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Energy levels and lysine, calcium and phosphorus adjustments on broiler nutrient digestibility and performance

Abstract

Chicken broilers digestibility and performance fed with different ME levels, with and without adjustments of digestible lysine, calcium, and available phosphorus, were evaluated. For digestibility, 210 male Cobb 500 chicken broilers were used and distributed into a 3x2+1 factorial arrangement, with three ME levels (3050; 3125 and 3200 kcal/kg) with and without nutrient adjustment, plus one control treatment (2975 kcal ME/kg), totaling seven treatments including six repetitions with five birds into each repetition. For initial performance, 1120 birds were distributed randomly with eight replications within treatments and 20 birds for each replication. For final performance, 1008 chickens were distributed with eight replications and 18 birds for each replication. The DCDM and DCCP were improved (P<0.05) according to the increase of ME and the adjustment in dietary nutrients, as well as GE digestibility. The final performance showed no interaction (P>0.05) between energy and nutrient adjustment, but the increase in energy levels improved the feed conversion ratio (FCR=1.370). Increasing energy density with nutrient adjustment improves both nutrient utilization and bird performance.

Key words
amino acids; animal nutrition; calorie; minerals

INTRODUCTION

Broiler nutrition is one of the poultry farming segments which has most contributed to its development. Thus, defining the energy level to be used in bird diets is an important decision, since the energetic ingredients are expensive and increment the diet total cost (Karomy et al. 2019KAROMY AS, HABIB HN & KASIM SA. 2019. Influence of Different Levels of Crude Protein and Metabolizable Energy on Production Performance of Ross Broiler. J Biol Agric Health 9: 20-24.). Moreover, the proper calorie-nutritional balance relationship in the diet may affect protein synthesis or degradation, the utilization of the other supplied nutrients and carcass yield (Sayed et al. 2017SAYED RE, IBRAHIM D & SAID EN. 2017. Effect of dietary calorie and protein content on performance, behaviour, expression of some growth-related genes and economic of broiler chickens. Zagazig Vet J 45: 326-339.).

In this perspective, metabolizable energy (ME) is considered a strategic nutritional factor since feed intake in birds is regulated, mainly, by the diet calorie density. Therefore, the amino acids requirements and other nutrients should be expressed as a function of the diet ME level (Karomy et al. 2019KAROMY AS, HABIB HN & KASIM SA. 2019. Influence of Different Levels of Crude Protein and Metabolizable Energy on Production Performance of Ross Broiler. J Biol Agric Health 9: 20-24.). Hence, these nutrients should be proportionally adjusted when the energy level of the diet is increased, in order to prevent excessive protein deposition and maintain growth rate (Leeson & Summers 2001LEESON S & SUMMERS JD. 2001. Nutrition of the chicken. 4th ed., Guelph: University Books, 413 p.).

Scientific literature has demonstrated the beneficial effect of diets with a higher energy density and adjustments in lysine, calcium and phosphorus nutrients on birds performance and carcass traits (Hidalgo et al. 2004HIDALGO MA, DOZIER WA, DAVIS AJ & GORDON RW. 2004. Live Performance and Meat Yield Responses of Broilers to Progressive Concentrations of Dietary Energy Maintained at a Constant Metabolizable Energy-to-Crude Protein Ratio. J Appl Poult Res 13: 319-327., Dozier et al. 2011DOZIER WA, GEHRING CK & CORZO UMA. 2011. Apparent metabolizable energy needs of male and female broilers from 36 to 47 days of age. Poult Sci 90: 804-814.). Diets without adjustments for calorie-to-amino acid ratio may affect plasma and tissues amino acid concentrations, resulting in decrease of feed intake and animal growth (Sayed et al. 2017SAYED RE, IBRAHIM D & SAID EN. 2017. Effect of dietary calorie and protein content on performance, behaviour, expression of some growth-related genes and economic of broiler chickens. Zagazig Vet J 45: 326-339.). Therefore, this concept indicates is the existence of an optimal balance between energy and amino acids (Aftab 2019AFTAB U. 2019. Energy and amino acid requirements of broiler chickens: keeping pace with the genetic progress. World Poult Sci J 75: 1-8.).

