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http://dx.doi.org/10.5713/ab.21.0301

Effects of maternal dietary energy restriction on laying performance, embryonic development, and lipid metabolism in broilers  

Sun, Hao (College of Animal Science and Technology, Northeast Agricultural University)
Chen, Zhihui (College of Animal Science and Technology, Northeast Agricultural University)
Ma, Chengzhan (College of Animal Science and Technology, Northeast Agricultural University)
Lian, Lina (College of Animal Science and Technology, Northeast Agricultural University)
Zhao, Zeyu (College of Animal Science and Technology, Northeast Agricultural University)
Niu, Shupeng (College of Animal Science and Technology, Northeast Agricultural University)
Xu, Liangmei (College of Animal Science and Technology, Northeast Agricultural University)
Sun, Jinhua (College of Animal Science and Technology, Northeast Agricultural University)
Publication Information
Animal Bioscience / v.35, no.5, 2022 , pp. 698-710 More about this Journal
Abstract
Objective: The objective of this study was to investigate the effects of different degrees of maternal dietary energy restriction on lipid deposition in embryonic tissues during the medium laying period (37 to 39 weeks) in Arbor Acres (AA) broiler breeders. Methods: A single factor design was adopted, and 400 AA broiler breeders (20 weeks of age) with a similar weight were randomly allocated into four groups. The birds in the control group were fed a corn-soybean meal based diet, and those in trial groups were fed diets with 80%, 70%, and 50% energy levels of the basal diet. Incubated eggs from the medium laying period were collected. Samples of developing embryos at various stages were prepared for composition analysis. Results: The embryo weight in the 80% energy group was higher than those of the other groups on embryonic day (E) 13, but at 21 E, they were significantly decreased with decreasing energy intake of the broiler breeders (p<0.05). Additionally, the levels of crude fat in tissues in the restriction groups were significantly decreased (p<0.05). The long axis and area of adipocytes in breast muscle, thigh muscle and the liver were significantly decreased (p<0.05) at 21 E in the 80%, 70%, and 50% energy groups. Conclusion: The effects of the 80% maternal dietary energy restriction energy affects egg production performance, egg quality, and nutrient deposition in egg weights, which then directly impacts on the developmental process of embryos, especially on fat utilization and deposition.
Keywords
Broiler Breeder; Embryo; Energy Restriction; Lipid Deposition; Lipoprotein Lipase;
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1 Wilson HR. Effects of maternal nutrition on hatchability. Poult Sci 1997;76:134-43. https://doi.org/10.1093/ps/76.1.134   DOI
2 Shafer DJ, Carey JB, Prochaska JF. Effect of dietary methionine intake on egg component yield and composition. Poult Sci 1996;75:1080-5. https://doi.org/10.3382/ps.0751080   DOI
3 Alheiroslira MC, Araujo LL, Trindade NGV, et al. Short-and long-term effects of a maternal low-energy diet ad libitum during gestation and/or lactation on physiological parameters of mothers and male offspring. Eur J Nutr 2015;54:793-802. https://doi.org/10.1007/s00394-014-0758-0   DOI
4 Sudano MJ, Rascado TDS, Tata A, et al. Lipidome signatures in early bovine embryo development. Theriogenology 2016;86:472-84.e1. https://doi.org/10.1016/j.theriogenology.2016.03.025   DOI
5 Cooper MK, Wassif CA, Kraabowiak PA. A defective response to hedgehog signaling in disorders of cholesterol biosynthesis. Nat Genet 2003;33:508-13. https://doi.org/10.1038/ng1134   DOI
6 Akinmoladun OF, Onibi GE, Babalola KO, Lomuwagun AT, Fabode AF. Growth performance, hematology and carcass characteristics of broiler chicks fed diets with varying energy levels. J Exp Agric Int 2016;10:1-6. https://doi.org/10.9734/AJEA/2016/13931   DOI
7 Tarugi P, Reggiani D, Ottaviani E, Ferrari S, Tiozzo R, Calandra S. Plasma lipoproteins, tissue cholesterol overload, and skeletal muscle apolipoprotein A-I synthesis in the developing chick. J Lipid Res 1989;30:9-22. https://doi.org/10.1016/S0022-2275(20)38391-7   DOI
