Avian Liver: The Forgotten Organ

Animals - Tập 9 Số 2 - Trang 63
F. Zaefarian1, M.R. Abdollahi1, A.J. Cowieson2, V. Ravindran1
1Monogastric Research Centre, School of Agriculture and Environment, Massey University, Private Bag 11 222, Palmerston North, 4442, New Zealand
2DSM Nutritional Products, Wurmisweg 576, CH-4303 Kaiseraugst, Switzerland

Tóm tắt

Despite having huge responsibilities in avian species, published reports on the influence of dietary factors and other possible constraints on the size, development and function of liver are limited. Consideration of the factors that could influence and alter liver function is therefore of critical relevance. In the current review, aspects of liver structure and function, and the influence of feed restriction, anti-nutritional factors, structural components and feed additives on liver are discussed. Effects of feed technology techniques such as thermal treatment and pelleting, feed particle size and whole grain feeding on the liver are also reviewed. A discussion of lipogenesis and lipid storage in poultry is presented to provide a better understanding and to differentiate the normal pathways of lipid metabolism from abnormal (i.e., disordered) pathways. The liver is the main site of fat synthesis in poultry, but under certain conditions, excessive fat can accumulate in the liver and cause problems. Factors contributing to the fatty liver syndrome are also examined.

Từ khóa


Tài liệu tham khảo

Whittow, G.C. (2000). Gastrointestinal anatomy and physiology. Sturkie’s Avian Physiology, Academic Press. [5th ed.].

Lucas, 1956, Morphology of the chicken liver, Poult. Sci., 35, 793, 10.3382/ps.0350793

Kmiec, 2001, Cooperation of liver cells in health and disease, Adv. Anat. Embryol. Cell Biol., 161, 1

Turk, 1982, The anatomy of the avian digestive tract as related to feed utilization, Poult. Sci. J., 60, 101

Akers, R.M., and Denbow, D.M. (2013). Digestive System. Anatomy and Physiology of Domestic Animals, John Wiley & Sons, Inc.. [2nd ed.]. Chapter 17.

Gordillo, 2015, Orchestrating liver development, Development, 142, 2094, 10.1242/dev.114215

Lumeij, J.T. (1994). Hepatology. Avian Medicine: Principles and Application, Wingers Publishing, Inc.

Bowes, 1988, Organ weights of normal broiler chickens and those dying of sudden death syndrome, Can. Vet. J., 29, 153

Nir, 1993, Comparative growth and development of the digestive organs and of some enzymes in broiler and egg type chicks after hatching, Br. Poult. Sci., 34, 523, 10.1080/00071669308417607

Ravindran, 2006, Influence of whole wheat feeding on the development of gastrointestinal tract and performance of broiler chickens, Aust. J. Agric. Res., 57, 21, 10.1071/AR05098

Hermier, 1997, Lipoprotein metabolism and fattening in poultry, J. Nutr., 127, 805s, 10.1093/jn/127.5.805S

Tancharoenrat, 2014, Digestion of fat and fatty acids along the gastrointestinal tract of broiler chickens, Poult. Sci., 93, 371, 10.3382/ps.2013-03344

Bensadoun, 1972, The form of absorption of lipids in the chicken, Gallus domesticus, Proc. Soc. Exp. Biol. Med., 141, 814, 10.3181/00379727-141-36878

Griffin, 1982, Hydrolysis of plasma triacylglycerol-rich lipoproteins from immature and laying hens (Gallus domesticus) by lipoprotein lipase in vitro, Biochem. J., 206, 647, 10.1042/bj2060647

Cherian, 2002, Dietary CLA alters yolk and tissue FA composition and hepatic histopathology of laying hens, Lipids, 37, 751, 10.1007/s11745-002-0957-4

Scott, M.L., Nesheim, M.C., and Young, R.J. (1982). Nutrition of the Chicken, M.L. Scott and Associates. [3rd ed.].

Koeppen, B.M., and Stanton, B.A. (2008). Berne and Levy Physiology, Mosby Elsevier. [6th ed.].

Scanes, C.G. (2015). Gastrointestinal anatomy and physiology. Sturkie’s Avian Physiology, Academic Press. [6th ed.].

