Impacts of Withania coagulans extracts, linseed, and fish oil on performance, tibia bone characteristics, and mineralization in broiler chicken

Document Type : Original Research Article (Regular Paper)

Authors

Department Animal Science, Higher Education Complex of Saravan. Saravan, Sistan and Baluchestan, Iran

Abstract

This study was designed to evaluate the impact of Withania coagulans extracts [fruit (WFE) and root (WRE)], linseed oil (LO), and fish oil (FO) on growth performance, tibia bone characteristics, calcium and phosphorus content in tibia and serum, biochemical indicators of bone metabolism, and certain blood parameters in broilers. The study involved 720 male Ross 308 broilers, which were allotted to a completely random design containing 9 treatments with 8 replications of 10 birds each. The experimental treatments included a basal diet (Control), basal diet + 200 mg/kg WRE or WFE, basal diet + 2% fish oil or flaxseed oil, a diet containing 2% fish oil + 200 mg/kg WRE or WFE, and a diet containing 2% flaxseed oil + 200 mg/kg WRE or WFE. Body weight and body weight gain increased from 1–21 and 22–42 days with the addition of FO and WFE compared to the control group. The highest values of bone stiffness, ultimate load, and mineral density (BMD) were observed in birds supplemented with a mixture of FO + WFE, while the lowest values were observed in birds fed the basal diet without supplements. Diets containing fish oil supplemented with WC extracts led to increased serum calcium and tibia calcium levels compared to other groups (P≤ 0.05). Supplementation with LO and FO reduced PGE2 concentration compared to other treatment groups (P ≤ 0.05). No significant difference was observed in serum serum tartrate-resistant acid phosphatase (TRAP) levels across all experimental groups (P>0.05). In conclusion, the combination of oil source (FO) and extract (WFE) in the diet improved the performance of birds, increased bone characteristics and calcium levels in serum and tibia, and altered biochemical indicators of bone metabolism in serum, suggesting that this combination could be beneficial to the health and performance of broilers.

