The effects of Hydroalcoholic Extract of Withania Somnifera Leaf and Fish Oil on Growth Performance, Bone Calcification, Morphological and Mechanical Characteristics and Gene Expression in Broiler Chickens

Document Type : Original Paper

Authors

1 Department of Animal Science, Higher Education Complex of Saravan. P.O. Box: 99516-34145, Saravan, Sistan and Baluchestan, Iran

2 Department of Biology, University of Sistan and Baluchestan, P.O. Box: +98155-987, Zahedan, Iran

Abstract

This experiment was conducted to study the effects of hydroalcoholic extract from Withania somnifera (WS) leaf and fish oil on performance, mineral retention, bone morphological and mechanical characteristics, and Calbindin-D 28K (CALB1) gene expression in broiler chickens. Treatments were arranged in a CRD with a 2 × 3 × 2 factorial arrangement consisted of two dietary Ca levels (low: 30% less than normal Ca level, and adequate: normal Ca level), three concentrations of WS (0, 100 and 200 mg/kg diet) and two concentrations of fish oil (0 and 2 %). A total of 600 one-day-old Ross 308 male broilers were divided into 12 treatments with 5 replicates and 10 chickens in each. At 24 d of age, one bird per replicate was randomly killed, and tibiae were removed. Results showed that dietary supplementation of WS significantly improved feed conversion ratio (FCR) (P < 0.05). Birds fed diets supplemented with WS had significantly higher Ca content in the tibia (P < 0.05). Dietary inclusion of fish oil significantly increased the width of the bone proliferative zone (P < 0.05). In biomechanical properties, dietary supplementation of WS and fish oil significantly increased the shear force (P < 0.05). Synergistic effects of WS and fish oil showed that the addition of WS at 200 mg/kg in birds fed diets containing fish oil led to a significant increase in tibial stiffness (P < 0.05). Low-Ca diet up-regulated duodenal CALB1 mRNA expression (P < 0.05). Supplementation of WS also resulted in a significant up-regulation in the gene expression of CALB1in both duodenum and jejunum (P < 0.001). In conclusion, dietary supplementation of WS may have beneficial effects on bone calcification and strength by increasing the CALB1 gene expression and Ca retention. Also, synergistic effects of WS and fish oil may improve the mechanical properties of the tibia.