Hurwitz, 1973, Absorption and secretion of fatty acids and bile acids in the intestine of the laying fowl, J. Nutr., 103, 543, 10.1093/jn/103.4.543

Sklan, 1973, Lipid absorption and secretion in the chick: Effect of raw soybean meal, J. Nutr., 103, 1299, 10.1093/jn/103.9.1299

Sklan, 1975, Fat digestion and absorption in chicks fed raw or heated soybean meal, J. Nutr., 105, 57, 10.1093/jn/105.1.57

Lavrenteva, 1963, Bile secretion in Chicken, Tru. Gor’ko. Sel’skokhoz. Inst., 13, 80

Andrews, 1975, Bile secretion in anesthetized Adelie penguin (Pygoscelis adeliae), J. Physiol., 246, 76P

Sturkie, P.D. (1986). Alimentary canal: Secretion and digestion, special digestive functions, and absorption. Avian Physiology, Springer.

Reece, W.O. (2004). Secretions of stomach and accessory glands. Dukes Physiology of Domestic Animals, Cornell University Press. [12th ed.].

Lisbona, 1981, Basal Biliary secretion in conscious chicken and role of enterohepatic circulation, Comp. Biochem. Physiol., 69A, 341, 10.1016/0300-9629(81)90305-4

Haslewood, G.A.D. (1978). The Biological Importance of Bile Salts, North-Holland. North-Holland research monographs.

Krogdahl, 1985, Digestion and absorption of lipid in poultry, J. Nutr., 115, 675, 10.1093/jn/115.5.675

Chen, 1975, Kinetic studies in bile acid micelles, J. Am. Chem. Soc., 97, 2052, 10.1021/ja00841a010

Lindsay, 1967, Intestinal absorption of bile salts in the cockerel, Poult. Sci., 46, 164, 10.3382/ps.0460164

Lin, 1974, Bilirubin and biliverdin excretion by the chicken, Am. J. Physiol., 226, 881, 10.1152/ajplegacy.1974.226.4.881

Bell, 1983, Physiology of digestive tract, Physiology and Biochemistry of Domestic Fowl, Volume 4, 31

Elkin, 1990, Biliary bile acid profiles of domestic fowl as determined by high performance liquid chromatography and fast atom bombardment mass spectrometry, Comp. Biochem. Physiol. B, 96, 157, 10.1016/0305-0491(90)90356-X

Yeh, 2001, High-performance liquid chromatographic determination for bile components in fish, chicken and duck, J. Chromatogr. B, 751, 1, 10.1016/S0378-4347(00)00448-5

Serafin, 1970, Influence of dietary heat-labile factors in soybean meal upon bile acid pools and turnover in the chick, J. Nutr., 100, 786, 10.1093/jn/100.7.786

Klasing, K.C. (1998). Nutritional strategies and adaptations. Comparative Avian Nutrition, CAB International.

Richards, 2003, Feed Restriction Significantly Alters Lipogenic Gene Expression in Broiler Breeder Chickens, J. Nutr., 133, 707, 10.1093/jn/133.3.707

Walzem, 1994, Overfeeding increases very low-density lipoprotein diameter and causes the appearance of a unique lipoprotein particle in association with failed yolk deposition, J. Lipid Res., 35, 1354, 10.1016/S0022-2275(20)40077-X

Alvarenga, 2011, Lipoprotein metabolism in poultry, World’s Poult. Sci. J., 67, 431, 10.1017/S0043933911000481

Speake, 1998, Transport and transformations of yolk lipids during development of the avian embryo, Prog. Lipid Res., 37, 1, 10.1016/S0163-7827(97)00012-X

Griffin, H., and Hermier, D. (1988). Plasma lipoprotein metabolism and fattening in poultry. Leanness in Domestic Birds, Butterworths.

Howard, 1982, Synthesis, processing, and secretion of apolipoprotein B by the chick liver cell, J. Biol. Chem., 257, 4292, 10.1016/S0021-9258(18)34720-3

Tarlow, 1977, Lipogenesis and the synthesis and secretion of very low-density lipoprotein by avian liver cells in nonproliferating monolayer culture. Hormonal effects, J. Cell Biol., 73, 332, 10.1083/jcb.73.2.332

Freeman, 1969, The mobilisation of hepatic glycogen in Gallus domesticus at the end of incubation, Comp. Biochem. Physiol., 28, 1169, 10.1016/0010-406X(69)90557-X

Goodridge, 1986, Metabolism of glucose-U-14C in vitro in adipose tissue from embryonic and growing chicks, Am. J. Physiol., 214, 897, 10.1152/ajplegacy.1968.214.4.897

Chin, 1987, Quantitation of renal uric acid synthesis in the chicken, Am. J. Physiol., 234, F446

Campbell, T.W. (1995). Avian Hematology and Cytology, Iowa State University Press. [2nd ed.].