Keywords

Main Subjects


References
Abraham, G., Gottschalk, J., Ungemach, F.R., 2005. Evidence for ototopical glucocorticoid-induced decrease in hypothalamic-pituitary-adrenal axis response and liver function. Endocrinology 146, 3163-3171.
Akbari Moghaddam Kakhki, R., Ma, D.W.L., Price, K.R., Moats, J.R., Karrow, N.A., Kiarie, E.G., 2020. Enriching ISA brown and Shaver white breeder diets with sources of n− 3 polyunsaturated fatty acids increased embryonic utilization of docosahexaenoic acid. Poultry Science 99, 1038-1051.
Alba, M., Esmaeilipour, O., Mirmahmoudi, R., 2015. Effects of Withania coagulans fruit powder and vitamin C on growth performance and some blood components in heat-stressed broiler chickens. Livestock Science 173, 64–68.
Albertazzi, P., Coupland, K., 2002. Polyunsaturated fatty acids. Is there a role in postmenopausal osteoporosis prevention?  Maturitas 42, 13–22.
Ali Tavakkoli, A., Mirakzehi, M.T., Saleh, H., Yousefi, M., 2021. The effects of supplementation of Withania coagulans and α-tocopherol acetate in diets containing oxidised oil on growth performance, immune response and antioxidant indices in broiler chickens. Archives of Animal Nutrition 75, 278-293.
Attia, Y.A., Al-Harthi, M.A., Abo-Al Maaty, H., 2020. The effects of different oil sources on performance, digestive enzymes, carcass traits, biochemical, immunological, antioxidant, and morphometric responses of broiler chicks. Frontiers in Veterinary Science  7, 181.
Azhar, M. F., Naseer, U., Aziz, A., Zafar, S., Qadir, I., Farooq, M., Ahmad, I., Anjum, K., 2020. Antioxidant and phytochemical composition of leaves, stem, and root extracts of Withania coagulans and Withania somnifera. Journal of Medicinal and Spice Plants 24, 27-30.
Baird, H.T., Eggett, D.L., Fullmer, S., 2008. Varying ratios of omega-6: omega-3 fatty acids on the pre-and postmortem bone mineral density, bone ash, and bone breaking strength of laying chickens. Poultry Science 87, 323-328.
Bautista-Ortega, J., Goeger, D.E., Cherian, G., 2009. Egg yolk omega-6 and omega-3 fatty acids modify tissue lipid components, antioxidant status, and ex vivo eicosanoid production in chick cardiac tissue. Poultry Science 88, 1167-1175.
Beck, M.M., Hansen, K.K., 2004. Role of estrogen in avian osteoporosis. Poultry Science 83, 200-206.
Boivin, G., Meunier, P.J., 2002. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcified Tissue International 70, 503.
Cipriani, C., Colangelo, L., Santori, R., Renella, M., Mastrantonio, M., Minisola, S., Pepe, J., 2020. The interplay between bone and glucose metabolism. Frontiers in Endocrinology 11, 122.
Coetzer, H., Claassen, N., Van Papendorp, D.H., Kruger, M.C., 1994. Calcium transport by isolated brush border and basolateral membrane vesicles: role of essential fatty acid supplementation. Prostaglandins, Leukotrienes, and Essential Fatty Acids 50, 257-266.
Croteau, R., Kutchan, T.M., Lewis, N.G., 2000. Natural products (secondary metabolites). Biochemistry and Molecular Biology of Plants 24, 1250-1319.
Ebeid, T., Eid, Y., Saleh, A., Abd El-Hamid, H., 2008. Ovarian follicular development, lipid peroxidation, antioxidative status, and immune response in laying hens fed fish oil-supplemented diets to produce n-3-enriched eggs. Animal 2, 84-91.
El-Samee, L. D., El-Wardany, I., Abdel-Fattah, S.H., Abd El-Azeem, N.A., Elsharkawy, M.S., 2019. Dietary omega-3 and antioxidants improve long-chain omega-3 and lipid oxidation of broiler meat. Bulletin of the National Research Centre; Berlin  43, 1-9.
El-Sayed, E., Ibrahim, K., 2017. Effect of the types of dietary fats and non-dietary oils on bone metabolism. Critical Reviews in Food Science and Nutrition 57, 653-658.
Evans, D.B., Bunning, R.A., Russell, R.G., 1990. The effects of recombinant human interleukin-1 beta on cellular proliferation and the production of prostaglandin E2, plasminogen activator, osteocalcin and alkaline phosphatase by osteoblast-like cells derived from human bone. Biochemical and Biophysical Research Communications 166, 208–216.
Gorelick, J., Rosenberg, R., Smotrich, A., Hanuš, L., Bernstein, N., 2015. Hypoglycemic activity of withanolides and elicitated Withania somnifera. Phytochemistry 116, 283-289.
Green, K.H., Wong, S.C.F., Weiler, H.A., 2004. The effect of dietary n-3 long-chain polyunsaturated fatty acids on femur mineral density and biomarkers of bone metabolism in healthy, diabetic, and dietary-restricted growing rats. Prostaglandins, Leukotrienes, and Essential Fatty Acids 71, 121-130.
Griel, A.E., Kris-Etherton, P.M., Hilpert, K.F., Zhao, G., West, S.G., Corwin, R.L., 2007. An increase in dietary n-3 fatty acids decreases a marker of bone resorption in humans. Nutrition Journal 6, 1-8.