8 Sato M, Tachibana T, Furuse M. Total lipid and triacylglycerol contents in the liver of broiler and layer chickens at embryonic stages and hatching. Anim Sci J 2006;77:526-31. https://doi.org/10.1111/j.1740-0929.2006.00381.x   DOI
9 Li F, Xu LM, Shan AS, Hu JW, Zhang YY, Li YH. Effect of daily feed intake in laying period on laying performance, egg quality and egg composition of genetically fat and lean lines of chickens. Br Poult Sci 2011;52:163-8. https://doi.org/10.1080/00071668.2011.559455   DOI
10 Li F, Shan AS, Hu JW, Zheng YB, Xu LM, Chen ZH. Changes to daily feed intake during the laying period alters embryonic mstn and myog gene expression in genetically fat and lean lines of chickens. Br Poult Sci 2013;54:728-37. https://doi.org/10.1080/00071668.2013.853868   DOI
11 Niu S, Xu LM, Zhang H, Lu L, Lv RC, Tian B. Effects of maternal dietary energy level on lipid metabolism related indexes in embryonic yolk and serum during the middle laying period in broiler breeders. Chinese J Anim Nutr 2013;25:50-8. https://doi.org/10.3969/j.issn.1006-267x.2013.01.008   DOI
12 Che L, Yang Z, Xu M, et al. Dietary energy intake affects fetal survival and development during early and middle pregnancy in large white and meishan gilts. Anim Nutr 2015;1:152-9. https://doi.org/10.1016/j.aninu.2015.08.009   DOI
13 Belknap WM, Dietschy JM. Sterol synthesis and low density lipoprotein clearance in vivo in the pregnant rat, placenta, and fetus. sources for tissue cholesterol during fetal development. J Clin Invest 1988;82:2077-85. https://doi.org/10.1172/jci113829   DOI
14 Cha MC, Jones PJ. Dietary fat type related changes in tissue cholesterol and fatty acid synthesis are influenced by energy intake level in rats. J Am Coll Nutr 1997;16:592-9. https://doi.org/10.1080/07315724.1997.10718724   DOI
15 Jiang Z, Cherian G, Robinson FE, Sim JS. Effect of feeding cholesterol to laying hens and chicks on cholesterol metabolism in pre- and posthatch chicks. Poult Sci 1990;69:1694-701. https://doi.org/10.3382/ps.0691694   DOI
16 van der Waaij EH, van den Brand H, van Arendonk JAM, Kemp B. Effect of match or mismatch of maternal-offspring nutritional environment on the development of offspring in broiler chickens. Animal 2011;5:741-8. https://doi.org/10.1017/S1751731110002387   DOI
17 Sunder GS, Kumar CV, Panda AK, Rao SVR, Raju MVLN Rao SVR, Raju MVLN. Influence of energy restriction and pre-incubation holding period of eggs on fertility and hatch-ability in aged broiler breeders. Asian-Australas J Anim Sci 2010;23:240-5. https://doi.org/10.5713/ajas.2010.90435   DOI
18 Bouvarel I, Nys Y, Panheleux M, Lescoat P. How diet influences the quality of eggs. INRA Productions Animales 2010;23:167-81.
19 Yuan K, Wu GB, Bryant MM, Roland DAS. Effect of molting method and dietary energy on postmolt performance, egg components, egg solid, and egg quality in bovans white and dekalb white hens during second cycle phases two and three. Poult Sci 2007;86:869-76. https://doi.org/10.1093/ps/86.5.869   DOI
20 Tian B, Huang F, Xu L, Li Z, Li J, Li S. Dietary energy level affects laying performance, egg quality and egg component of broiler breeders during the early laying period. Chin J Anim Nutr 2012;24:327-33. https://doi.org/10.3969/j.issn.1006-267x.2012.02.020   DOI
21 Noble RC, Cocchi M. Lipid metabolism and the neonatal chicken. Progress in lipid research. Prog Lipid Res 1990;29:107-40. https://doi.org/10.1016/0163-7827(90)90014-c   DOI
22 Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006;443:651-7. https://doi.org/10.1038/nature05185   DOI
23 Ashino NG, Saito KN, Souza FD, et al. Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem 2012;23:341-8. https://doi.org/10.1016/j.jnutbio.2010.12.011   DOI
24 Yoshida S, Wada Y. Transfer of maternal cholesterol to embryo and fetus in pregnant mice. J Lipid Res 2005;46:2168-74. https://doi.org/10.1194/jlr.m500096-jlr200   DOI