Pang, P.K.T., and Schreibman, M.P. (1989). Phylogenetic and evolutionary aspects of vitamin D from phytoplankton to humans. Vertebrate Endocrinology: Fundamentals and Biomedical Implications, Academic Press, Inc. (Harcourt Brace Jovanovich).

Konig, 2008, Effects of fish oil and conjugated linoleic acids on expression of target genes of PPARα and sterol regulatory element-binding proteins in the liver of laying hens, Br. J. Nutr., 100, 355, 10.1017/S0007114507883024

Royan, 2011, Effects of conjugated linoleic acid, fish oil and soybean oil on PPARs (α & γ) mRNA expression in broiler chickens and their relation to body fat deposits, Int. J. Mol. Sci., 12, 8581, 10.3390/ijms12128581

Campioli, 2012, n-3 dietary supplementation and lipid metabolism: Differences between vegetable- and fish-derived oils, J. Funct. Foods, 4, 207, 10.1016/j.jff.2011.10.006

Huang, 2005, Dietary lipid level influences fatty acid profiles, tissue composition, and lipid peroxidation of soft-shelled turtle, Pelodiscus sinensis, Comp. Biochem. Physiol. A Mol. Integr. Physiol., 142, 383, 10.1016/j.cbpa.2005.09.004

Senkoylu, 2006, Nutritional evaluation of a high-oil sunflower meal in broiler starter diets, J. Appl. Poult. Res., 15, 40, 10.1093/japr/15.1.40

Smink, 2010, Effect of dietary fat sources on fatty acid deposition and lipid metabolism in broiler chickens, Poult. Sci., 89, 2432, 10.3382/ps.2010-00665

Pinchasov, 1992, Effect of dietary polyunsaturated fatty acid concentration on performance, fat deposition, and carcass fatty acid composition in broiler chickens, Poult. Sci., 71, 1504, 10.3382/ps.0711504

Ferrell, 1988, Contribution of visceral organs to animal energy expenditures, J. Anim. Sci., 66, 23

Pearson, 1983, Biochemical changes in layer and broiler chickens when fed on a high-glucosinolate rapeseed meal, Br. Poult. Sci., 24, 417, 10.1080/00071668308416756

Milligan, L.P., Grovum, W.L., and Dobson, A. (1986). Splanchnic metabolism of glucose and related energy substrates. Control of Digestion and Metabolism in Ruminants, Prentice-Hall.

Knight, 1998, Nutritional programming in hatchling poultry: Why a good start is important, Poult. Dig., 57, 20

Canas, 1982, Maintenance energy requirements during lactation in rats, J. Nutr., 112, 1876, 10.1093/jn/112.10.1876

Lacy, 1985, Effect of intrahepatic glucose infusion on feeding in heavy and light breed chicks, Poult. Sci., 64, 751, 10.3382/ps.0640751

Lacy, 1986, Food intake in the domestic fowl: Effect of intrahepatic lipid and amino acid infusions, Physiol. Behav., 36, 533, 10.1016/0031-9384(86)90327-6

Bartov, 1989, Lack of interactive effect of nicarbazin and dietary energy-to-protein ratio on performance and abdominal fat pad weight of broiler chicks, Poult. Sci., 68, 1535, 10.3382/ps.0681535

Bartov, I. (1992, January 19–24). Effect of feed withdrawal on yield, fat content and fatty acid composition of various tissues in broilers. Proceedings of the XIX World’s Poultry Congress, Amsterdam, The Netherlands.

Bartov, 1996, Inter-relationship between the effects of dietary factors and feed withdrawal on the content and composition of liver fat in broiler chicks, Poult. Sci., 75, 632, 10.3382/ps.0750632

Wiseman, J. (1984). Fat deposition in broilers. Fats in Animal Nutrition, Butterworths.