Keywords

References

Abou‐Douh AM. 2002. New withanolides and other constituents from the fruit of Withania somnifera. Archiv der Pharmazie: An International Journal Pharmaceutical and Medicinal Chemistry, 335: 267-276. DOI: 10.1002/1521-4184(200208)335: 6<267::AID-ARDP267>3.0.CO;2-E
Alexander RT, Rievaj J & Dimke H. 2014. Paracellular calcium transport across renal and intestinal epithelia. Biochemistry and Cell Biology, 92: 467-480. DOI: 10.1139/bcb-2014-0061
An BS, Kang SK, Shin JH & Jeung EB. 2002. Stimulation of calbindin-D(9k) mRNA expression in the rat uterus by octyl-phenol, nonylphenol and bisphenol. Molecular and Cellular Endocrinology, 191: 177-186. DOI: 10.1016/S0303-7207(02)00042-4
AOAC International. 2005. Official Methods of Analysis of AOAC International. 18th ed. (Gaithersburg, MD, AOAC Int.). DOI: 10.1093/jaoac/80.6.127A
Ariel A & Serhan CN. 2007. Resolvins and protectins in the termination program of acute inflammation. Trends in Immunology, 28: 176-183. DOI: 10.1016/j.it.2007.02.007
Aviagen. 2007. Ross 308: broiler nutrition specifications. Aviagen, Huntsville, Alabama, USA.
Barreira IC, Ferreira IC, Oliveira MBP, Pereira JA. 2008. Antioxidant activities of the extracts from chestnut flower, leaf, skins and fruit. Food chemistry, 107: 1106-1113. DOI: 10.1016/j.foodchem.2007.09.030
Brini M & Carafoli E. 2011. The plasma membrane Ca2+ ATPase and the plasma membrane sodium calcium exchanger cooperate in the regulation of cell calcium. Cold Spring Harbor Perspectives in Biology, 3: a004168.  DOI: 10.1101/cshperspect. a0041681
Carmeliet G, Dermauw V & Bouillon R. 2015. Vitamin D signaling in calcium and bone homeostasis: a delicate balance. Best Practice & Research Clinical Endocrinology & Metabolism, 29: 621-631. DOI: 10.1016/j.beem.2015.06.001
Dhuley J, Raman P, Mujumdar A & Naik S. 1993. Inhibition of lipid peroxidation by piperine during experimental inflammation in rats. Indian Journal of Experimental Biology, 31(5): 443-445.
Dibner J, Richards J, Kitchell M & Quiroz M. 2007. Metabolic challenges and early bone development. Journal of Applied Poultry Research, 16(1): 126-137. DOI: 10.1093/japr/16.1.126
Dimke H, Hoenderop JG & Bindels RJ. 2011. Molecular basis of epithelial Ca2+ and Mg2+ transport: insights from the TRP channel family. Journal of Physiology, 589(7): 1535-1542. DOI: 10.1113/jphysiol.2010.199869
Dwivedi V, Singh V, Tewari D, Gautam S & Singh S. 2015. Effect of ashwagandha (Withania somnifera) on performance, hemato-biochemical parameters and economics of broiler production. Animal Nutrition and Feed Technology, 15(2): 207-216. DOI: 10.5958/0974-181X.2015.00023.2
Gloux A, Le Roy N, Brionne A, Bonin E, Juanchich A, Benzoni G, Piketty M, Prié D, Nys Y & Gautron J. 2019. Candidate genes of the transcellular and paracellular calcium absorption pathways in the small intestine of laying hens. Poultry Science, 98: 6005-6018. DOI: 10.3382/ps/pez407
González-Cerón F, Rekaya R & Aggrey S. 2015. Genetic analysis of bone quality traits and growth in a random mating broiler population. Poultry Science, 94(5): 883-889. DOI: 10.3382/ps/pev056
Güz B, Molenaar R, de Jong I, Kemp B, van den Brand H & van Krimpen M. 2019. Effects of dietary organic minerals, fish oil, and hydrolyzed collagen on growth performance and tibia characteristics of broiler chickens. Poultry Science, 98: 6552-6563. DOI: 10.3382/ps/pez427
Ichikawa H, Takada Y, Shishodia S, Jayaprakasam B, Nair MG & Aggarwal BB. 2006. Withanolides potentiate apoptosis, inhibit invasion, and abolish osteoclastogenesis through suppression of nuclear factor-κB (NF-κB) activation and NF-κB–regulated gene expression. Molecular Cancer Therapeutics, 5(6): 1434-1445. DOI: 10.1158/1535-7163.MCT-06-0096
Kathirvel A & Sujatha V.  2016. Phytochemical studies, antioxidant activities and identification of active compounds using GC–MS of Dryopteris cochleata leaves. Arabian Journal of Chemistry, 9: S1435-S1442. DOI: 10.1016/j.arabjc.2012.03.018
Kim W, Bloomfield S & Ricke S. 2011. Effects of age, vitamin D3, and fructooligosaccharides on bone growth and skeletal integrity of broiler chicks. Poultry Science, 90: 2425-2432. DOI: 10.3382/ps.2011-01475
Kruger M, Claassen N, Smuts C & Potgieter H. 1997. Correlation between essential fatty acids and parameters of bone formation and degradation. Asia Pacific Journal of Clinical Nutrition, 6: 235-238.