Likewise, minerals act synergistically with energy density. Rostagno et al. (2011)ROSTAGNO HS, ALBINO LFT, DONZELE JL, GOMES PC, OLIVEIRA RF, LOPES DC, FERREIRA AS, BARRETO SLT & EUCLIDES RF. 2011. Tabelas Brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 3nd ed. Minas Gerais: Viçosa, p. 252. found positive correlation between weight gain rate and phosphorus and calcium requirements. Thus, when increasing the ME inclusion in broiler diets, also is important the adjustments of calcium and phosphorus levels, so that skeletal development can be enhanced to support weight gain (Leeson & Summers 2001LEESON S & SUMMERS JD. 2001. Nutrition of the chicken. 4th ed., Guelph: University Books, 413 p.). Additionally, those minerals participate in several metabolic and structural reactions for life maintenance, especially in fast-growing chickens, requiring adequate nutritional supply. According to Shafey et al. (1990)SHAFEY TM, MCDONALD MW & PYM RA. 1990. Effects of dietary calcium, available phosphorus and vitamin D on growth rate, food utilisation, plasma and boné constituents and calcium and phosphorus retention of comercial broiler strains. Bras Poult Sci 31: 587-602., insufficient or excessive supply of one or both minerals alters homeostasis, compromising growth rate and bone mineralization.

Given the above considerations, defining the energy level of broiler diets is essential to meet the correct energy requirements, as well as making nutritional adjustments as a function of ME, providing and maximizing production performance. In the same way, the impact of energy values on nutrients digestibility must also be evaluated. Thus, the present study aimed to determine nutrient diets digestibility and broilers performance fed with formulated diets with different metabolizable energy levels, with and without adjustments in digestible lysine, calcium and available phosphorus.

MATERIALS AND METHODS

Ethical Considerations

All experimental procedures applied in this study were approved by the Animal Ethics Committee of the Federal University of Viçosa - MG, Brazil (approval no. 002/2015).

Digestibility Trial

A total of 210 Cobb 500 male broiler chicks with an initial weight average of 490± 2g were subjected to the experimental treatments in the initial phase from 14 to 21 days of age. Those birds were evaluated in a randomized complete block design with a 3×2+1 factorial arrangement, where block factor was the shed, also were adopted three ME levels, and with and without nutrients adjustment (Dig Lys, Ca and AP), plus one control treatment, completing seven treatments with six replicates for each treatment and five birds per experimental unit. The following treatments were tested:

Treatment 1: 3050 kcal ME/kg, without nutritional adjustments;

Treatment 2: 3125 kcal ME/kg, without nutritional adjustments;

Treatment 3: 3200 kcal ME/kg, without nutritional adjustments;

Treatment 4: 3050 kcal ME/kg + 2.5% nutritional adjustment; (Dig Lys, Ca and AP);

Treatment 5: 3125 kcal ME/kg + 5.0% nutritional adjustment (Dig Lys, Ca and AP);

Treatment 6: 3200 kcal ME/kg + 7.5% nutritional adjustment (Dig Lys, Ca and AP);

Treatment 7: 2975 kcal ME/kg (control).

The experimental diets are detailed in Table I. The nutritionally adjusted diets had digestible lysine, calcium and available phosphor increased by 2.5, 5.0 and 7.5%, respectively, for the three ME levels tested, while the diets without nutritional adjustments showed the same digestible lysine, calcium and available phosphor as control diet, but ME levels of 3050, 3125 and 3200 kcal/kg. Control diet contained 2975 kcal ME/kg, 1.174% of digestible lysine, 0.819% of calcium and 0.391% of available phosphor, and was formulated meeting the nutritional requirements of medium-performance broilers, as proposed by Rostagno et al. (2011)ROSTAGNO HS, ALBINO LFT, DONZELE JL, GOMES PC, OLIVEIRA RF, LOPES DC, FERREIRA AS, BARRETO SLT & EUCLIDES RF. 2011. Tabelas Brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 3nd ed. Minas Gerais: Viçosa, p. 252..

Table I
Ingredients and calculated nutritional composition of the experimental basal diets (8 to 21 days).

Washed sand (inert) and starch were used to adjust the digestible lysine, calcium and available phosphor.

Birds were housed in a shed with concrete floor with wood shavings from the 1st to 13th days of age where both feed and water were offered ad libitum. After this period, they were transferred to metabolic cages (0.60×0.50×0.40 m) equipped with trough feeders and nipple drinkers, where the chicks were kept during the entire first experimental period (14 to 21 days of age). The first five days were used as adaptation period to the diets and metabolic cages; thereafter, excreta samples were collected as recommended by Sakomura & Rostagno (2016)SAKOMURA NK & ROSTAGNO HS. 2016. Métodos de pesquisa em nutrição de monogátricos. 2nd ed., Jaboticabal: Funep, p. 262..