Imaizumi, 1972, Nutritional regulation of lipid metabolism in rats. Part I. The effect of overnight fasting on the concentration and composition of liver and its microsomal lipids, Agric. Biol. Chem., 36, 234

Leveille, 1975, Lipid biosynthesis in the chick. A consideration of site of synthesis, influence of diet and possible regulatory mechanisms, Poult. Sci., 54, 1075, 10.3382/ps.0541075

Leveille, 1963, Fatty acid composition of plasma and liver lipid components as influenced by diet in the growing chick, J. Nutr., 81, 357

Fujii, 1985, Fatty acid compositions of triacylglycerols and phospholipids in hen liver lipids before and after sexual maturity, Poult. Sci., 64, 1371, 10.3382/ps.0641371

Shapira, 1979, Effects of isocaloric supplements of glucose or soyabean oil on lipids in tissues and plasma lipoproteins of starved and overfed chicks, Nutr. Metab., 23, 368, 10.1159/000176282

Rosebrough, 1986, Effect of early feed restriction in broilers. II. Lipid metabolism, Growth, 50, 217

Fontana, 1993, Early feed restriction of broilers: Effects on abdominal fat pad, liver, and gizzard weights, fat deposition and carcass composition, Poult. Sci., 72, 243, 10.3382/ps.0720243

Hocking, 1996, Relationship between the degree of food restriction and welfare indices in broiler breeder females, Br. Poult. Sci., 37, 263, 10.1080/00071669608417858

Hocking, 1993, Welfare assessment of broiler breeder and layer females subjected to food restriction and limited access to water during rearing, Br. Poult. Sci., 34, 443, 10.1080/00071669308417600

Zubair, 1994, Effect of early feed restriction and realimentation on heat production and changes in sizes of digestive organs of male broilers, Poult. Sci., 73, 529, 10.3382/ps.0730529

Susbilla, 1994, Weight of internal organs and carcass yield of early food restricted broilers, Br. Poult. Sci., 35, 677, 10.1080/00071669408417734

Liener, I.E. (1980). Toxic Constituents of Plant Foodstuffs, Academic Press.

Ortiz, 1994, Effects of faba bean tannins on the growth and histological structure of the intestinal tract and liver of chicks and rats, Br. J. Nutr., 35, 743

Emiola, 2007, Performance and histological responses of internal organs of broiler chicken fed raw, dehulled, and aqueous and dry-heated kidney bean meals, Poult. Sci., 86, 1234, 10.1093/ps/86.6.1234

Eisenberg, 1963, Biosynthesis of inositol in rat testis homogenate, Biochem. Biophys. Res. Commun., 12, 72, 10.1016/0006-291X(63)90416-9

Lee, 2016, Inositol—An effective growth promotor?, World’s Poult. Sci. J., 72, 743, 10.1017/S0043933916000660

Hayashi, 1974, The effect of myo-inositol deficiency on lipid metabolism in rats. II. The mechanism of triacylglycerol accumulation in the liver of myo-inositol deficient rats, Biochim. Biophys. Acta, 360, 146, 10.1016/0005-2760(74)90164-7

Croze, 2013, Potential role and therapeutic interests of myoinositol in metabolic diseases, Biochimie, 95, 1811, 10.1016/j.biochi.2013.05.011

Croze, 2015, Abnormalities in myo-inositol metabolism associated with type 2 diabetes in mice fed a high-fat diet: Benefits of a dietary myo-inositol supplementation, Br. J. Nutr., 113, 1862, 10.1017/S000711451500121X

Liu, 2010, Effect of dietary sodium phytate and microbial phytase on the lipase activity and lipid metabolism of broiler chickens, B. J. Nutr., 103, 862, 10.1017/S0007114509992558

Katayama, 1995, Effect of Dietary Sodium Phytate on the Hepatic and Serum Levels of Lipids and on the Hepatic Activities of NADPH-generating Enzymes in Rats Fed on Sucrose, Biosci. Biotechnol. Biochem., 59, 1159, 10.1271/bbb.59.1159

Viveros, 2002, Effects of microbial phytase supplementation on mineral utilization and serum enzyme activities in broiler chicks fed different levels of phosphorus, Poult. Sci., 81, 1172, 10.1093/ps/81.8.1172

Karadas, 2005, The effects of dietary phytase activity on the concentration of Coenzyme Q10 in the liver of young turkeys and broilers, Br. Poult. Abstr., 1, 1, 10.1080/00071660500068882

Karadas, 2010, Effects of different dietary phytase activities on the concentration of antioxidants in the liver of growing broilers, J. Anim. Physio. Anim. Nutr., 94, 519

Sharma, 2016, Performance, litter quality and gaseous odour emissions of broilers fed phytase supplemented diets, Anim. Nutr., 2, 288, 10.1016/j.aninu.2016.10.003

