Digestible Threonine Levels in the Starter Diet of Broilers Derived from Breeders of Different Ages

ABSTRACT

The aim of this study was to evaluate the effect of digestible threonine supplementation in the starter diet on the performance, intestinal parameters, and nutrient metabolism of broilers derived from breeders of different ages. In total, 480 one-day-old Cobb chicks, derived from 38-or 49-week-oldbreeders, were housed in experimental battery cages until 21 days of age and fed four different threonine levels (800, 900, 1,000, or 1,100 mg/kg) in the starter feed. A completely randomized experimental design in a 2x4 factorial arrangement (breeder age x threonine levels) was applied, totaling eight treatments with five replicates of 12 birds each. Broilers from older breeders fed 800 mg digestible threonine/kg of diet presented higher weight gain, with a positive linear effect. There was also an interaction between breeder age and threonine levels for the weight gain of 21-d-old broilers supplemented at maximum level of 1,003 mg Thr/kg diet during the starter phase. There was no effect of breeder age or threonine levels on nutrient metabolism during the period of 17-21 days. There was no influence of breeder age or threonine levels in the starter diet on intestinal morphometric measurements, absorption area, or percentage of goblet cells.

Keywords:
Development; metabolism; nutrition; poultry.

INTRODUCTION

Breeder age can influence egg quality, composition and size, which determine the availability of nutrients to the chick during the post-hatching period (Reis et al., 1997; Vieira & Moran Jr., 1999). Older breeders lay larger eggs, with greater yolk and albumen contents, compared with younger ones (Peebles, 2004; Tona et al., 2004).

The development of the digestive tract during the first week of life of broilers is also essential for the expression of their maximum genetic potential to allow reaching optimal market weight in the shortest possible period of time (Nitsan, 1995). Therefore, any limitations during the transition period between embryonic and free life may impair the performance of broiler strains selected for rapid growth (Almeida, 2003).

Protein and amino acids perform several functions in the body, including tissue synthesis and maintenance (Alleman et al., 2000). Therefore, broiler feeds must be formulated to supply sufficient aminoacids and protein for synthesis; however, any crude protein excesses may reduce efficiency of amino acid utilization and increase the requirements of essential amino acids (Sklan & Plavnik, 2002).

Threonine is the third limiting amino acid for broilers after methionine and lysine in diets based on corn and soybean meal (Fernandezet al., 1994; Berreset al., 2007). It is a critical factor in least-cost formulations, and its supplementation allows reducing dietary crude protein levels, thereby contributing to reduce uric acid and water excretion, which consequently decreases nitrogen excretion in the environment (Kidd et al., 2002; Kiddet al., 2005). Threonine is required for body protein synthesis and feather renewal, body maintenance, and collagen and elastin synthesis (Fernandez et al., 1994; Sá et al., 2007). It is also found in the gastrointestinal epithelium (mucosal cells, mucus, and digestive enzymes) and as a component of immunoglobulin molecules (Wu, 1998; Ojano-Dirain & Waldroup, 2002).

The threonine requirement for maintenance is high relative to the other amino acids due to its high content in endogenous intestinal secretions (Fernandez et al., 1994). Faure et al. (2005) conducted experiments in rats and reported that dietary threonine restriction impairs the synthesis of mucins in all segments of the small intestine, with up to 40% loss in the duodenum.

Ammerman et al. (1995) studied threonine digestibility in poultry and concluded that it can range up to 29% among different feedstuffs, and its bioavailability is 89% in soybean meal, 84% in corn, 81% in sorghum, and 100% in L-threonine. The recommendation for digestible threonine for male broilers in the starter phase found by Rostagno et al. (2011) is 0,763%/3.000 kcal of metabolizable energy.

In the present study, we aimed at evaluating the effect of four different threonine levels in the starter diet (1-21 days of age) of broilers derived from breeders of two different ages on broiler growth performance, nutrient metabolism, and intestinal development parameters.

MATERIALS AND METHODS

The experiment was carried out in the facilities of the Federal University of Goiás (UFG), Goiânia, Brazil. All animal care procedures were approved before the start of the experiment by the UFG Ethics Committee in Research (protocol 15346/2012) and were in accordance with the Ethical Principles in Animal Experimentation adopted by the Brazilian Society for Laboratory Animal Science (SBCAL).