Metabolizability of nutrients ( % ) = Nutrient ingested Nutrient excreted Nutrient ingested

After the end of the collection period, the excreta samples were thawed, homogenized, pre-dried at 55 °C for 72 hours in a forced-air oven, ground through a ball mill and prepared for laboratory analyses of dry matter (DM) (Method 934.01; AOAC Int., 2012), nitrogen (Method 990.03; AOAC Int., 2012) and ether extract (Method 920.39; AOAC Int., 2012AOAC. 2012. AOAC official methods of analysis. 19th ed., Arlington: Association of Official Analytical Chemists.). Gross energy (GE) was determined using a bomb calorimeter (Calorimeter System C200, IKA), with benzoic acid as standard calibration. The metabolizability coefficients of DM, GE and CP and nitrogen retention were estimated in accordance with Sakomura & Rostagno (2016)SAKOMURA NK & ROSTAGNO HS. 2016. Métodos de pesquisa em nutrição de monogátricos. 2nd ed., Jaboticabal: Funep, p. 262..

Performance Trial

All birds were acquired with 1 day of age and kept until the 7th day in shed with concrete floor covered by wood shavings, provided with heating system recommended for this production phase, fed with corn feed and soybean meal, receiving water and feed ad libitum.

The performance trial was divided into two productive phases, birds in the initial phase from 8 to 21 days and, later on, both the growing and finishing phase from 22 to 42 days of age. At the end of the initial phase, the birds were redistributed and introduced into the performance experiment for the next phase.

Birds were housed in a shed with concrete floor lined by wood shavings, which was divided into fifty-six cages of 2 m2 (1.0 m × 2.0 m) containing one semiautomatic trough feeder, one cup-type nipple drinker, light bulbs for heating and wood shavings bedding.

The initial phase performance trial (8 to 21 days) involved 1120 male broilers with an initial weight average of 190±0.19g. The experimental design and treatments were similar to those adopted in the digestibility trial. For the performance trial in growing and finishing production phase (22 to 42 days of age), 1008 broilers with an initial weight average of 855±6 g were evaluated in a completely randomized design, into a 3×2+1 factorial arrangement, with seven treatments and eight replicates by treatment, and 18 birds per experimental unit.

In this phase, the nutritionally adjusted experimental diets contained digestible lysine, calcium and available phosphor increased by 2.5%, 5.0% and 7.5%, respectively (Table II). The unadjusted diets had the same digestible lysine, calcium and available phosphor as control diet, with variations only in ME (3100, 3175 and 3250 kcal/kg). Washed sand (inert) and starch were used to adjust the ME, digestible lysine, calcium and available phosphor values. Lastly, control diet consisted of 3025 kcal ME/kg, 1.050% digestible lysine, 0.685% calcium and 0.320% available phosphor, following the Rostagno et al. (2011)ROSTAGNO HS, ALBINO LFT, DONZELE JL, GOMES PC, OLIVEIRA RF, LOPES DC, FERREIRA AS, BARRETO SLT & EUCLIDES RF. 2011. Tabelas Brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 3nd ed. Minas Gerais: Viçosa, p. 252. nutritional recommendations for medium-performance broilers.

Table II
Feed ingredients and calculated nutrients composition of the experimental diets (22 to 42 days).

A 23:1 lighting program (23 light hours and 1 dark hour) was adopted, with feed and water available ad libitum. The temperature was measured using a thermo-hygrometer at the height of the birds.

Birds were weighed weekly and feed supply was recorded to determine the performance parameters. Mortality was checked daily to adjust the feed conversion ratio.

The following performance parameters were evaluated in each experimental period: final weight (g/bird), weight gain (g/bird), feed intake (g/bird) and feed conversion ratio (g/g). These variables were calculated based on the recorded mortality.

Statistical Analysis

The experimental results were analyzed using SAS 9.0 software (SAS Institute Inc. 2004), in which the GLM procedure was applied within a linear model containing two factors: ME levels and nutrient adjustment, and their interaction. Arithmetic means were compared by Tukey’s test at the 5% significance level. Control diet was compared to the other experimental diets by contrast analysis to determine the effects of energy and nutrients.

