa, N., Aziza, A., Orma, O., & Ibrahim, T. (2020). Effect of supplementation of broiler diets with essential oils on growth performance, antioxidant status, and general health. Mansoura Veterinary Medical Journal, 21(1), 14-20. http://dx.doi.org/10.21608/MVMJ.2020.21.103
54. Nezhady, M. A. M., Zabihi, S. L., & Kalhori, M. M. (2011). Effect of different level of butyric acid glycerides on performance and serum composition of broiler chickens. World Journal of Zoology, 6(2), 179-182.
55. Nouri, M., Ghorbani, M. R., Tatar, A., & Mehrnia, M. A. (2018). Effect of clove essential oil nanoemulsion on performance of broiler chickens fed diet based on wheat. Animal Production, 20(2), 315-327. http://dx.doi.org/10.22059/jap.2018.254359.623268
56. Ogwuegbu, M., Oyeagu, C., Edeh, H., Dim, C., Ani, A., & Lewu, F. (2021). Effects of sodium butyrate and rosemary leaf meal on general performance, carcass traits, organ sizes and nutrient digestibility of broiler chickens. Iranian Journal of Applied AnimalSciences, 11(2), 365-379. http://dx.doi.org/20.1001.1.2251628.2021.11.2.18.2
57. Olgun, O. (2016). The effect of dietary essential oil mixture supplementation on performance, egg quality and bone characteristics in laying hens. Annals of Animal Science, 16(4), 1115-1125. http://dx.doi.org/10.1515/aoas-2016-0038
58. Onyango, E. M., Hester, P. Y., Stroshine, R., & Adeola, O. (2003). Bone densitometry as an indicator of percentage tibia ash in broiler chicks fed varying dietary calcium and phosphorus levels. Poultry Science, 82(11), 1787-1791. http://dx.doi.org/10.1093/ps/82.11.1787
59. Panda, A. K., Rao, S. V., Raju, M. V. L. N., & Sunder, G. S. (2009). Effect of butyric acid on performance, gastrointestinal tract health and carcass characteristics in broiler chickens. Asian-Australasian Journal of Animal Sciences, 22(7), 1026-1031. http://dx.doi.org/10.5713/AJAS.2009.80298
60. Park, J., Kim, M., Kang, S. G., Jannasch, A. H., Cooper, B., Patterson, J., & Kim, C. H. (2015). Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR–S6K pathway. Mucosal Immunology, 8(1), 80-93. http://dx.doi.org/10.1038/mi.2014.44
61. Paul, S. S., Rama Rao, S. V., Hegde, N., Williams, N. J., Chatterjee, R. N., Raju, M. V. L. N., Reddy, G. N., Kumar, V., Phani Kumar, P. S., Mallick, , & Gargi, M. (2022). Effects of dietary antimicrobial growth promoters on performance parameters and abundance and diversity of broiler chicken gut microbiome and selection of antibiotic resistance genes. Frontiers in Microbiology, 16(13), 1-19. http://dx.doi.org/10.3389/fmicb.2022.905050
62. Pham, V. H., Kan, L., Huang, J., Geng, Y., Zhen, W., Guo, Y., Abbas, W., & Wang, Z. (2020). Dietary encapsulated essential oils and organic acids mixture improves gut health in broiler chickens challenged with necrotic enteritis. Journal of Animal Science and Biotechnology, 11(1), 1-18. http://dx.doi.org/1186/s40104-019-0421-y
63. Sabbieti, M. G., Agas, D., Maggi, F., Vittori, S., & Marchetti, L. (2011). Molecular mediators involved in Ferulago campestris essential oil effects on osteoblast metabolism. Journal of Cellular Biochemistry, 112(12), 3742-3754. http://dx.doi.org/10.1002/jcb.23306
64. Sadeghiyan, Z., Kazemi fard, M., Rezaei, M., Jafarpour, S. A. (2023). Effect of encapsulated organic acids on intestinal microbial population, blood parameters, digestibility of nutrients, carcass characteristics and performance of broiler chickens. Iranian Journal of Animal Science Research, 15(1), 77-92. http://dx.doi.org/10.22067/ijasr.2022.75043.1065
65. Salimian, A. M., Tabeidian, S. A., & Irandoust, H. (2016). Dietary effects of cinnamon, turmeric and carnation powders on performance, morphological changes of intestine and blood serum oxidation status of broilers. Animal Production, 18(1), 141-150. http://dx.doi.org/22059/jap.2016.55235
66. SAS (2003). SAS user’s guide: statistics. Version 7.0. Cary (NC): SAS Institute.
67. Sevim, B., & Cufadar, Y. (2021). Effects of essential oils and their combinations added to broiler diets on the mineral contents of some tissues and bone breaking strength. Roczniki Naukowe Polskiego Towarzystwa Zootechnicznego, 17(2), 1-12. http://dx.doi.org/10.5604/01.3001.0015.3121
68. Sikandar, A., Zaneb, H., Younus, M., Masood, S., Aslam, A., Khattak, F., Ashraf, S., Yousaf, M. SH., & Rehman, H. (2017). Effect of sodium butyrate on performance, immune status, microarchitecture of small intestinal mucosa and lymphoid organs in broiler chickens. Asian-Australasian Journal of Animal Sciences, 30(5), 690-699. http://dx.doi.org/10.5713/ajas.16.0824 .