In total, 480 one-day-old Cobb male chicks derived from 38- or 49-week-old breeders were fed different starter diets containing four different threonine levels(800, 900, 1,000, or 1,100 mg/kg). A completely randomized experimental design in a 2x4 factorial arrangement (breeder age x threonine levels) was applied, totaling eight treatments with five replicates of 12 birds each. Feeds were based on corn and soybean meal, and formulated to contain equal nutrient and energy levels, according to the nutritional requirement recommendations and feedstuff composition proposed byRostagno et al. (2005) (Table 1). The increasing threonine levels of the experimental diets were obtained by supplementing the basal diet with L-threonine at the expense of ground corn.

Table 1
Ingredients and nutritional composition of the experimental starter basal diet supplemented with threonine.

Ingredients	Starter diet (kg)
Corn	61.96
Soybean meal	31.31
Soybean oil	1.83
Dicalcium phosphate	1.00
Calcitic limestone	0.84
Salt	0.44
Vitamin-trace mineral supplement*	0.50
Corn flour	1.00
L-Lysine HCL	0.67
DL-Methionine	0.30
L-Threonine	0.15
Total	100.00
Calculated nutritional composition
Crude Protein (%)	20.50
Metabolizable energy (kcal/kg)	3.000
Calcium (%)	0.899
Available phosphorus (%)	0.449
Digestible Lysine (%)	1.434
Digestible Arginine (%)	1.210
Digestible Methionine (%)	0.576
Digestible Methionine + Cystine (%)	0.921
Digestible Tryptophan (%)	0.217
Digestible Threonine (%)	0.800
Digestible Valine (%)	0.809
Sodium (%)	0.218

• ^*
  Composition/kg of feed: vitamin supplement for broilers - starter phase: vit. A - 3,125,000 IU; vit. D3 - 550,000 IU; vit. E - 3750 mg; vit. K3 - 625 mg; vit. B1 - 250 mg; vit. B2 - 1,125 mg; vit. B6 - 250 mg; vit. B12 - 3,750 mg; niacin - 9,500 mg; calcium pantothenate , 3,750 mg; folic acid - 125 mg; DL-methionine - 350,000 mg; choline chloride 50% - 150,000 mg; growth promoter - 12,500 mg; coccidiostat - 15,000 mg; Se - 50 mg; antioxidant - 2,500 mg; q.s.p. vehicle 1000 g, Mineral supplement: Fe - 100,000 mg; Cu - 16,000 mg; Zn - 100,000 mg; I - 1,500 mg.

Chicks were reared in cages until 21 days of age, with feed and water ad libitum. A program continuous light was used, providing 24 hour light. Birds and feed residues were weighed on days 4, 7, 10, 14 and 21. Weight gain (calculated as the difference between live weight at the end of each period and the initial weight at housing), feed intake (per period) and feed conversion ratio (calculated by dividing the total feed intake by weight gain, corrected for the weight of dead chicks) were calculated.

A metabolism assay was conducted when broilers were between 17 to 21 days of age, using the method of total excreta collection. The objective was to determine the coefficient of metabolization of dry matter (CMDM), nitrogen balance (NB), the coefficient of nitrogen metabolization (CNM), dry matter retention (DMR), and nitrogen retention (NR), according to Silva (1990). Excreta were collected twice daily, samples were placed in plastic bags duly identified per treatment and replicate, and frozen until analysis.

For the histomorphometric analysis of the digestive system, five broilers per treatment were sacrificed by cervical dislocation on days 7, 14, 21, and 28 days of age, after six hours of fasting. Three-inch segments of the duodenum, jejunum, and ileum were collected, opened by the mesenteric border, stretched by the serous tunic, washed in saline solution, and fixed in formalin at 10% for 24 hours. The tissues were washed under running distilled water, and dehydrated in increasing concentrations of alcohol (70-95%). Two changes of absolute alcohol 75% were performed within an interval of one hour each, and the intestinal fragments were embedded in paraffin at 58°C. After setting, the paraffin blocks were cut in five-micrometer slices. The sections were fixed on slides and stained by PAS technique (Luna, 1968).

Slides for histological evaluation were examined under light field optical microscope (Carl Zeiss model Juvenal) coupled to an Axio Vision 3.0 (Zeiss) image analyzing system. The captured images were further investigated by Image J software, where 40 villus height (magnification 3.2x) and crypt depth (10x magnification) measures of each intestinal segment were performed (Figures 1 and 2). Villus height was measured from the base to the tip of the villi, and crypt depth from the base of the crypt to the transition region to the villus (Fukayamaet al., 2005). Villus to crypt ratio was calculated by dividing villus height by crypt depth.