2010, Comparison of gastrointestinal transit times between chickens from D+ and D− genetic lines selected for divergent digestion efficiency, Animal, 4, 1861, 10.1017/S1751731110001266

Mateos, 2002, The feasibility of using nutritional modifications to replace drugs in poultry feeds, J. Appl. Poult. Res., 11, 437, 10.1093/japr/11.4.437

Mateos, 2012, Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics, J. Appl. Poult. Res., 21, 156, 10.3382/japr.2011-00477

Hetland, 2003, Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat, Br. Poult. Sci., 44, 275, 10.1080/0007166031000124595

Hetland, 2005, Role of insoluble fiber on gizzard activity in layers, J. Appl. Poult. Res., 14, 38, 10.1093/japr/14.1.38

Amerah, 2007, Influence of feed particle size on the performance, energy utilization, digestive tract development and digestive parameter of broiler starters, Poult. Sci., 86, 2615, 10.3382/ps.2007-00212

Mateos, 2010, Effect of inclusion of oat hulls and sugar beet pulp in the diet on productive performance and digestive traits of broilers from 1 to 42 days of age, Anim. Feed Sci. Technol., 162, 37, 10.1016/j.anifeedsci.2010.08.010

Svihus, 2011, Limitation to wheat starch digestion in growing broiler chickens: A brief review, Anim. Prod. Sci., 51, 583, 10.1071/AN10271

Akiba, 1982, The role of dietary fibers on hepatic lipid metabolism in chicks, Nutr. Rep. Int., 26, 223

Akiba, 1978, Effects of force-feeding and dietary cellulose on liver lipid accumulation and lipid composition of liver and plasma in growing chicks, J. Nutr., 108, 739, 10.1093/jn/108.5.739

Woyengo, 2011, Growth performance, organ weights, and blood parameters of broilers fed diets containing expeller-extracted canola meal, Poult. Sci., 90, 2520, 10.3382/ps.2011-01436

Parke, 1981, The role of nutrition in toxicology, Annu. Rev. Nutr., 1, 207, 10.1146/annurev.nu.01.070181.001231

Bauman, 1988, The effect of dietary protein and sulfur amino acids on hepatic glutathione concentration and glutathione-dependent enzyme activities in the rat, Can. J. Physiol. Pharmacol., 66, 1048, 10.1139/y88-171

Mossami, A. (2011). Effects of Different Inclusions of Oat Hulls on Performance, Carcass Yield and Gut Development in Broiler Chickens. [Master’s Thesis, Swedish University of Agricultural Science].

Zhu, 2014, Effects of enzyme supplementation on performance and digestive parameters of broilers fed corn-soybean diets, Poult. Sci., 93, 1704, 10.3382/ps.2013-03626

Dworkin, 1976, Small intestinal mass of the rat is partially determined by indirect effects on intraluminal nutrition, Gastroenterology, 71, 626, 10.1016/S0016-5085(76)80554-9

Wang, 2005, Effects of enzyme supplementation on performance, nutrient digestibility, gastrointestinal morphology, and volatile fatty acid profiles in the hindgut of broilers fed wheat-based diets, Poult. Sci., 84, 875, 10.1093/ps/84.6.875

Brenes, 1993, Effect of enzyme supplementation on the performance and digestive tract size of broiler chickens fed wheat- and barley-based diets, Poult. Sci., 72, 1731, 10.3382/ps.0721731

Wu, 2004, Influence of whole wheat inclusion and xylanase supplementation on the performance, digestive tract measurements and carcass characteristics of broiler chickens, Anim. Feed Sci. Technol., 116, 129, 10.1016/j.anifeedsci.2004.02.011

Latorre, 2004, Feeding regimen and enzyme supplementationto rye-based diets for broilers, Poult. Sci., 83, 152, 10.1093/ps/83.2.152

Rutkowski, 2006, The effect of β-glucanase supplementation of barley- and oat-based diets on growth performance and fermentation in broiler chicken gastrointestinal tract, Br. Poult. Sci., 47, 57, 10.1080/00071660500475145

Sayyazadeh, 2006, Influence of enzyme supplementation of maize, wheat and barley-based diets on the performance of broiler chickens, Pak. J. Biol. Sci., 9, 616, 10.3923/pjbs.2006.616.621

Leeson, 2000, Effect of dietary lipase enzyme on gut morphology, gastric motility, and long-term performance of broiler chicks, Poult. Sci., 79, 956, 10.1093/ps/79.7.956