Gupta, G.L., Rana, A.C., 2007. Withania somnifera (Ashwagandha): a review. Pharmacognosy Reviews 1,129-136
Hie, M., Tsukamoto, I., 2010. Increased expression of the receptor for activation of NF-kappaB and decreased runt-related transcription factor 2 expression in bone of rats with streptozotocin-induced diabetes. International Journal of Molecular Medicine 26, 611–618.
Hosseini, S.J., Kermanshahi, H., Nassirimoghaddam, H., Nabipour, A., Mirakzehi, M.T., Saleh, H., Kazemifard, M., 2016. Effects of 1.25-dihydroxycholecalciferol and hydroalcoholic extract of Withania coagulans fruit on bone mineralization and mechanical and histological properties of male broiler chickens. Brazilian Journal of Poultry Science 18, 73-86.
Hothersall, E. J., Livingstone, S.J., Looker, H.C., Ahmed, S.F., Cleland, S., Leese, G.P., Lindsay, R.S., McKnight, J., Pearson, D., Philip, S., Wild, S.H., Colhoun, H.M., 2014. Contemporary risk of hip fracture in type 1 and type 2 diabetes: A national registry study from scotland.  Journal of Bone and Mineral Research 29, 1054-1060.
Huang, S., Kong, A., Cao, Q., Tong, Z., Wang, X., 2019. The role of blood vessels in broiler chickens with tibial dyschondroplasia. Poultry Science 98, 6527-6532.
Incharoen, T., Tartrakoon, W., Nakhon, S., Treetan, S., 2016. Effects of dietary silicon derived from rice hull ash on the meat quality and bone breaking strength of broiler chickens. Asian Journal of Animal and Veterinary Advances 11, 417-422.
Jain, R., Kachhwaha, S., Kothari, S.L., 2012. Phytochemistry, pharmacology, and biotechnology of Withania somnifera and Withania coagulans: A review. Journal of Medicinal Plants Research 6, 5388-5399.
Jämsä, T., Jalovaara, P., Peng, Z., Väänänen, H.K., Tuukkanen, J., 1998. Comparison of three-point bending test and peripheral quantitative computed tomography analysis in the evaluation of the strength of mouse femur and tibia. Bone 23, 155-161.
Jia, W., Slominski, B.A., 2010. Means to improve the nutritive value of flaxseed for broiler chickens: The effect of particle size, enzyme addition, and feed pelleting. Poultry Science 89, 261-269.
Kajii, T., Suzuki, K., Yoshikawa, M., Imai, T., Matsumoto, A., Nakamura, S., 1999. Long-term effects of prostaglandin E2 on the mineralization of a clonal osteoblastic cell line (MC3T3-E1). Archives of Oral Biology  44, 233-241.
Kalakuntla, S., Nagireddy, N.K., Panda, A.K., Jatoth, N., Thirunahari, R., Vangoor, R., 2017. Effect of dietary incorporation of n-3 polyunsaturated fatty acids rich oil sources on fatty acid profile, keeping quality and sensory attributes of broiler chicken meat. Animal Nutrition (Zhongguo xu mu shou yi xue hui) 3, 386-391.
Khattak, F., Ronchi, A., Castelli, P., Sparks, N., 2014. Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poultry Science 93, 132-137.
Khedgikar, V., Ahmad, N., Kushwaha, P., Gautam, J., Nagar, G.K., Singh, D., Trivedi, P.K., Mishra, P.R., Sangwan, N.S., Trivedi, R.J.N., 2015. Preventive effects of withaferin A isolated from the leaves of an Indian medicinal plant Withania somnifera (L.): Comparisons with 17-β-estradiol and alendronate. Nutrition (Burbank, Los Angeles County, Calif.) 31, 205-213.
Koreleski, J., Swiatkiewicz, S., Sciences, F., 2006. The influence of dietary fish oil and vitamin E on the fatty acid profile and oxidative stability of frozen stored chicken breast meat. Journal of Animal and Feed Sciences 15, 631.
Lau, B.Y., Cohen, D.J., Ward, W.E., Ma, D.W., 2013. Investigating the role of polyunsaturated fatty acids in bone development using animal models. Molecules 18, 14203-14227.
Lau, B.Y., Fajardo, V.A., McMeekin, L., Sacco, S.M., Ward, W.E., Roy, B.D., Peters, S.J., Leblanc, P.J., 2010. Influence of high-fat diet from differential dietary sources on bone mineral density, bone strength, and bone fatty acid composition in rats. Applied Physiology, Nutrition, and Metabolism 35, 598–606.
Liu, D., Veit, H.P., Wilson, J.H., Denbow, D.M., 2003. Long-term supplementation of various dietary lipids alters bone mineral content, mechanical properties and histological characteristics of Japanese quail. Poultry Science 82, 831-839.
Lukas, R., Gigliotti, J.C., Smith, B.J., Altman, S.,Tou, J.C, 2011. Consumption of different sources of omega-3 polyunsaturated fatty acids by growing female rats affects long bone mass and microarchitecture. Bone 49, 455-462.
Mailhot, G., Rabasa-Lhoret, R., Moreau, A., Berthiaume, Y., Levy, E., 2010. CFTR depletion results in changes in fatty acid composition and promotes lipogenesis in intestinal Caco 2/15 cells. PLoS One 5, e10446.
Marshall, L.A., Johnston, P.V., 1982. Modulation of tissue prostaglandin synthesizing capacity by increased ratios of dietary alpha‐linolenic acid to linoleic acid. Lipids 17, 905-913.
