ABSTRACT
The objective of this study was to evaluate the effects of supra-nutritional level of selected B vitamins in different types of diet on broiler performance. Two experiments were conducted using male and female one-day-old chicks (n=288 each; initial body weights in experiment I and II was, respectively, 47.57 ± 0.43, and 47.98 ± 0.31) reared in batteries up to 18 days. In experiment I, the chicks were fed a corn and soybean meal-based diet and, in experiment II, a diet containing oxidized animal by-product meals and soybean oil was used. Both experiments followed a completely randomized design in a 3 × 2 factorial arrangement, consisting of the factors: i) supplementation levels of selected B vitamins (control, 3- or 6-times control of the vitamins riboflavin, pantothenic acid, niacin, folic acid and vitamin B12); ii) dietary nutritional density (low or high), totaling 6 treatments and 8 replicates of 6 birds each (3 males and 3 females). As result of this study, in Exp. I, chicks showed higher weight gain (741.1 g vs. 697.3 g) and feed intake (920.2 vs. 878.5 g) when fed low-nutritional density diet with supra-nutritional vitamin level 6-times higher than the control. However, this effect was not found in the performance of chickens fed high-nutritional density diet. Despite the poor quality of the ingredients used in Exp. II, no statistical effect was shown of the use of vitamin super-dose in rations with different dietary nutrient density. Feed conversion ratio (FCR) was significantly improved for chickens fed high-nutritional density diet (1.191 vs. 1.246 in experiment I, 1.244 vs. 1.275 in experiment II, p<0.01). We conclude that birds fed a vegetable diet formulated with low-dietary density improved body weight (BW) and feed intake (FI) when receiving supra-nutritional levels of vitamins 6-times higher than the control.
Keywords:
Animal by-product; B vitamins complex; Dietary nutrient density; Performance parameters, Vegetable diet
INTRODUCTION
Most of the poultry diets in Brazil are based on corn and soybean meal, which supplies the greater part of energy and protein in the feed. The use of by-products of the meat processing industry is a safe way to use low-cost products that contribute to the nutritional quality and cost of the diets (Caires et al., 2010Caires CM, Fernandes EA, Fagundes NS, Carvalho AP, Maciel MP, Oliveira BR. The use of animal byproducts in broiler feeds. Use of animal co-products in broilers diets. Brazilian Journal of Poultry Science 2010;12(1):41-46.). Among these ingredients are residues such as inedible viscera, feathers, bones, blood and fat, which have no commercial purpose for human consumption. Despite of the use of antioxidants in the processing of this ingredients, animal by-products are susceptible to autoxidation. Because its rich nutritional composition, especially the high percentage of fat, makes them very susceptible to chemical and bacterial spoilage (Amaral et al., 2018Amaral AB, Silva MV, Lannes SCS. Lipid oxidation in meat: mechanisms and protective factors - a review. Food Science and Technology 2018;38(1):1-15.).
Together, different components of food, nutrients, and dietary patterns have a high capacity to change the growth of different microbial species and/or the modulation of community dynamics of the gut microbiota (Ishiguro et al., 2018Ishiguro E, Haskey N, Campbell K. Impact of nutrition on the gut microbiota. In: Ishiguro E, Haskey N, Campbell K, editor. Gut microbiota: interactive effects on nutrition and health. Amsterdam: Elsevier; 2018. p. 105-131.). For example, Bacteroides spp. are associated with diets containing animal protein sources, while Prevotella spp. are related to vegetable diets (Wu et al., 2011Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keibaugh SA, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334(6052):105-108.). Diets rich in vegetable ingredients including polyphenols and fibers are shown to be beneficial for gut health by providing substrates such as vitamins, short chain fatty acids, etc. to the host during microbial fermentation (Zoetendal & De Vos, 2014Zoetendal EG, De Vos WM. Effect of diet on intestinal microbiota and its activity. Current Opinion in Gastroenterology 2014;30(2):189-195.). Moreover, the consumption of diets containing carbohydrates from vegetable sources and fibers provides a greater variety of bacteria than diets containing animal protein (Martízez et al., 2015). In humans, it has been shown that microbial diversity was reduced in association with worse metabolic and inflammatory status (Rosario et al., 2016Rosario VA, Fernandes R, Trindade EBSM. Vegetarian diets and gut microbiota: important shifts in markers of metabolism and cardiovascular disease. Nutrition Reviews Advance Access 2016;74(7):444-454.).