Intestinal absorption area was calculated by measuring total villus height and width, and crypt width, with 10 readings per histological slide. All indices were analyzed using Image J software. The absorption surface area was estimated using the equation proposed by Kisielinski et al. (2002) as: M= [( (Wv x Lv) + (Wv/2 + Wc/2)² - (Wv/2)²⁾ / (Wv/2 + Wc/2)² ], where: M = Number of times the surface of the intestinal mucosa is increased; Wv = average villus width; Lv = average villus length; and Wc = average crypt width.

Images of the intestinal mucosa were used to obtain the percentage of goblet cells in the same slides used for histomorphometry. In each slide, 10 villus sections from the duodenum, jejunum and ileum were analyzed at 10x magnification. The images were segmented by the Image J(r) program, in which the areas marked as goblet cells were highlighted. A quantitative analysis of goblet cells along the crypt and villus fragments was conducted. Measured areas were marked and cut in the region where there were only goblet cells, and their percentage was calculated.

Data were analyzed using the Statistical Analysis System SAS^(r) software (Statistical Analysis System, Cary, NC, USA) using analysis of variance (GLM) and average comparison by Tukey test with a significance level of 5%.When necessary, data were submitted to polynomial regression.

RESULTS AND DISCUSSION

Feed intake, feed conversion ratio, and body weight were not influenced by the treatments (p>0.05). It is known that breeder age affects egg weight, quality, and composition and, consequently, chick weight (Wilson, 1991; Almeida et al., 2003; Rocha et al., 2008), suggesting that chicks derived from eggs laid by older breeders have more nutrients available, and therefore, those birds present better performance during the starter phase than those derived from younger breeders (Table 2).

Table 2
Statistical probability of the effects of breeder age (BA) and dietary digestible threonine levels (Thr; mg/ kg diet) on the feed intake (FI), weight gain (WG), feed conversion ratio (FCR) and body weight (BW) of 14-d-old broilers.

Treatments	FI(g/chick)	WG (g/chick)	FCR (g/g)	BW (g)
BA	0.52	<0.05	0.31	0.42
Thr	0.32	<0.05	0.22	0.38
Thr x BA	0.24	<0.05	0.18	0.26
CV (%)	4.83	3.79	4.85	3.46

• Different letters in the same column differ (p <0.05) by Tukey's test (5%) CV - coefficient of variation

The lowest digestible threonine level (800 mg/kg) was sufficient to meet the broiler's maintenance requirements. Stringhiniet al. (2003) found that chick average weight at hatch influenced feed intake up to 21 days of age, but this relationship was not observed at 35 and 42 days. Higher threonine levels did not to activate the mechanisms regulating the appetite of broilers or changed the plasma amino acid profile or balance (Harper, 1970). Therefore, the brain mechanism that is sensitive to variations in amino acid blood levels and that reduces feed intake (Bertechini, 2012) was probably not stimulated in the current experiment.

The significant interaction between breeder age and digestible threonine dietary levels showed that the addition of digestible threonine in the diet of broilers derived from young breeders had a positive linear effect on weight gain (p<0.05) determined on day 14, with the level of 1,000mg/kg yielding the best results (Table 3). Broilers derived from the older breeders also tended to present higher weight gain when supplemented with 1,000mg/kg. Abassi et al.(2014) recommended feeding broilers after 12 days of age with at least 10% higher threonine levels than those recommended by the strain's manual to increase weight gain.

Table 3
Effect of the interaction between breeder age and digestible threonine levels (mg/kg) in the starter diet on the weight gain of 14-d-old broilers.

Breeder age (weeks)	800mg/kg	900mg/kg	1,000 mg/kg	1,100mg/kg	P (%)	CV (%)
38	367.08B	398.98	419.96	416.78	<0.051	4.83
49	414.98A	413.10	415.24	411.76	0.66	4.35

• Different letters in the same column differ by Tukey's test (5%)¹Y= 239.124 + 0.1700080x / R² = 0.82 CV- coefficient of variation; P - statiscal probability

Feed conversion ratio and feed intake of 21-d-old broilers were not influenced by the treatments (p>0.05; Table 4).