Emadinia, 2014, Effect of wet feeding and enzyme supplementation on performance and immune responses of broiler chicks, J. Appl. Anim. Res., 42, 32, 10.1080/09712119.2013.795901

Parsaie, 2007, Influence of wheat-based diets supplemented with xylanase, bile acid and antibiotics on performance, digestive tract measurements and gut morphology of broilers compared with a maize-based diet, Br. Poult. Sci., 48, 594, 10.1080/00071660701615788

Rutkowski, 2007, Effects of dietary inclusion of triticale, rye and wheat and xylanase supplementation on growth performance of broiler chickens and fermentation in the gastrointestinal tract, Anim. Feed Sci. Technol., 132, 79, 10.1016/j.anifeedsci.2006.03.011

Iji, 2001, Intestinal structure and function of broiler chickens on diets supplemented with a mannan oligosaccharide, J. Sci. Food Agric., 81, 1186, 10.1002/jsfa.925

Abdollahi, 2011, Influence of feed form and conditioning temperature on performance, apparent metabolisable energy and ileal digestibility of starch and nitrogen in broiler starters fed wheat-based diet, Anim. Feed Sci. Technol., 168, 88, 10.1016/j.anifeedsci.2011.03.014

Abdollahi, 2013, Influence of pellet diameter and length on the quality of pellets and, performance, nutrient utilisation and digestive tract development of broilers fed wheat-based diets, Br. Poult. Sci., 54, 337

Abdollahi, 2013, The effect of manipulation of pellet size (diameter and length) on pellet quality and performance, apparent metabolisable energy and ileal nutrient digestibility in broilers fed maize-based diets, Anim. Prod. Sci., 53, 114, 10.1071/AN12166

Abdollahi, 2014, Influence of feed form on growth performance, ileal nutrient digestibility, and energy utilisation in broiler starters fed a sorghum-based diet, Livest. Sci., 165, 80, 10.1016/j.livsci.2014.04.002

Selle, 2014, Steam-pelleting temperatures and grain variety of finely-ground, sorghum-based broiler diets. I. Influence on growth performance, relative gizzard weights, nutrient utilisation, starch and nitrogen digestibility, Anim. Prod. Sci., 54, 339, 10.1071/AN13080

Marks, 1984, The roles of protein level and diet form in water consumption and abdominal fat pad deposition of broilers, Poult. Sci., 63, 1617, 10.3382/ps.0631617

Plavnik, 1989, Effect of dietary protein, energy, and feed pelleting on the response of chicks to early feed restriction, Poult. Sci., 68, 1118, 10.3382/ps.0681118

Rezaeipour, 2014, Effects of feed form and feed particle size with dietary L-threonine supplementation on performance, carcass characteristics and blood biochemical parameters of broiler chickens, J. Anim. Sci. Technol., 56, 20, 10.1186/2055-0391-56-20

Mannion, 1997, The effect of steam and cold pelleting of four grain legumes at different inclusion levels in broiler starter diets, Proc. Aust. Poult. Sci., 9, 133

Preston, 2000, Effect of diet form and enzyme supplementation on growth, efficiency and energy utilisation of wheat-based diets for broilers, Br. Poult. Sci., 41, 324, 10.1080/713654933

Scott, 2002, Evaluation of lighting programs, diet density, and short-term use of mash as compared to crumbled starter to reduce incidence of sudden death syndrome in broiler chicks to 35 days of age, Can. J. Anim. Sci., 82, 375, 10.4141/A01-067

Mateos, 2007, Effects of cereal, heat processing, and fiber on productive performance and digestive traits of broilers, Poult. Sci., 86, 1705, 10.1093/ps/86.8.1705

Mirghelenj, 2009, Effects of feed form on development of digestive tract, performance and carcass traits of broiler chickens, J. Anim. Vet. Adv., 8, 1911

Ghobadi, 2012, Effect of feed processing and enzyme supplementation of wheat-based diets on performance of broiler chicks, J. Appl. Anim. Res., 40, 260, 10.1080/09712119.2012.672307

Naderinejad, 2016, Influence of feed form and particle size on performance, nutrient utilisation, and gastro intestinal tract development and morphometry in broiler starters fed maize-based diets, Anim. Feed Sci. Technol., 215, 92, 10.1016/j.anifeedsci.2016.02.012

Benedetti, 2011, Corn texture and particle size in broiler diets, Rev. Bras. Cienc. Avic., 13, 227, 10.1590/S1516-635X2011000400002