Dietary nutrient density is also a factor that has an impact on the health and growth of animals (Coelho & McNaughton, 1995Coelho MB, McNaughton JL. Effect of composite vitamin on broilers. Journal of Applied Poultry Research 1995;4:219-229.). A physiological stress condition can be promoted using diets with high nutritional density due to increased rates of growth and metabolism. The levels of nutrients provided in the feed may not be adequate for the functioning of the immune system and animals’ maximum resistance to disease under these circumstances. Thus, the requirements for certain nutrients may increase in order to achieve the maximum performance of poultry raised in intensive commercial systems.
Broilers raised in commercial systems are exposed to adverse environmental conditions that can increase stress and diseases. Coelho et al. (2001Coelho MB, McKnight W, Cousins B. Effect of a targeted B-vitamin regimen on rate and efficiency of fast growing broilers from 0 to 49 days. Indianapolis: Poutry Science Association; 2001. p. 201.) reported that the use of super-dose 16-times higher than the basal level recommended by the NRC (1994) of the vitamins riboflavin, pantothenic acid, niacin, folic acid, and vitamin B12 resulted in improved performance when chickens were submitted to stress conditions similar to those found in the field. These vitamins are closely linked to the metabolism of carbohydrates, amino acids, synthesis of methyl groups, and nucleic acids. The use of super-doses of water-soluble vitamins may be used to meet the metabolic needs, as well as the needs of intestinal microorganisms, being a simple alternative to be implemented in the field. Therefore, our purpose was to evaluate the effect of the use of supra-nutritional levels of selected B vitamins, riboflavin, pantothenic acid, niacin, folic acid, and vitamin B12, on broiler performance using different dietary patterns.
MATERIAL AND METHODS
All procedures used in these experiments were approved by the institutional animal care and use committee of the College of Agriculture “Luiz de Queiroz”, University of Sao Paulo (process n. 2017.5.1809.11.9). Two experiments were conducted using male and female one-day-old chicks Ross AP 95 (n=288 each) housed in metallic batteries up to 18 days. Chicks were weighed by cage for equal distribution. Both the experiments consisted in a completely randomized design using a 3 × 2 factorial arrangement with supplementation levels of selected B vitamins (control, 3- or 6-times control of vitamins riboflavin, pantothenic acid, niacin, folic acid and vitamin B12), and dietary nutritional density (low or high) as a factors, totaling 6 treatments and 8 replicates of 6 birds each (3 males and 3 females). The basal feed differed between experiments: Exp. I - corn and soybean meal-based diet; Exp. II - diet containing oxidized animal by-products (meat and bone meal, feather meal, and poultry by-products meal) and oxidized soybean oil (Table 1).
The treatments for both experiments were as follows: Lo-Cont (low-dietary density with control level of selected B vitamins); Lo-3× (low-dietary density with 3-times control level of selected B vitamin); Lo-6× (low-dietary density with 3-times control level of selected B vitamin); Hi-Cont (high-dietary density with control level of selected B vitamins); Hi-3× (high-dietary density with 3-times control level of selected B vitamin); and Hi-6× (high-dietary density with 3-times control level of selected B vitamin).The birds had ad libitum access to water and feed in mash the entire experimental period.
The feed and vitamin supplement were formulated to meet the nutrient specifications of the Brazilian Tables (Rostagno et al., 2017Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Costa FGP, et al. Tabelas brasileiras para aves e suínos. 4th ed. Viçosa: Universidade Federal de Viçosa; 2017.), and are presented in Tables 1 and 2. At the feed mill, the control diets (Lo-Cont and Hi-Cont) were produced in a single batch and subdivided for the addition of the super-dose of the vitamin supplement. These super-doses were included in the diets over the top. The total weight of these ingredients represents 0.17% and 0.43% for the treatments with 3- or 6-times control of selected B vitamin, respectively. Thus, it ensured that there was no difference between the experimental diets, except for vitamin supplementation. The amount of vitamins present in the control diets were accounted for when the over the top supplementation was calculated.
At 6, 12 and 18 days of age, the chickens and the feed were weighed by cage to calculate the body weight gain (BWG), feed intake (FI) and feed conversion ratio (FCR).