69. Souza, C. S., Vieites, F. M., Justino, L. R., Lima, M. F. D., Chaves, A. S., Minafra, C. S., & Lima, C. A. R. D. (2021). Orange essential oil in the diet of broilers: performance, organ biometrics, bone characteristics, and intestinal morphometry. Revista Brasileira de Zootecnia, 50(78), 1-11. http://dx.doi.org/10.37496/rbz5020200097
70. Su, G., Wang, L., Zhou, X., Wu, X., Chen, D., Yu, B., Huang, Z., Luo, Y., Mao, X., Zheng, P., Yu, J., Luo, J., & He, J. (2021). Effects of essential oil on growth performance, digestibility, immunity, and intestinal health in broilers. Poultry Science, 100(8), 101242- 101242. http://dx.doi.org/10.1016/j.psj.2021.101242
71. Świątkiewicz, S., Koreleski, J., & Arczewska, A. (2010). Effect of organic acids and prebiotics on bone quality in laying hens fed diets with two levels of calcium and phosphorus. Acta Veterinaria Brno, 79(2), 185-193. http://dx.doi.org/2754/avb201079020185
72. Taherpour, K., Moravej, H., Shivazad, M., Adibmoradi, M., & Yakhchali, B. (2009). Effects of dietary probiotic, prebiotic and butyric acid glycerides on performance and serum composition in broiler chickens. African Journal of Biotechnology, 8(10), 2329-2334. http://dx.doi.org/10.2141/jpsa.011031
73. Toghyani, M., Toghyani, M., Gheisari, A., Ghalamkari, G., & Mohammadrezaei, M. (2010). Growth performance, serum biochemistry and blood hematology of broiler chicks fed different levels of black seed (Nigella sativa) and peppermint (Mentha piperita). Livestock science, 129(1-3), 173-178. http://dx.doi.org/10.1016/j.livsci.2010.01.021
74. Torki, M., Mohebbifar, A., & Mohammadi, H. (2021). Effects of supplementing hen diet with Lavandula angustifolia and/or Mentha spicata essential oils on production performance, egg quality and blood variables of laying hens. Veterinary Medicine and Science, 7(1), 184-193. http://dx.doi.org/10.1002/vms3.343
75. Van Immerseel, F., De Zutter, L., Houf, K., Pasmans, F., Haesebrouck, F., & Ducatelle, R. (2009). Strategies to control Salmonella in the broiler production chain. World's Poultry Science Journal, 65(3), 367-392. http://dx.doi.org/10.1017/S004393390900027.
76. Vinolya, R. E., Balakrishnan, U., Yasir, B., & Chandrasekar, S. (2021). Effect of dietary supplementation of acidifiers and essential oils on growth performance and intestinal health of broiler. Journal of Applied Poultry Research, 30(3), 100179. http://dx.doi.org/10.1016/j.japr.2021.100179
77. Weber, G. M., Michalczuk, M., Huyghebaert, G., Juin, H., Kwakernaak, C., & Gracia, M. I. (2012). Effects of a blend of essential oil compounds and benzoic acid on performance of broiler chickens as revealed by a meta-analysis of 4 growth trials in various locations. Poultry Science, 91(11), 2820-2828. http://dx.doi.org//10.3382/ps.2012-02243
78. Wu, W., Xiao, Z., An, W., Dong, Y., & Zhang, B. (2018). Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PLOS One, 13(5), e0197762. http://dx.doi.org/10.1371/journal.pone.0197762
79. Yildirim, B. A., Tunc, M. A., Gül, M., Yildirim, F., & Yıldız, A. (2018). The effect of Rosemary (Rosmarinus officinalis) extract supplemented into broiler diets, on performance and blood parameters. GSC Biological and Pharmaceutical Sciences, 2(3), 001-009. http://dx.doi.org/10.30574/gscbps.2018.2.3.0057
80. Yin, F., Yu, H., Lepp, D., Shi, X., Yang, X., Hu, J., & Gong, J. (2016). Transcriptome analysis reveals regulation of gene expression for lipid catabolism in young broilers by butyrate glycerides. PLOS One, 11(8), e0160751. http://dx.doi.org/10.1371/journal.pone.0160751
81. Zhang, B., & Coon, C. N. (1997). The relationship of various tibia bone measurements in hens. Poultry Science, 76(12),1698-1701. http://dx.doi.org/10.1093/ps/76.12.1698
82. Zhao, X., Zheng, S., Wei, S., Tian, Q., Tao, Y., Bo, R., & Li, J. (2022). The protective effect and potential mechanisms of eugenol against Salmonella in vivo and in vitro. Poultry Science, 101(5), 101801. http://dx.doi.org/10.1016/j.psj.2022.101801
83. Zhou, Z. Y., Packialakshmi, B., Makkar, S. K., Dridi, S., & Rath, N. C. (2014). Effect of butyrate on immune response of a chicken macrophage cell line. Veterinary Immunology and Immunopathology, 162(1-2), 24-32. http://dx.doi.org/10.1016/j.vetimm.2014.09.002