Table 4
Statistical probability of the effects of breeder age (BA) and dietary digestible threonine levels (Thr; mg/kg diet) on the feed intake (FI), weight gain (WG), feed conversion ratio (FCR) and body weight (BW) of 21-d-old broilers.

Treatments	FI (g/bird)	WG (g/bird)	FCR (g/g)	BW (g)
BA	0.34	<0.05	0.19	0.71
Thr	0.22	<0.05	0.66	0.54
Thr x BA	0.51	<0.05	0.32	0.48
CV (%)	5.27	5.98	6.13	6.57

• CV - coefficient of variation

The interaction between breeder age and digestible threonine levels had a quadratic effect on weight gain (Table 5), with a peak at 1,003 mg digestible threonine/kg of diet. Chickens from younger breeders presented higher weight gain when fed 1,000 mg digestible threonine/kg diet. Thus, higher digestible threonine levels than those used for the formulation of experimental diets proposed by Rostagno et al. (2005), of 800 mg digestible threonine/kg of diet, are recommended. The results of the present experiment do not agree with those of Reginatto et al. (2000), who found no effect of dietary threonine on broiler weight gain, feed intake, or feed conversion ratio, independently of dietary energy level.

Table 5
Effect of the interaction between breeder age and digestible threonine levels (mg/kg) in the starter diet on the weight gain of 21-d-old broilers.

Breeder Age	800 mg/kg	900mg/kg	1,000mg/kg	1,100mg/kg	P (%)	CV (%)
38	682.98	714.08	773.66 A	735.08	<0.051	5.29
49	719.68	749.00	681.64 B	718.66	0.34	6.81

• Different letters in the same column differ (p<0.05) by Tukey's test (5%).
• ¹Y= -1,029.02 + 3.52568x - 0.00170080x²; R² = 0.82;Maximum= 1,003 mg.
• CV - coefficient of variation. p - statiscal probability

There was no effect (p>0.05) of breeder age or digestible threonine levels on any variable evaluated in the metabolism assay conducted during the starter phase (Table 6). It is noteworthy that all the amino acids that exceed maintenance and production requirements are catabolized, thereby reducing nitrogen retention and increasing the losses of nutrients that were not digested and utilized by the metabolism (Bertechini, 2012).

Table 6
Metabolism of nutrients in diets supplemented with increasing digestible threonine levels (Thr; mg/kg of feed) fed to broilers derived from breeders of two different ages (BA) during the period of 17-21 days of age.

Treatments	CMDM (%)	NB (g)	CNM (%)	DMR (g/kg BW)	NR (g/kg BW)
BA	0.23	0.44	0.38	0.55	0.37
Thr	0.42	0.39	0.71	0.39	0.51
Thr x BA	0.33	0.30	0.50	0.43	0.49
CV (%)	6.62	31.84	11.09	29.48	32.46

• CMDM: coefficient of metabolization of dry matter; NB: nitrogen balance; CNM: coefficient of nitrogen metabolization; DMR: dry matter retention; NR: nitrogen retention; BW: body weight. CV - coefficient of variation.

There was no effect of breeder age or digestible dietary threonine levels (p>0.05) on villus height, crypt depth, or villus:crypt ratio as measured in 14- and 21-d-old broilers (Tables 7 and 8).

Table 7
Statistical probability of the effects of breeder age (BA) and dietary digestible threonine levels (Thr; mg/kg diet) on villus height (V; µm), crypt depth (H; µm), and villus:crypt ratio (V:C) in the duodenum, jejunum, and ileum of 14-d-old broilers.

Treatments		Duodenum			Jejunum			Ileum
	V	C	V:C	V	C	V:C	V	C	V:C
BA	0.47	0.66	0.41	0.52	0.61	0.49	0.32	0.48	0.50
Thr	0.51	0.52	00.39	0.42	0.49	0.38	0.61	0.44	0.66
Thr x BA	0.39	0.41	00.59	0.32	0.38	0.39	0.33	0.39	0.41
CV (%)	8.01	90.56	9.23	7.41	9.16	8.92	9.57	11.03	10.84

• CV - coefficient of variation

Table 8
Statistical probability of the effects of breeder age (BA) and dietary digestible threonine levels (Thr; mg/kg diet) on villus height (V; µm), crypt depth (H; µm), and villus:crypt ratio (V:C) in the duodenum, jejunum, and ileum of 21-d-old broilers.