MEASURING INGREDIENTS QUALITY
In order to ensure that the animal by-product meals and soybean oil used in experiment II had lower quality standards, these ingredients were submitted to the laboratory analyzes (Table 3). For comparative purpose, the analyzes of the soybean oil used in experiment I was also included. The analyzes of peroxide value, acidity (method 27 for animal by-products meal, and method 28 for vegetable oils), and rancidity were performed according to the methodologies described by the Compêndio Brasileiro de Alimentação Animal (SINDIRAÇÕES, 2017). Thiobarbituric acid reactive substances (TBARS) determination was quantified in triplicate for each ingredient according to AOAC (1990) recommendations with some modifications. It was used as standard 1,1,3,3-tetraethoxypropane (TEP), which on acid hydrolysis produces malonaldehyde ratio of 1 mol: 1 mol, to obtain a standard curve consisting of five points of different concentrations (0.6; 1.0; 2.5; 5.0; 10.0 µmol / L of TEP). For each sample of animal by-product meals, the aldehydes were extracted by ultrahomogenization at 3500 rpm using Ultra Turrax (Ika T18 basic, Wilmington, North Carolina, USA) of 15 mL of trichloroacetic acid solution (7.5%) with addition of 0.015 g of propyl gallate, and 0.015 g of ethylenediaminetetraacetic acid, with approximately 7 g of sample. After filtration of the homogenate, 2.5 mL of the filtrate were transferred to a test tube and added to 2.5 mL of thiobarbituric acid reagent 46 mM. These samples were immersed in water bath at 95 °C for 35 min and then cooled in an ice bath for about 5 min. The absorbance was measured at 532 nm using spectrophotometer (Shimadzu, UV-Vis mini 1240, Chiyoda-ku, Tokyo, Japão). For these quantification, standard solutions of malonaldialdehyde (MDA) in 7.5% TCA were prepared from TEP and calibration curves. The results were calculated from the TEP curve and expressed in mg MDA per kg of sample.
Peroxide value, acidity, TBARS and rancidity of the animal by-product meals and the soybean oil fresh (experiment I) and oxidized (experiment II) used in the feed.
For the determination of the TBARS values of the soybean oil samples, the analysis was adapted according to the procedure described by Papastergiadis et al. (2012Papastergiadis A, Mubiru E, Langenhove HV, Meulenae B. Malondialdehyde measurement in oxidized foods: evaluation of the spectrophotometric thiobarbituric acid reactive substances (TBARS) test in various foods. Journal of Agriculture and Food Chemistry 2012;60:9589-9594.) for the extraction of aldehydes. The aqueous layer was collected, and the procedure was repeated twice. The collected extract reacted with the TBA reagent, as described above.
Vitamin analyzes of feed samples
The levels of riboflavin, pantothenic acid, niacin, folic acid and vitamin B12 present in the feed were determined at the laboratory Eurofins CLF (Friedrichsdorf, Germany). The assay comprised extraction of riboflavin and its coenzyme forms in an autoclave using diluted sulfuric acid. Phosphor ester bonds were cleaved enzymatically. After dilution and centrifugation of the extract, the riboflavin content was determined by reversed phase HPLC using fluorimetric detection (Rubaj et al., 2008Rubaj J, Bielecka G, Korol W, Kwiatek K. Determination of riboflavin in premixture and compound feed by liquid chromatography method. Bulletin of the Veterinary Institute in Pulawy 2008;52:619-624.). Nicotinic acid and nicotinamide were extracted from feed using 0.001N-sulfuric acid. After dilution of the extract with mobile phase and centrifugation an aliquot of the clear solution was chromatographed using a reversed phase HPLC system (detection at 260 nm) (Van Niekerk et al., 1984Van Niekerk PJ, Smit SCC, Strydom ESP, Armbruster G. Comparison of high-performance liquid chromatographic and microbiological methods for the determination of niacin in foods. Journal of Agricultural and Food Chemistry 1984;32(2):304-307.). Free pantothenic acid was extracted with water and analyzed by reversed-phase HPLC. Folic acid and vitamin B12 were also determined by HPLC methodology (Heudi et al., 2005Heudi O, Kilinç T, Fontannaz P. Separation of water-soluble vitamins by reversed-phase high performance liquid chromatography with ultra-violet detection: Application to polyvitaminated premixes. Journal of Chromatography 2005;1070(1/2):49-56.).
Statistical analysis
The data of productive performance was analyzed by ANOVA with procedures appropriate for a completely randomized design in a factorial arrangement 3 × 2 using the GLM procedure of the statistical program SAS 9.4, and the means were compared using Tukey’s test. All data were checked for homogeneity of variances and normality of residues.