Kuang Z, Bai J, Ni L, Hang K, Xu J, Ying L, Xue D & Pan Z. 2020. Withanolide B promotes osteogenic differentiation of human bone marrow mesenchymal stem cells via ERK1/2 and Wnt/β-catenin signaling pathways. International Immunopharmacology, 88: 106960. DOI: 10.1016/j.intimp.2020.106960
Lau BY, Ward WE, Kang JX & Ma DW. 2009. Femur EPA and DHA are correlated with femur biomechanical strength in young fat-1 mice. The Journal of Nutritional Biochemistry, 20(6): 453-461. DOI: 10.1016/j.jnutbio.2008.05.004
Li J, Yuan J, Guo Y, Sun Q & Hu X. 2012. The influence of dietary calcium and phosphorus imbalance on intestinal NaPi-IIb and calbindin mRNA expression and tibia parameters of broilers. Asian-Australasian Journal of Animal Sciences, 25: 552-558. DOI: 10.5713/ajas.2011.11266
Liang T, Yue W & Li Q. 2010. Comparison of the phenolic content and antioxidant activities of Apocynum venetum L. (Luo-Bu-Ma) and two of its alternative species. International Journal of Molecular Sciences, 11: 4452-4464. DOI: 10.3390/ijms11114452
Liel Y, Shany S, Smirnoff P & Schwartz B. 1999. Estrogen increases 1, 25-dihydroxyvitamin D receptors expression and bioresponse in the rat duodenal mucosa. Endocrinology, 140: 280-285. DOI: 10.1210/endo.140.1.6408
Liu D, Veit H, Wilson J & Denbow D. 2003a. Maternal dietary lipids alter bone chemical composition, mechanical properties, and histological characteristics of progeny of Japanese quail. Poultry Science, 82: 463-473. DOI: 10.1093/ps/82.3.463
Liu D, Veit H, Wilson JH & Denbow DM. 2003b. Long-term supplementation of various dietary lipids alters bone mineral content, mechanical properties and histological characteristics of Japanese quail. Poultry Science, 82: 831-839. DOI: 10.1093/ps/82.5.831
Liu XS, Ardeshirpour L, VanHouten JN, Shane E & Wysolmerski JJ. 2012. Site‐specific changes in bone microarchitecture, mineralization, and stiffness during lactation and after weaning in mice. Journal of Bone and Mineral Research, 27: 865-875. DOI: 10.1002/jbmr.1503
Livak KJ & Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25: 402-408. DOI: 10.1006/meth.2001.1262
Lorand T, Vigh E & Garai J. 2010. Hormonal action of plant derived and anthropogenic non-steroidal estrogenic compounds: phytoestrogens and xenoestrogens. Current Medicinal Chemistry, 17: 3542-3574. DOI: 10.2174/092986710792927813
Mirakzehi MT, Hosseini S & Saleh H. 2018. Effects of two plant extracts and vitamin D3 on bone mechanical and histological properties of broiler chickens. Journal of Animal and Plant Sciences, 28: 686-694.
Mirakzehi MT, Kermanshahi H, Golian A & Raji AR. 2013. The effects of dietary 1, 25-dihydroxycholecalciferol and hydroalcoholic extract of Withania somnifera root on bone mineralisation, strength and histological characteristics in broiler chickens. British Poultry Science, 54: 789-800. DOI: 10.1080/00071668.2013.850469
Mishra LC, Singh BB & Dagenais S. 2000. Scientific basis for the therapeutic use of Withania somnifera (ashwagandha): a review. Scientific Review of Alternative Medicine, 5: 334-346.
Mushtaq S, Abbasi BH, Uzair B & Abbasi R. 2018. Natural products as reservoirs of novel therapeutic agents. EXCLI Journal, 17: 420-451. DOI: 10.17179/excli2018-1174
Nagareddy PR & Lakshmana M. 2006. Withania somnifera improves bone calcification in calcium‐deficient ovariectomized rats. Journal of Pharmacy and Pharmacology, 58: 513-519. DOI: 10.1211/jpp.58.4.0011
Nie X, Jin H, Wen G, Xu J, An J, Liu X, Xie R & Tuo B. 2020. Estrogen regulates duodenal calcium absorption through differential role of estrogen receptor on calcium transport proteins. Digestive Diseases and Science, 65: 3502-3513. DOI: 10.1007/s10620-020-06076-x
Oyaizu M. 1986. Studies on products of browning reaction prepared from glucose amine products derived from bees. Journal of Pharmaceutical and Biomedical Analysis, 41: 1220-1234.  DOI: 10.5264/eiyogakuzashi.44.307
Plumstead P, Leytem A, Maguire R, Spears J, Kwanyuen P & Brake J. 2008. Interaction of calcium and phytate in broiler diets. 1. Effects on apparent prececal digestibility and retention of phosphorus. Poultry Science, 87: 449-458. DOI: 10.3382/ps.2007-00231
Proszkowiec-Weglarz M & Angel R. 2013. Calcium and phosphorus metabolism in broilers: effect of homeostatic mechanism on calcium and phosphorus digestibility. Journal of Applied Poultry Research, 22: 609-627. DOI: 10.3382/japr.2012-00743
Rasool M & Varalakshmi P. 2006. Immunomodulatory role of Withania somnifera root powder on experimental induced inflammation: An in vivo and in vitro study. Vascular Pharmacology, 44(6): 406-410. DOI: 10.1016/j.vph.2006.01.015