Treatments		Duodenum			Jejunum			Ileum
	V	C	V:C	V	C	V:C	V	C	V:C
BA	0.32	0.29	0.41	0.33	0.40	0.38	0.41	0.28	0.47
Thr	0.33	0.38	0.55	0.45	0.35	0.51	0.39	0.32	0.50
Thr x BA	0.66	0.71	0.59	0.58	0.71	0.63	0.50	0.51	0.69
CV (%)	10.01	10.56	10.65	9.56	8.16	9.02	8.56	8.95	9.09

• CV - coefficient of variation

Geyra et al. (2001) emphasized that crypt development influences the maintenance of crypt-cell turnover rates and intestinal maturation; therefore, the deeper the crypt, the greater the villus growth in the enterocyte, consequently maximizing intestinal absorption surface area. The similar villus heights and crypt depths measured in the intestinal segments among treatments confirm that there were no digestion and intestinal absorption improvements in the early stages of development. According to Yamauchi & Ishiki (1991), villus density is different in the various intestinal segments (duodenum, jejunum and ileum), and the number of villi is reduced when broilers are 10 days old. Those researchers concluded that this does not imply in lower absorption capacity, but in further development of the villi, and therefore, the number of villi/area is reduced with age.

The absorption area of the intestinal segments of broilers during the starter phase was not affected by dietary digestible threonine levels or breeder age (p <0.05;Table 9).

Table 9
Statistical probability of the effects of breeder age (BA) and dietary digestible threonine levels (Thr; mg/kg diet) on the absorption surface area (μm²) of the duodenum, jejunum, and ileum of 14- and 21-d-old broilers.

Treatments				Absorption surface area
	Duodenum (µm)			Jejunum (µm)				Ileum (µm)
	14 days	21 days	14 days	21 days	14 days	21 days
BA	0.46	0.44	0.56	0.52	0.49	0.61
Thr	0.55	0.33	0.41	0.60	0.59	0.69
Thr x BA	0.60	0.52	0.48	0.66	0.70	0.77
CV (%)	17.85	16.55	18.01	17.54	17.30	18.74

• CV - coefficient of variation.

Moreover, there was no influence of breeder age or digestible threonine levels on goblet cell counts in the duodenum, jejunum, or ileum (p>0.05; Table 10). These findings are not consistent with those reported by Abassi et al.(2014), who showed that the jejunal histological changes observed in broilers fed increasing dietary threonine levels (100, 110, and 120%)promotes an increase in intestinal absorption surface area during the starter, grower, and finisher phases. Those authors reported that threonine influenced the number of structures, intestinal functions, and the number of goblet cells of broilers. In the digestive tract of poultry, morphological changes, such as increased length, height, and density of the intestinal villi, as well as higher physiological capacity, enhance nutrient digestion and absorption (Maiorkaet al., 2002). Maiorka et al. (2003) stated that the absorption capacity of any intestinal segment is directly proportional to the number of villi present, villus size, and surface area available for absorption.

Table 10
Statistical probability of the effects of breeder age (BA) and dietary threonine levels (Thr; mg/kg diet) on goblet cell counts (%) in the duodenum, jejunum, and ileum of 14- and 21-d-old broilers.

Treatments			Globet Cells
	Duodenum (%)		Jejunum (%)			Ileum (%)
	14 days	21 days	14 days	21 days	14 days	21 days
BA	0.64	0.55	0.51	0.60	0.71	0.80
Thr	0.62	0.66	0.42	0.52	0.51	0.70
Thr x BA	0.55	0.59	0.47	0.72	0.61	0.74
CV (%)	29.74	28.63	30.52	27.24	29.81	28.93

• CV - coefficient of variation

CONCLUSION

The best performance results were obtained when broilers derived from young breeders were fed 1,000 mg digestible threonine/kg of diet and when those derived from older breeders were fed 800 mg digestible threonine/kg of diet. Digestible threonine dietary levels and breeder age did not affect nutrient metabolism or promoted any morphological changes in the intestinal mucosa during the starter phase.