RESULTS

The average temperature recorded during the experimental period was 27.6 °C (minimum 22.7 °C; maximum 32.5 °C).

Effect of Diets on Digestibility

There was an interaction effect (P<0.05) between ME level and nutritional adjustment on the digestibility coefficients of dry matter (DCDM) and crude protein (DCCP). Birds fed with high ME diets adjusted for 7.5% nutrients (Dig. Lys, Ca and AP) showed better CDMS and CDPB digestibility (Table III).

Table III
Digestibility coefficient of dry matter (DCDM), crude protein (DCCP), gross energy (DCGE) and nitrogen retention (NR) in broilers fed diets with different metabolizable energy levels with/without nutrients adjustment1.

In contrast, for the unadjusted treatments, only the diet with 3050 kcal ME/kg improved DCDM. Nevertheless, nutritional adjustment improved DCDM at the three energy levels when compared to the energy level of control diet.

The higher nutrient supply through the adjusted diets influenced DCGE (P<0.05), improving energy utilization in relation to the unadjusted diets (Table III). Nitrogen retention did not respond (P>0.05) to the treatments. In addition, diets were adjusted with 5.0% of nutrients providing numerical increase of 119 kcal AME/kg compared to the diet without nutritional adjustment (Table IV).

Table IV
Crude protein, apparent metabolizable energy (AME kcal/kg) observed as a result of experimental treatments1, and feed intake (FI) of broilers, 14 to 21 days old.

Effect of energy and nutrient adjustment on initial bird performance

There was no interaction effect (P>0.05) between the ME levels and nutritional adjustment on the initial performance variables (Table V). However, the diets with higher ME inclusion led to an increase of up to 24 g in weight gain and an improvement in feed conversion, compared to the diets including 3050 kcal ME/kg.

Table V
Weight gain (WG), feed intake (FI) and feed conversion ratio (FCR) of broilers (8 to 21 days old), fed diets with different metabolizable energy levels with/without nutrients adjustment1.

The contrast between the control and test treatments revealed that weight gain increased with the energy density of the diets (WG=726 g), thus feed conversion was also affected by the greater ME inclusion into diets (P<0.05).

Effect of energy and nutritional adjustment on performance of broilers in the growing-finishing phase

No interaction effect (P>0.05) between ME levels and nutritional adjustment (Dig. Lys, Ca and AP) was observed on broiler performance during growing and finishing phases (Table VI). The factors analysis separately showed that feed intake (FI) decreased (P<0.05) as ME was elevated (3250 kcal/kg), which proportionally led to improve FCR.

Table VI
Weight gain (WG), feed intake (FI) and feed conversion ratio (FCR) of broilers (22 to 42 days old), fed diets with different metabolizable energy levels with/without nutrients adjustment1.

Contrast analysis showed that control diet (3025 kcal ME/kg) provided the lowest weight gain, but similar FI to those obtained with the diets containing 3100 and 3175 kcal ME/kg, with and without nutritional adjustments. In contrast, control diet (FI=3347g) differed (P<0.05) only from that with the treatment with the highest energy level (3250 kcal/kg) plus nutritional adjustments, which provided the lowest feed intake (3144 g).

These combinations between intake and gain influenced feed conversion, which worsened (P<0.05) in the animals fed the control diet with the least metabolizable energy (FCR= 1.746) compared to the others.

DISCUSSION

In general, it can be observed the positive effect of the most energetic adjusted diets on DCDM, birds fed with the diet of 2975 kcal ME/kg (control diet) provided the lowest DCDM in relation to diets with nutrient adjustment. This demonstrates, therefore, the additive effect of increasing minerals and amino acids.