RESULTS AND DISCUSSION
The analyzed concentration of the vitamins riboflavin, pantothenic acid, niacin, folic acid, and vitamin B12 in the experimental diets are reported in Table 4, along with the expected values. The laboratory analyzes are one of the biggest issues in research with vitamins, because even with the attention at the feed mill, sample collection, etc., the analyzed values in the complete feed may not coincide with the expected ones. In this study, feed processing did not affect severely the retention of the vitamins used in the diets, since there was no heat treatment in the feed such as pelleting, expansion or extrusion. However, values for folic acid were higher than expected in the diet with supra-nutritional levels of vitamins, whereas the other vitamins analyzed presented values relatively close to the expected. In agreement to our results, Stahly et al. (2007Stahly TS, Williams NH, Lutz TR, Ewan RC, Swenson SG. Dietary B vitamin needs of strains of pigs with high and moderate lean growth. Journal of Animal Science 2007;85(1):188-195.) evaluated the same 5 test vitamins in a swine experiment and found a high concentration of folic acid in the feed compared to the calculated value. In both experiments, the same supplement of the selected B vitamins was added in the feed over the top and the same equipment was used to mix these feeds; even though the values of the vitamins recovered in the feed Lo-3× were analytically lower in experiment II than in experiment I.
In experiment I, BW (p=0.032) and BWG (p=0.040) were affected by vitamins supplementation level in the 1-6d period (Table 5). Body weight and body weight gain were higher when chicks were fed the 6-times vitamin level. Feed conversion ratio also tended (p=0.082) to be improved in this treatment. There was a significant (p=0.051) vitamin supplementation × dietary nutrient level interaction for FI. Feed intake of chicks increased when the 6-times vitamin level was used in the diet formulated with low-dietary nutrient density (Table 6). However, FI was not affected by supra-nutritional levels of vitamins when the high-density diet was fed.
When the period of 1 to 12 days was evaluated (Table 5), there was also a significant (p=0.036) interaction for FI, similar to that observed in the initial period (Table 6). Body weight (p=0.005) and body weight gain (p=0.005) improved when chickens were fed a diet supplemented with 6-times vitamin level. In addition, broilers fed with high-dietary nutrient density had better performance compared with those fed the low-density (p<0.001).
For the entire experimental period (1-18d), there were significant interactions between vitamin supplementation and dietary nutrient density for BW (p=0.053), BWG (p=0.050) and FI (p=0.022). In this respect, super-dose of 6-times control of selected B vitamins affected more the BW, BWG, and FI of chickens fed low-dietary nutritional density than with the high-density diets (Table 6). Feed conversion ratio was improved (p<0.001) for chickens fed a diet formulated with high-dietary nutritional density, irrespective of vitamin supplementation level.
The impact of the dietary levels of the same five vitamins tested were evaluated by Stahly et al. (2007Stahly TS, Williams NH, Lutz TR, Ewan RC, Swenson SG. Dietary B vitamin needs of strains of pigs with high and moderate lean growth. Journal of Animal Science 2007;85(1):188-195.) on performance of pigs with a high or moderate genetic capacity for lean tissue accretion. In that study, as the concentration of vitamins increased in the diet, body weight gain and feed conversion ratio improved. The results were more pronounced for animals with high lean tissue growth and this finding may be explained by the changes in metabolic pathways and not the highest energy intake or body energy incorporation rate.
In our experiment, we expected an increase in performance responses of chickens fed the supra-nutritional levels of the selected B vitamins compared with the control level with advancing age. Weight gain and feed intake were stimulated by the super-dose of 6-times vitamin levels in both dietary nutrient densities. Nevertheless, less pronounced response was noted for chickens receiving high-density diets. As we know, birds fed high energy density diets have improved body weight and feed efficiency (Lott et al., 1992Lott BD, Day EJ, Deaton W, May JD. The effect of temperature, dietary energy level, and corn particle size on broiler performance. Poultry Science 1992;71:618-624.). Because of that, vitamin super-dose did not influence the performance of chickens fed high-dietary nutrient density in our research.
The treatment 3-times vitamin levels with low-nutrient density diet resulted in lower performance of the chickens, beginning in the first period evaluated (1-6d). This effect was not observed for the high-density diet receiving the same vitamin dose. Because specific treatment effect of vitamin supplementation was not expected in this period, there is no reasonable explanation for this loss in performance other than an uncontrolled experimental error. This loss in performance was more pronounced in the latter periods.
In experiment II, no interactions between the main effects of vitamin supplementation and dietary nutrient level were observed for any of the traits studied (Table 7). However, feed conversion ratio was improved in broilers fed high-dietary nutritional density in the 1-18d period (p=0.008).