25 Woollett LA. Maternal cholesterol in fetal development: transport of cholesterol from the maternal to the fetal circulation. Am J Clin Nutr 2005;82:1155-61. https://doi.org/10.1093/ajcn/82.6.1155   DOI
26 Kiiskinen T, Helander E. Effects of restricted methionine and energy intake on egg weight and shell quality. Agric Food Sci Finland 2015;7:513-21. https://doi.org/10.23986/afsci.5615   DOI
27 Feng L, Yang X, Yang Y, et al. Maternal energy restriction by low starch or fat affects carcase trait, meat quality and muscle antioxidative properties in Arbor Acres broilers. Ital J Anim Sci 2019;18:1419-30. https://doi.org/10.1080/1828051X.2019.1679044   DOI
28 Li JF, Xu LM, Zhang YY, et al. Effects of maternal dietary energy restriction on fat deposition of offspring. J Northeast Agric Univ 2014;21:46-52. https://doi.org/10.1016/S1006-8104(14)60033-7   DOI
29 Li F, Mou SY, Liu Y, et al. Maternal dietary energy levels affected the lipid deposition of offspring embryos at the end of the laying period of broiler breeder hens. Ital J Anim Sci 2018;17:180-3. https://doi.org/10.1080/1828051X.2017.1345665   DOI
30 Enting H, Boersma WJA, Cornelissen JBWJ, Winden SCLV, Verstegen MWA, van der Aar PJ. The effect of low-density broiler breeder diets on performance and immune status of their offspring. Poult Sci 2007;86:282-90. https://doi.org/10.1093/ps/86.2.282   DOI
31 Blamberg DL, Bossard EH, Combs GF. Influence of energy intake on egg weight with dietsvarying in fat content and physical form. Poult Sci 1964;43:1304.
32 Peebles ED, Zumwalt CD, Doyle SM, et al. Effects of breeder age and dietary fat source and level on broiler hatching egg characteristics. Poult Sci 2000;79:698-704. https://doi.org/10.1093/ps/79.5.698   DOI
33 Xu M, Che L, Yang Z, et al. Effect of high fat dietary intake during maternal gestation on offspring ovarian health in a pig model. Nutrients 2016;8:498. https://doi.org/10.3390/nu8080498   DOI
34 Gardner FA, Young LL. The influence of dietary protein and energy levels on the protein and lipid content of the hen's egg. Poult Sci 1972;51:994-7. https://doi.org/10.3382/ps.0510994   DOI
35 West E, Mary J. Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B Mol Dev Evol 2005;304:610-8. https://doi.org/10.1002/jez.b.21071   DOI
36 Bhattacharya A, Sun D, Rahman M, Fernandes G. Different ratios of eicosapentaenoic and docosahexaenoic omega-3 fatty acids in commercial fish oils differentially alter proinflammatory cytokines in peritoneal macrophages from C57BL/6 female mice. J Nutr Biochem 2007;18:23-30. https://doi.org/10.1016/j.jnutbio.2006.02.005   DOI
37 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262   DOI
38 Zhong C, Nakaue HS, Hu CY, Mirosh LW. Effect of full feed and early feed restriction on broiler performance, abdominal fat level, cellularity, and fat metabolism in broiler chickens. Poult Sci 1995;74:1636-43. https://doi.org/10.3382/ps.0741636   DOI
39 Kurnick AA, Hinds HB, Pasvogel MW, Reid BL. Dietary energy levels for laying hens as related to age and environmental temperatures: 1. Effect on egg production, body weight and feed conversion. Poult Sci 1961;40:1483-91. https://doi.org/10.3382/ps.0401483   DOI
40 Newcombe M, March BE. Effects of energy source and feed access on abdominal adipose tissue in chickens of two broiler strains. Poult Sci 1988;67:766-77. https://doi.org/10.3382/ps.0670766   DOI
41 Garcia-Pelaez B, Vila R, Remesar X. Treatment of pregnant rats with oleoyl-estrone slows down pup fat deposition after weaning. Reprod Biol Endocrinol 2008;6:23. https://doi.org/10.1186/1477-7827-6-23   DOI
42 Olivecrona G. Role of lipoprotein lipase in lipid metabolism. Curr Opin Lipidol 2016;27:233-41. https://doi.org/10.1097/mol.0000000000000297   DOI
43 Zhao S, Ma H, Zou S, Chen W, Zhao R. Hepatic lipogenesis in broiler chickens with different fat deposition during embryonic development. J Vet Med 2007;54:1-6. https://doi.org/10.1111/j.1439-0442.2007.00898.x   DOI
44 Bergo M, Olivecrona G, Olivecrona T. Diurnal rhythms and effects of fasting and refeeding on rat adipose tissue lipoprotein lipase. Am J Physiol Endocrinol Metab 1996;271:E1092-7. https://doi.org/10.1152/ajpendo.1996.271.6.e1092   DOI