The DCDM reflects the digestibility of nutrients; i.e., its increase means better nutrients absorption (Abdulla et al. 2016ABDULLA N, LOH T, AKIT H, SAZILI A & FOO H. 2016. Effects of dietary oil sources and calcium: phosphorus levels on growth performance, gut morphology and apparent digestibility of broiler chickens. S Afr J Anim Sci 46: 42-53.), this fact may be related to the increase of diets energy density, which is mainly obtained by including soybean oil on it. This lipid source can inhibit gastric emptying when reaching duodenum and, consequently, increasing the time that food stays inside the intestine (Honda et al. 2009HONDA K, KAMISOYAMA H, ISSHIKI Y & HASEGAWA. 2009. Effects of dietary fat levels on nutrient digestibility at different sites of chicken intestines. J Poult Sci 46: 291-295., Kim et al. 2013KIM JH, SEO S, KIM CH, KIM JW, LEE BB, LEE GI, SHIN HS, KIM MC & KIL DY. 2013. Effect of dietary supplementation of crude glycerol or tallow on intestinal transit time and utilization of energy and nutrients in diets fed to broiler chickens. Livest Sci 154: 165-168.), favoring the digestive enzymes actions and improving nutrients digestibility (Hu et al. 2018HU YD, LAN D, ZHU Y, PANG HZ, MU XP & HU XF. 2018. Effect of diets with different energy and lipase levels on performance, digestibility and carcass trait in broilers. Asian-Australas J Anim Sci 31: 1275-1284.). Mandalawia et al. (2017)MANDALAWIA HA, MALLOB JJ, MENOYOA D, LÁZAROA R & MATEOSA GG. 2017. Metabolizable energy content of traditional and re-esterifiedlipid sources: Effects of inclusion in the diet on nutrientretention and growth performance of broilers from 7 to21 days of age. Anim Feed Sci Tech 224: 124-135., observed that adding oils to broiler diet increased nutrient retention, possibly due to the lower rate of passage (Mateos et al. 1982MATEOS GG, VENDER JL & EASTWOOD JA. 1982. Rate of food passage (transit time) as influenced by level of supplemental fat. Poult Sci 61: 94-100.).

Another factor that may influence dry matter digestibility is the presence of minerals, Wilkinson et al. (2014)WILKINSON SJ, BRADBURY EJ, THOMSON PC, BEDFORD MR & COWIESON AJ. 2014. Nutritional geometry of calcium and phosphorus nutrition in broiler chicks. The effect of different dietary calcium and phosphorus concentrations and ratios on nutrient digestibility. Animal 8: 1080-1088., observed that increasing calcium supply (0.64 to 1.0%) is propitious to increase dry matter digestibility in broilers up to 22 days of age. Corroborating with the present study data, in which diets adjusted to 7.5% with about 0.88% of Ca, provided greater CDMS, when compared to diets without adjustments.

The effects of increasing ME and nutrient levels were also observed on DCCP, indicating that low-energy diets (2975 kcal/kg) without nutritional adjustments reduce the protein digestibility and, consequently, performance. Regarding DCGE, can be inferred that the better utilization of the energy components of the diets is related to the adjustment of lysine, that through ideal protein methodology, changed all the amino acids of the diets, being Gly and Ser one of them. According to Ospina-Rojas et al. (2013)OSPINA-ROJAS IC, MURAKAMI AE, OLIVEIRA CA & GUERRA AF. 2013. Supplemental glycine and threonine effects on performance, intestinal mucosa development, and nutrient utilization of growing broiler chickens. Poult Sci 92: 2724-2731., glycine promotes increase of dietary fat digestibility, which is mainly because it is a component of the bile salts (Moran 2014MORAN ET. 2014. Intestinal Events and Nutritional Dynamics Predispose Clostridium Perfringens Virulence in Broilers. Poult Sci 93: 3028-3036.).

Values found for AME of the diets showed the importance of correcting its ME, Chrystal et al. (2020)CHRYSTAL PV, MOSS AF, KHODDAMI A, NARANJO VD, SELLE PH & LIU SY. 2020. Effects of reduced crude protein levels, dietary electrolyte balance, and energy density on the performance of broiler chickens offered maize-based diets with evaluations of starch, protein, and amino acid metabolism. Poultr Sci 99: 1421-1431. infer that AME values tend to decrease when birds have low feed intake.

Although the increasing on adjustment of diet nutrients (Dig. Lys, Ca and AP) and respective ME levels, positively affected DCDM and DCCP, initial performance was not improved. As stated by Liu et al. (2017)LIU SY, CHRYSTAL PV, COWIESON AJ, TRUONG HH, MOSS AF & SELLE PH. 2017. The influence of the selection of macronutrients coupled with dietary energy density on the performance of broiler chickens, Plos One 12: e0185480., the energy level of a diet, which is obtained from starch, protein and lipids, influences weight gain and feed conversion. Nevertheless, digestibility and performance do not always walk hand-in-hand since the combination of higher levels of starch and protein, in certain diets, leads to better performance results, but not necessarily to better digestibility.