Rasool M & Varalakshmi P. 2007. Protective effect of Withania somnifera root powder in relation to lipid peroxidation, antioxidant status, glycoproteins and bone collagen on adjuvant‐induced arthritis in rats. Fundamental & Clinical Pharmacology, 21: 157-164. DOI: 10.1111/j.1472-8206.2006.00461.x
Rath N, Balog J, Huff W, Huff G, Kulkarni G & Tierce J. 1999. Comparative differences in the composition and biomechanical properties of tibiae of seven-and seventy-two-week-old male and female broiler breeder chickens. Poultry Science, 78: 1232-1239. DOI: 10.1093/ps/78.8.1232
Reddy NP, Lakshmana M & Udupa UV. 2004. Antiosteoporotic activity of OST‐6 (Osteocare), a herbomineral preparation in calcium deficient ovariectomized rats. Phytotherapy Research, 18(1): 25-29. DOI: 10.1002/ptr.1347
Reiter K & Bessei W. 2009. Effect of locomotor activity on leg disorder in fattening chicken. Berliner und Münchener Tierärztliche Wochenschrift, 122(7-8): 264-270.
Salari P, Rezaie A, Larijani B & Abdollahi M. 2008. A systematic review of the impact of n-3 fatty acids in bone health and osteoporosis. Medical Science Monitor 14: RA37-44. DOI: DOI: 10.1017/S0007114512001638
SAS (Statistical Analysis System). 2003. SAS/STAT 9.1. User's Guide. SAS Institute Inc., Cary, NC.
Saunders-Blades J, MacIsaac J, Korver D & Anderson D. 2009. The effect of calcium source and particle size on the production performance and bone quality of laying hens. Poultry Science, 88(2): 338-353. DOI: 10.3382/ps.2008-00278
Setchell KD & Lydeking-Olsen E. 2003. Dietary phytoestrogens and their effect on bone: evidence from in vitro and in vivo, human observational, and dietary intervention studies. American Journal of Clinical Nutrition, 78: 593S-609S. DOI: 10.1093/ajcn/78.3.593S
Tahmasbi AM, Mirakzehi MT, Hosseini SJ, Agah MJ & Fard MK. 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. DOI: 10.1080/00071668.2012.662628
Tancharoenrat P & Ravindran, V. 2014. Influence of tallow and calcium concentrations on the performance and energy and nutrient utilization in broiler starters. Poultry Science, 93: 1453-1462. DOI: 10.3382/ps.2013-03817
Vasanthakumar P, Pangayarselvi B, Sasikumar P, Chandrasekaran D, Doraisamy K & Purushothaman M. 2015. Performance of broilers fed ashwagandha (Withania somnifera) incorporated diets during summer season for alleviating heat stress. Indian Journal of Animal Research, 2646: 1-3. DOI: 10.5958/0976-0555.2015.00082.5
Watkins BA, Li Y, Lippman HE & Feng S. 2003. Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins, Leukotrienes & Essential Fatty Acids, 68: 387-398. DOI: 10.1016/S0952-3278(03)00063-2
Watkins BA, Li Y, Lippman HE, Seifert MF. 2001. Omega-3 polyunsaturated fatty acids and skeletal health. Experimental Biology and Medicine, 226(6): 485-497. DOI: 10.1177/153537020122600601
Watkins BA, Shen CL, McMurtry JP, Xu H, Bain SD, Allen KG & Seifert MF. 1997. Dietary lipids modulate bone prostaglandin E2 production, insulin-like growth factor-I concentration and formation rate in chicks. Journal of Nutrition, 127: 1084-1091. DOI: 10.1093/jn/127.6.1084
Watkins BA, Shen CL, Allen KG & Seifert MF. 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(9): 1321-1332. DOI: 10.1002/jbmr.5650110917
Whitehead CC. 2004. Overview of bone biology in the egg-laying hen. Poultry Science, 83(2): 193-199. DOI: 10.1093/ps/83.2.193
Williams C, David DJ & Iismaa O. 1962. The determination of chromic oxide in faeces samples by atomic absorption spectrophotometry. Journal of Agricultural Science, 59: 381-385. DOI: 10.1017/S002185960001546X
Woudenberg-Vrenken TE, Lameris AL, Weissgerber P, Olausson J, Flockerzi V, Bindels RJ, Freichel M & Hoenderop JG. 2012. Functional TRPV6 channels are crucial for transepithelial Ca2+ absorption. American Journal of Physiology-Gastrointestinal and Liver Physiology, 303: G879-885. DOI: 10.1152/ajpgi.00089.2012
Yang LP, Dong YP, Luo WT, Zhu T, Li QW, Zhang LJ, Kong J, Yuan ZW & Zhao Q. 2018. Calbindin‐D28K mediates 25 (OH) D3/VDR‐regulated bone formation through MMP13 and DMP1. Journal of Cellular Biochemistry, 119: 8035-8047. DOI: 10.1002/jcb.26722
Zanu H, Kheravii S, Morgan N, Bedford M & Swick R. 2020. Interactive effect of dietary calcium and phytase on broilers challenged with subclinical necrotic enteritis: 3. Serum calcium and phosphorus, and bone mineralization. Poultry Science, 99: 3617-3627. DOI: 10.1016/j.psj.2020.04.012
Poultry Science Journal
Volume 10, Issue 2
September 2022
Pages 169-183

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