Favero, 2009, Influence of feed form and corn particle size on the live performance and digestive tract development of turkeys, J. Appl. Poult. Res., 18, 772, 10.3382/japr.2009-00069

Singh, 2014, Whole grain feeding: Methodologies and effects on performance, digestive tract development and nutrient utilisation of poultry, Anim. Feed Sci. Technol., 190, 1, 10.1016/j.anifeedsci.2014.01.010

Nahas, 2001, Effects of feeding locally grown whole barley with or without enzyme addition and whole wheat on broiler performance and carcass trait, Poult. Sci., 80, 195, 10.1093/ps/80.2.195

Singh, 2014, Influence of feeding coarse corn on performance, nutrient utilisation, digestive tract measurements, carcass characteristics, and cecal microflora counts of broilers, Poult. Sci., 93, 607, 10.3382/ps.2013-03542

Svihus, 2004, Causes for improvement in nutritive value of broiler chicken diets with whole wheat instead of ground wheat, Br. Poult. Sci., 45, 55, 10.1080/00071660410001668860

Aghazadeh, 2012, Effect of butyric acid supplementation and whole wheat inclusion on the performance and carcass traits of broilers, S. Afr. J. Anim. Sci., 42, 241, 10.4314/sajas.v42i3.5

Mabelebele, 2018, Whole sorghum inclusion and feed form on performance and nutrient digestibility of broiler chickens, J. Appl. Anim. Nutr., 6, e5, 10.1017/JAN.2018.3

Salway, J.G. (2004). Metabolism at a Glance, Blackwell Publishing Ltd.. [3rd ed.].

Lamot, D.M., Sapkota, D., Wijtten, P.J.A., van den Anker, I., Heetkamp, M.J.W., Kemp, B., and van den Brand, H. (2018). Diet density during the first week of life: Effects on growth performance, digestive organ weight, and nutrient digestion of broiler chickens. Poult. Sci.

Buyse, 2004, Assessment of age-related glucose oxidation rates of broiler chickens by using stable isotopes, Life Sci., 75, 2245, 10.1016/j.lfs.2004.05.016

Crespo, R., and Shivaprasad, H.L. (2003). Developmental, metabolic, and other noninfectious disorders. Diseases of Poultry, Iowa State Press. [11th ed.].

Butler, 1976, Fatty liver disease in the domestic fowl: A review, Avian Pathol., 5, 1, 10.1080/03079457608418164

Wolford, 1972, Lipid accumulation and hemorrhage in livers of laying chickens. A study on fatty liver-hemorrhagic syndrome (FLHS), Poult. Sci., 51, 1707, 10.3382/ps.0511707

Wolford, 1972, Effect of diet on fatty liver-hemorrhagic syndrome incidence in laying chickens, Poult. Sci., 51, 2087, 10.3382/ps.0512087

Whitehead, 1979, Nutritional and metabolic aspects of fatty liver disease in poultry, Vet. Q., 1, 150, 10.1080/01652176.1979.9693738

Meijering, 1980, Fatty liver syndrome in laying hens. An attempt to review, World’s Poult. Sci. J., 35, 79, 10.1079/WPS19790007

Butler, 1975, Lipid metabolism in the fowl under normal and abnormal circumstances, Proc. Nutr. Soc., 34, 29, 10.1079/PNS19750007

Polin, 1976, Various types of diets, sources of energy, and positive energy balance in the induction of fatty liver hemorrhagic syndrome, Poult. Sci., 55, 325, 10.3382/ps.0550325

Pearson, 1978, Influence of dietary cereal and energy content on the accumulation of lipids in the liver in fatty liver haemorrhagic syndrome in the fowl, Res. Vet. Sci., 24, 72, 10.1016/S0034-5288(18)33101-1

Polin, 1982, Lipid: The unidentified factor for alleviating fatty liver syndrome, Poult. Sci., 61, 2075, 10.3382/ps.0612075

Jensen, 1976, Influence of carbohydrate source on liver fat accumulation in hens, Poult. Sci., 55, 700, 10.3382/ps.0550700

Maurice, 1978, Influence of diet composition on hepatic lipid accumulation and hemorrhages in caged layers, Poult. Sci., 57, 989, 10.3382/ps.0570989

Olomu, 1975, Effects of span rapeseed meal on productive performance, egg quality, composition of liver and hearts and incidence of “fatty livers” in laying hens, Can. J. Anim. Sci., 55, 71, 10.4141/cjas75-009