The animal by-product meals and soybean oil used in experiment II had poor quality relative to the recommended standards according to Compêndio Brasileiro de Alimentação Animal (SINDIRAÇÕES, 2017). The analyses of lipid oxidation to characterize the quality of animal by-product meals and soybean oils (experiment I and II) should be studied together (Table 3). According to the industry, crude degummed soybean oil should have values of up to 2.0% acidity and 10.0 mEq/kg for peroxide value. The oil samples from both experiments were within the limits for acidity and peroxide value, but, the acidity for the oil in experiment II was 10-times as high and the TBARS value confirms that the oil used in experiment II had been oxidized. Although the birds fed a high pro-oxidant diet with 3% oxidized oil showed the higher inflammation scores at 21 d compared with the standard group receiving non oxidized oil (Lu et al., 2014Lu T, Harper AF, Zhao J, Corl BA, LeRoith T, Dalloul RA. Effects of a dietary antioxidant blend and vitamin E on fatty acid profile, liver function, and inflammatory response in broiler chickens fed a diet high in oxidants. Poultry Science 2014;93:1658-1666.), suggesting a stress condition; in our study, the birds were healthy and well nourished, which may have limited the effects of using vitamin super-doses. Additionally, the final level of lipid oxidation in these diets was low, due to the low inclusion of animal by-products.
The quality standards by Compêndio Brasileiro de Alimentação Animal (SINDIRAÇÕES, 2017) for animal by-product meals are 6.0 mg NaOH/g acidity and 3.0 mEq/kg peroxide value. In our study, feather meal (10.0% ether extract) presented values within the standard for these parameters. On the other hand, meat and bone meal and poultry by-product meal (13.0 and 11.8% of ether extract, respectively) showed a high degree of oxidation. Rancidity was also detected in poultry by-products meal. Therefore it is possible to ascertain that these ingredients were in the process of auto-oxidation.
Studies on the animal by-product meals utilization in comparison to corn and soybean-meal-based diets for chickens showed an improvement in intestinal health. Birds fed a diet containing animal by-product meals had a low number of congestive or hemorrhagic points recorded in the intestine during the visual analysis of the duodenum at 21 days of age (Bellaver et al., 2005Bellaver C, Fagonde Costa CA, Avila VS, Fraha M, Lima GJMM, Hackenhar L, et al. Substituição de farinhas de origem animal por ingredientes de origem vegetal em dietas para frangos de corte. Ciência Rural 2005;35(3):671-677.) and a low lesion score for ileum histological analysis, such as lamina propria thickness, mixed inflammatory cell infiltration, necrosis and presence of oocysts, at 28 days of age (Belote et al., 2017Belote BL, Pont GCD, Panisson J, Wammes J, Bittencourt L, Maiorka A, et al . Differences of animal or vegetable diets on broiler performance and intestinal integrity. Proceedings of the 2017 PSA Annual Meeting; 2017; Orlando, Florida. Champaign: Poultry Science Association; 2017. p. 59.).
Unexplained experimental results in our study may be justified by the lack of knowledge about the interactions that occur between the intestinal microbiota and the nutrients provided in the rations. We did not collect intestinal contents for microbiota analysis. However, the microbiota analysis could show the variation between individual birds per dietary treatment are more pronounced in comparison to the variation caused by feed composition as reported by Van Der Hoeven-Hangoor et al. (2013Van Der Hoeven-Hangoor E, Van Der Vossen JMBM, Schuren FHJ, Verstegen MWA, Oliveira JE, Montijn RC, et al. Ileal microbiota composition of broilers fed various commercial diet compositions. Poultry Science 2013;92:2713-2723.). Moreover, Steinert et al. (2016Steinert RE, Sadabad MS, Harmsen HJM, Weber P. The prebiotic concept and human health: a changing landscape with as a novel prebiotic candidate? European Journal of Clinical Nutrition 2016;70(12):1348-1353.) discussed different concepts for the characterization of a substance as a prebiotic for humans, and the use of vitamin riboflavin as a “new” prebiotic was proposed. Although it does not provide a direct substrate for microbial fermentation, riboflavin may beneficially modulate the composition of the gut microbiota by being metabolized and changing the gastrointestinal redox state. That is in accordance with the definition of Gibson & Roberfroid (1995Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 1995;125(6):1401-1412.) that prebiotics are ingredients that promote beneficial effects to the host by stimulating the growth and / or activity of one or a limited number of bacteria in the colon, promoting improvement in host intestinal health.