The performance results in growing and finishing phases suggest that the increasing energy density led to a decrease in feed intake. Studies have shown that increasing soybean oil inclusion levels in a diet may be the responsible factor for alterations in the feed passage and digestibility rates (Mateos et al. 1982MATEOS GG, VENDER JL & EASTWOOD JA. 1982. Rate of food passage (transit time) as influenced by level of supplemental fat. Poult Sci 61: 94-100.), and this may explain the lower feed intake of the birds fed with diets enriched with higher amounts of soybean oil. In this sense, enlarging energy density might have led to increased secretion of cholecystokinin, hormone that acts by inhibiting gastric emptying, when the food bolus reaches the duodenum (McDonald et al. 2010MCDONALD P, EDWARDS RA, GREENHALGH JF D, MORGAN CA, SINCLAIR LA & WILKSON RG. 2010. Animal Nutrition. 7th ed., London, UK: Prentice Hall, p. 692.). Chrystal et al. (2020)CHRYSTAL PV, MOSS AF, KHODDAMI A, NARANJO VD, SELLE PH & LIU SY. 2020. Effects of reduced crude protein levels, dietary electrolyte balance, and energy density on the performance of broiler chickens offered maize-based diets with evaluations of starch, protein, and amino acid metabolism. Poultr Sci 99: 1421-1431., analyzing different energy inclusion levels in broiler diets up to 42 days of age, observed that using 3071 kcal ME/kg reduced birds feed intake by up to 5.0%, compared to the diet with 2870 kcal ME/kg.

These alterations in intake interfered feed conversion ratio, which was improved by 0.036 points in the diets with the highest energy level and nutritionally adjusted. Similar results were observed by Hidalgo et al. (2004)HIDALGO MA, DOZIER WA, DAVIS AJ & GORDON RW. 2004. Live Performance and Meat Yield Responses of Broilers to Progressive Concentrations of Dietary Energy Maintained at a Constant Metabolizable Energy-to-Crude Protein Ratio. J Appl Poult Res 13: 319-327. and Saleh et al. (2004)SALEH EA, WALTKINS SE, WALDROUP AL & WALDROUP PW. 2004. Effects of dietary nutrient density on performance and carcass quality of male broilers grown for further processing. Int J Poult Sci 3: 1-10.. Baião & Lara (2005)BAIÃO NC & LARA LJC. 2005. Oil and Fat in Broiler Nutrition. Braz J Poult Sci 7: 129-141. stated that using oils and fats in diets, increases their palatability, reduces nutrient losses and improves feed conversion, besides other positive effects.

In conclusion, to improve broiler performance, it is essential to adjust digestible lysine, calcium and available phosphorus when the metabolizable energy content in the diet is increased from 3050 to 3200 kcal ME/kg. This will significantly improve dry matter and protein digestibility.

ACKNOWLEDGMENTS

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001, and to Conselho Nacional de Desenvolvimento Científico e Tecnológico – Brazil (CNPq). The authors have declared that no competing interests exist.