Maurya, R., 2010. Chemistry and pharmacology of Withania coagulans: an Ayurvedic remedy. The Journal of Pharmacy and Pharmacology  62, 153-160.
Minkin, C., 1982. Bone acid phosphatase: tartrate-resistant acid phosphatase as a marker of osteoclast function. Calcified Tissue International 34, 285-290.
Mirakzehi, M., Hosseini, S.J., Saleh, H., 2017. The effects of hydroalcoholic extracts of Withania somnifera root, Withania coagulans fruit, and 1, 25-dihydroxycholecalciferol on immune response and small intestinal morphology of broiler chickens. Journal of Applied Animal Research 45, 591-597.
Mollard, R.C., Gillam, M.E., Wood, T.M., Taylor, C.G., Weiler, H.A., 2005. (n-3) Fatty acids reduce the release of prostaglandin E2 from bone but do not affect bone mass in obese (fa/fa) and lean Zucker rats. The Journal of Nutrition 135, 499-504.
Prasad, S.K., Kumar, R., Patel, D.K., Hemalatha, S., 2010. Wound healing activity of Withania coagulans in streptozotocin-induced diabetic rats. Pharmaceutical Biology 48, 1397-1404.
Saleh, H., Golian, A., Kermanshahi, H., Farhoosh, R., Mirakzehi, M., 2016. Effect of α-tocopherol acetate, pomegranate peel and extract on performance, nutrient digestibilities, and tibia bone calcification in broiler chickens. Research On Animal Production 6, 1-11.
Saleh, H., Rahimi, S., Karimi, M.T., 2009. The effect of a diet that contained fish oil on performance, serum parameters, the immune system, and the fatty acid composition of meat in broilers.  Iranian Journal of Veterinary Medicine 3, 69-75.
Saleh, H., Golian, A., Kermanshahi, H., Mirakzehi, M., 2018. Antioxidant status and thigh meat quality of broiler chickens fed a diet supplemented with α-tocopherolacetate, pomegranate pomace, and pomegranate pomace extract.  Italian Journal of Animal Science 17, 386-395.
Shang, X.G., Wang, F.L., Li, D.F., Yin, J.D., Li, J.Y., 2004. Effects of dietary conjugated linoleic acid on the productivity of laying hens and egg quality during refrigerated storage. Poultry Science 83, 1688-1695.
Simopoulos, A.P., 2010. The omega-6/omega-3 fatty acid ratio: health implications. Oléagineux, Corps Gras, Lipides 17, 267-275.
Sousa, C.P., Nery, F., Azevedo, J.T., Viegas, C.A., Gomes, M.E., Dias, I.R., 2011. Tartrate-resistant acid phosphatase as a biomarker of bone turnover in dog. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia Overview 63, 40-45.
Tahmasbi, A.M., Mirakzehi, M.T., Hosseini, S.J., Agah, M.J., Kazemi Fard, M., 2012. The effects of phytase and root hydroalcoholic extract of Withania somnifera on productive performance and bone mineralisation of laying hens in the late phase of production. British Poultry Science 53, 204-214.
Tarlton, J.F., Wilkins, L.J., Toscano, M.J., Avery, N.C., Knott, L., 2013. Reduced bone breakage and increased bone strength in free range laying hens fed omega-3 polyunsaturated fatty acid supplemented diets. Bone 52, 578-586.
Uddin, Q., Samiulla, L., Singh, V.K., Jamil, S.S., 2012. Phytochemical and pharmacological profile of Withania somnifera Dunal: a review. Journal of Applied Pharmaceutical Science 2, 170-175.
Van Straalen, J.P., Sanders, E., Prummel, M.F., Sanders, G.T.,1991. Bone-alkaline phosphatase as indicator of bone formation. Clinica Chimica Acta; International Journal of Clinical Chemistry  201, 27-33.
Wang, Y.B., Yang, X.J., Qin, D.K., Feng, Y., Guo, Y.M., Yao, J.H., 2011. Effects of eicosapentaenoic acid and docosahexaenoic acid on responses of LPS-stimulated intestinal B lymphocytes from broiler chickens studied in vitro. European Food Research and Technology 233, 677-683.
Watkins, B.A., Li, Y., Lippman, H.E., Feng, S., 2003. Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins, Leukotrienes, and Essential Fatty Acids 68, 387-398.
Watkins, B.A., Shen, C.L., Allen, K.G., Seifert, M.F., 1996. Dietary (n-3) and (n-6) polyunsaturates and acetylsalicylic acid alter ex vivo PGE2 biosynthesis, tissue IGF-I levels, and bone morphometry in chicks. Journal of Bone and Mineral Research 11, 1321-1332.
Williams, B., Solomon, S., Waddington, D., Thorp, B., Farquharson, C., 2000. Skeletal development in the meat-type chicken. British Poultry Science 41, 141-149.
You, L., Sheng, Z.Y., Tang, C.L., Chen, L., Pan, L., Chen, J.Y., 2011. High cholesterol diet increases osteoporosis risk via inhibiting bone formation in rats. Acta Pharmacologica Sinica 32, 1498-1504.
Zhang, G.F., Yang, Z.B., Wang, Y., Yang, W.R., Jiang, S.Z., Gai, G.S., 2009. Effects of ginger root (Zingiber officinale) processed to different particle sizes on growth performance, antioxidant status, and serum metabolites of broiler chickens. Poultry Science 88, 2159-2166.