The dynamics of the microbiota is also affected by the facilities where the study is conducted. Birds raised in metallic batteries are more demanding in vitamins than those raised on floor pens, which exhibit coprophagy. Birds raised on the floor consume the vitamins synthesized by the lower gut bacteria that are excreted to the environment because they are not absorbed in the cecum (Vispo & Karasov, 1997Vispo C, Karasov WH. The interaction of avian gut microbes and their host: an elusive symbiosis. In: Mackie RI, White BA, editor. Gastrointestinal microbiology. Boston: Chapman & Hall; 1997. p.116-155.). On the other hand, these chickens are also exposed to other stress factors, interfering at the vitamin level for maximum growth. In addition, the variation in microbiota also occurred between individual birds with the same genetics and housed in the same environment (Van Der Hoeven-Hangoor et al., 2013Van Der Hoeven-Hangoor E, Van Der Vossen JMBM, Schuren FHJ, Verstegen MWA, Oliveira JE, Montijn RC, et al. Ileal microbiota composition of broilers fed various commercial diet compositions. Poultry Science 2013;92:2713-2723.).
The use of supra-nutritional levels of vitamins riboflavin, pantothenic acid, niacin, folic acid, and vitamin B12 resulted in improved productive performance for chickens raised in batteries and fed a corn and soybean-based diet formulated with low-dietary density. It is known that vegetable diets are more aggressive to the intestinal mucosa of birds in relation to diets containing animal by-product meals. Therefore, the results obtained in this study allow to conclude that when we use low nutritional density in corn-soybean meal-based diets, the use of supra-nutritional level of vitamin supplementation may be needed for the birds to reach their maximum production potential.
ACKNOWLEDGEMENTS
D. Suckeveris received a scholarship financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001, and by the Conselho Nacional de Pesquisa - Brazil (CNPq) - process n. 142307/2018-1 and 140123/2019-9.
The authors acknowledge the funding from DSM Nutritional Products.
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- Coelho MB, McKnight W, Cousins B. Effect of a targeted B-vitamin regimen on rate and efficiency of fast growing broilers from 0 to 49 days. Indianapolis: Poutry Science Association; 2001. p. 201.
- Coelho MB, McNaughton JL. Effect of composite vitamin on broilers. Journal of Applied Poultry Research 1995;4:219-229.
- Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition 1995;125(6):1401-1412.
- Heudi O, Kilinç T, Fontannaz P. Separation of water-soluble vitamins by reversed-phase high performance liquid chromatography with ultra-violet detection: Application to polyvitaminated premixes. Journal of Chromatography 2005;1070(1/2):49-56.
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- Lott BD, Day EJ, Deaton W, May JD. The effect of temperature, dietary energy level, and corn particle size on broiler performance. Poultry Science 1992;71:618-624.
- Lu T, Harper AF, Zhao J, Corl BA, LeRoith T, Dalloul RA. Effects of a dietary antioxidant blend and vitamin E on fatty acid profile, liver function, and inflammatory response in broiler chickens fed a diet high in oxidants. Poultry Science 2014;93:1658-1666.
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- Rosario VA, Fernandes R, Trindade EBSM. Vegetarian diets and gut microbiota: important shifts in markers of metabolism and cardiovascular disease. Nutrition Reviews Advance Access 2016;74(7):444-454.
- Rostagno HS, Albino LFT, Hannas MI, Donzele JL, Sakomura NK, Costa FGP, et al. Tabelas brasileiras para aves e suínos. 4th ed. Viçosa: Universidade Federal de Viçosa; 2017.
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- Steinert RE, Sadabad MS, Harmsen HJM, Weber P. The prebiotic concept and human health: a changing landscape with as a novel prebiotic candidate? European Journal of Clinical Nutrition 2016;70(12):1348-1353.
- Van Der Hoeven-Hangoor E, Van Der Vossen JMBM, Schuren FHJ, Verstegen MWA, Oliveira JE, Montijn RC, et al. Ileal microbiota composition of broilers fed various commercial diet compositions. Poultry Science 2013;92:2713-2723.
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- Zoetendal EG, De Vos WM. Effect of diet on intestinal microbiota and its activity. Current Opinion in Gastroenterology 2014;30(2):189-195.
Publication Dates
-
Publication in this collection
02 Nov 2020 -
Date of issue
2020
History
-
Received
28 Nov 2019 -
Accepted
29 June 2020