Bhatnagar, 1980, Ultrastructural study of liver fibrosis in turkeys fed diets containing rapeseed meal, Res. Vet. Sci., 29, 260, 10.1016/S0034-5288(18)32674-2

Martland, 1984, Rapeseed induced liver haemorrhage, reticulolysis and biochemical changes in laying hens: The effects of feeding high and low glucosinolate meals, Res. Vet. Sci., 36, 298, 10.1016/S0034-5288(18)31950-7

Hemsley, 1973, A comparison of barley, oats, sorghum and wheat in the production of the fatty liver and kidney syndrome, Br. Vet. J., 129, lxv, 10.1016/S0007-1935(17)36400-X

Payne, 1974, Involvement of biotin in the fatty liver and kidney syndrome of broilers, Br. Poult. Sci., 15, 489, 10.1080/00071667408416137

Frigg, 1976, Bioavailability of biotin in cereals, Poult. Sci., 55, 2310, 10.3382/ps.0552310

Bryden, 1979, The influence of vitamin A status on the response of chickens to aflatoxin B1 and changes in liver lipid metabolism associated with aflatoxicosis, Br. J. Nutr., 41, 529, 10.1079/BJN19790068

Jensen, 1976, Liver lipid accumulation and performance of hens as affected by cage density and initial body weight, Poult. Sci., 55, 1926, 10.3382/ps.0551926

Hansen, 1993, Avian fatty liver hemorrhagic syndrome: A comparative review, Adv. Vet. Sci. Comp. Med., 37, 451

Weitzenburger, 2005, Effect of furnished small group housing systems and furnished cages on mortality and causes of death in two layer strains, Br. Poult. Sci., 46, 553, 10.1080/00071660500303206

Shini, S., Stewart, G., Shini, A., and Bryden, W. (2006, January 10–14). Mortality rates and causes of death in laying hens kept in cage and alternative housing systems. Proceedings of the 12th European Poultry Conference, Verona, Italy.

Pearson, 1978, Environmental temperature as a factor in the aetiology of fatty liver-haemorrhagic syndrome in the fowl, Res. Vet. Sci., 25, 133, 10.1016/S0034-5288(18)32967-9

Ivy, 1973, Factors influencing the liver fat content of laying hens, Poult. Sci., 52, 281, 10.3382/ps.0520281

Akiba, 1983, The influence of environmental temperature, thyroid status and a synthetic oestrogen on the induction of fatty livers in chicks, Br. Poult. Sci., 24, 71, 10.1080/00071668308416715

Ayo, J.O., Obidi, J.A., and Rekwot, P.I. (2011). Effects of heat stress on the well-being, fertility, and hatchability of chickens in the northern guinea savannah zone of Nigeria: A review. ISRN Vet. Sci.

Clark, 1974, Effect of high environmental temperature on internal organs of chickens, Poult. Sci., 53, 859, 10.3382/ps.0530859

Lee, 1975, Factors affecting liver fat accumulation and liver hemorrhages associated with fatty liver-hemorrhagic syndrome in laying chickens, Poult. Sci., 54, 374, 10.3382/ps.0540374

Pearson, 1978, The oestrogenised chick as an experimental model for fatty liver-haemorrhagic syndrome in the fowl, Res. Vet. Sci., 24, 82, 10.1016/S0034-5288(18)33103-5

Walzem, 1999, Estrogen induction of VLDLy assembly in egg-laying hens, J. Nutr., 129, 467s, 10.1093/jn/129.2.467S

Scheele, 1997, Pathological changes in metabolism of poultry related to increasing production levels, Vet. Q., 19, 127, 10.1080/01652176.1997.9694756

Polin, 1977, Role of oestrogen as a cause of fatty liver hemorrhagic syndrome, J. Nutr., 107, 873, 10.1093/jn/107.5.873

Couch, 1956, Fatty livers in laying hens—A condition which may occur as a result of increased strain, Feedstuffs, 28, 46

Stake, 1981, Induction of fatty liver-hemorrhagic syndrome in laying hens by exogenous beta-estradiol, Avian Dis., 25, 410, 10.2307/1589933

Abplanalp, 1988, Genetic predisposition for fatty liver rupture in White Leghorn hens of a highly inbred line, Poult. Sci., 67, 52

Squires, 1988, Aetiology of fatty liver syndrome in laying hens, Br. Vet. J., 144, 602, 10.1016/0007-1935(88)90031-0