REFERENCES

  • ABDULLA N, LOH T, AKIT H, SAZILI A & FOO H. 2016. Effects of dietary oil sources and calcium: phosphorus levels on growth performance, gut morphology and apparent digestibility of broiler chickens. S Afr J Anim Sci 46: 42-53.
  • AFTAB U. 2019. Energy and amino acid requirements of broiler chickens: keeping pace with the genetic progress. World Poult Sci J 75: 1-8.
  • AOAC. 2012. AOAC official methods of analysis. 19th ed., Arlington: Association of Official Analytical Chemists.
  • BAIÃO NC & LARA LJC. 2005. Oil and Fat in Broiler Nutrition. Braz J Poult Sci 7: 129-141.
  • CHRYSTAL PV, MOSS AF, KHODDAMI A, NARANJO VD, SELLE PH & LIU SY. 2020. Effects of reduced crude protein levels, dietary electrolyte balance, and energy density on the performance of broiler chickens offered maize-based diets with evaluations of starch, protein, and amino acid metabolism. Poultr Sci 99: 1421-1431.
  • DOZIER WA, GEHRING CK & CORZO UMA. 2011. Apparent metabolizable energy needs of male and female broilers from 36 to 47 days of age. Poult Sci 90: 804-814.
  • HIDALGO MA, DOZIER WA, DAVIS AJ & GORDON RW. 2004. Live Performance and Meat Yield Responses of Broilers to Progressive Concentrations of Dietary Energy Maintained at a Constant Metabolizable Energy-to-Crude Protein Ratio. J Appl Poult Res 13: 319-327.
  • HU YD, LAN D, ZHU Y, PANG HZ, MU XP & HU XF. 2018. Effect of diets with different energy and lipase levels on performance, digestibility and carcass trait in broilers. Asian-Australas J Anim Sci 31: 1275-1284.
  • HONDA K, KAMISOYAMA H, ISSHIKI Y & HASEGAWA. 2009. Effects of dietary fat levels on nutrient digestibility at different sites of chicken intestines. J Poult Sci 46: 291-295.
  • KAROMY AS, HABIB HN & KASIM SA. 2019. Influence of Different Levels of Crude Protein and Metabolizable Energy on Production Performance of Ross Broiler. J Biol Agric Health 9: 20-24.
  • KIM JH, SEO S, KIM CH, KIM JW, LEE BB, LEE GI, SHIN HS, KIM MC & KIL DY. 2013. Effect of dietary supplementation of crude glycerol or tallow on intestinal transit time and utilization of energy and nutrients in diets fed to broiler chickens. Livest Sci 154: 165-168.
  • LEESON S & SUMMERS JD. 2001. Nutrition of the chicken. 4th ed., Guelph: University Books, 413 p.
  • LIU SY, CHRYSTAL PV, COWIESON AJ, TRUONG HH, MOSS AF & SELLE PH. 2017. The influence of the selection of macronutrients coupled with dietary energy density on the performance of broiler chickens, Plos One 12: e0185480.
  • MATEOS GG, VENDER JL & EASTWOOD JA. 1982. Rate of food passage (transit time) as influenced by level of supplemental fat. Poult Sci 61: 94-100.
  • MANDALAWIA HA, MALLOB JJ, MENOYOA D, LÁZAROA R & MATEOSA GG. 2017. Metabolizable energy content of traditional and re-esterifiedlipid sources: Effects of inclusion in the diet on nutrientretention and growth performance of broilers from 7 to21 days of age. Anim Feed Sci Tech 224: 124-135.
  • MCDONALD P, EDWARDS RA, GREENHALGH JF D, MORGAN CA, SINCLAIR LA & WILKSON RG. 2010. Animal Nutrition. 7th ed., London, UK: Prentice Hall, p. 692.
  • MORAN ET. 2014. Intestinal Events and Nutritional Dynamics Predispose Clostridium Perfringens Virulence in Broilers. Poult Sci 93: 3028-3036.
  • OSPINA-ROJAS IC, MURAKAMI AE, OLIVEIRA CA & GUERRA AF. 2013. Supplemental glycine and threonine effects on performance, intestinal mucosa development, and nutrient utilization of growing broiler chickens. Poult Sci 92: 2724-2731.
  • ROSTAGNO HS, ALBINO LFT, DONZELE JL, GOMES PC, OLIVEIRA RF, LOPES DC, FERREIRA AS, BARRETO SLT & EUCLIDES RF. 2011. Tabelas Brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. 3nd ed. Minas Gerais: Viçosa, p. 252.
  • SAKOMURA NK & ROSTAGNO HS. 2016. Métodos de pesquisa em nutrição de monogátricos. 2nd ed., Jaboticabal: Funep, p. 262.
  • SALEH EA, WALTKINS SE, WALDROUP AL & WALDROUP PW. 2004. Effects of dietary nutrient density on performance and carcass quality of male broilers grown for further processing. Int J Poult Sci 3: 1-10.
  • SHAFEY TM, MCDONALD MW & PYM RA. 1990. Effects of dietary calcium, available phosphorus and vitamin D on growth rate, food utilisation, plasma and boné constituents and calcium and phosphorus retention of comercial broiler strains. Bras Poult Sci 31: 587-602.
  • SAYED RE, IBRAHIM D & SAID EN. 2017. Effect of dietary calorie and protein content on performance, behaviour, expression of some growth-related genes and economic of broiler chickens. Zagazig Vet J 45: 326-339.
  • WILKINSON SJ, BRADBURY EJ, THOMSON PC, BEDFORD MR & COWIESON AJ. 2014. Nutritional geometry of calcium and phosphorus nutrition in broiler chicks. The effect of different dietary calcium and phosphorus concentrations and ratios on nutrient digestibility. Animal 8: 1080-1088.

Publication Dates

  • Publication in this collection
    18 Sept 2023
  • Date of issue
    2023

History

  • Received
    13 Nov 2019
  • Accepted
    16 May 2020
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