REFERENCES

• Abassi MA, Mahdavi AH, Samie AH, Jahanian R. Effects of Different Levels of Dietary Crude Protein and Threonine on Performance, Humoral Immune Responses and Intestinal Morphology of Broiler Chicks. Brazilian Journal of Poultry Science 2014;16(1):35-44.
• Alleman F, Michel J, Chagneau AM, Leclercq B. The effects of dietary protein independent of essential amino acids on growth and body composition in genetically lean and fat chickens. British Poultry Science 2000;41:214-218.
• Almeida JG, Faria Filho de, Dahlke F, Maiorka A, Macari M, Furlan RL. Efeito da idade da matriz e do tempo de jejum entre o nascimento e o alojamento sobre a absorção do saco vitelino. Revista Brasileira de Ciência Avícola 2003;5:93.
• Ammerman CB, Baker DH, Lewis AJ. Bioavalability of nutrients for animals. San Diego: Academic Press; 1995.
• Berres J, Vieira SL, Coneglian JLB, Olmos AR, Freitas DM, Bortolini TCK, et al. Respostas de frangos de corte a aumentos graduais na relação entre treonina e lisina. Ciência Rural 2007; 37(2):510-517.
• Bertechini AG. Nutrição de monogástricos. 2ª ed. Lavras: UFLA; 2012.
• Faure M, Moennoz D, Montigon F, Mettraux C, Breuille D, Ballevre O. Dietary threonine restriction specifically reduces intestinal mucin synthesis in rats. Journal of Nutrition 2005;135:486-491.
• Fernandez RS, Aoyagi S, Han Y, Parsons CM, Baker DH. Limiting order to amino acids in corn and soybean meal for growth of the chick. Poultry Science 1994;73:1887-1889.
• Fukayama EH, Bertechini AG, Geraldo A, Kato RK, Murgas LDS. Extrato de orégano como aditivo em rações para frangos de corte.Revista Brasileira de Zootecnia 2005;34(6):2316-2326.
• Han Y, Suzuki H, Parsons CM, Baker DH. Amino acid fortification of a low protein corn-soybean meal diet for maximal weight gain and feed efficiency of chicks. Poultry Science1992;71:1168-1178.
• Geyra A, Uni Z, Sklan D. The effect of fasting at different ages on growth and tissues dynamics in the small intestine of the young chick. British Journal of Nutrition2001;86(1):53-61.
• Harper AE, Benevenga NJ, Wohlhueter RM. Effects of ingestion of disproportionate amounts of amino acids. Phsiological Reviews 1970;50(4):428-547.
• Kidd MT, Zumwalt CD, Chamblee DW, Carden ML, Burnham DJ. Broiler growth and carcass responses to diets containing L-threonine versus diets containing threonine from intact protein sources. Journal of Applied Poultry Research 2002;11:83-89.
• Kidd, MT, Virden, WS, Corzo A, Dozier WA, Burnham DJ. Amino acid density and L-Threonine responses in Ross Broilers. International Journal of Poultry Science2005;4(5):258-262.
• Kisielinski K, Willis S, Prescher A, Klosterhalfen B, Schumpelick V. A simple new method to calculate small intestine absorptive surface in the rat. Clinical and Experimental Medicine 2002;2:131-135.
• Luna LG. Manual of histologic staining methods of the armed forces institute of pathology. 3ªed. New York: McGraw-Hill; 1968.
• Maiorka A, Boleli IC,. Macari M desenvolvimento e reparo da mucosa intestinal. In:, Macari MFurlan RL, Gonzáles E. Fisiologia aviária aplicada a frangos de corte. 2ªed. Jaboticabal: FUNEP/UNESP; 2002. p.113-124.
• Maiorka A, Santin E, Dahlke F, Boleli IC, Furlan RL,. Macari M Posthatching water and feed deprivation affect gastrointestinal tract and intestinal mucosa development of broiler chicks. Journal of Applied Poultry Research2003;12:483-492.
• Nitsan Z. The development of digestive tract in posthatched chicks. Poultry Science1995;10:21-28.
• Ojano-Dirain CP, Waldroup PW. Evaluation of lysine, methionine and threonine needs of broilers three to six week of age under moderate temperature stress. Journal of Poultry Science2002;1(1):16-21.
• Peebles ED, Keirs RW, Benett LW, Cummings TS, Whitmarsh SK, Gerard, PD. Relationships among Post-Hatch Physiological Parameters in Broiler Chicks Hatched from Young Breeders Hens and Subjected to Delayed Brooding Placement. International Journal of Poultry Science2004;3(9):578-585.
• Rocha JSR, Lara LJC, Baião NC, Cançado SV, Baião LEC, Silva TR. Efeito da classificação dos ovos sobre o rendimento de incubação e os pesos do pinto e do saco vitelino. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 2008;60(4):979-986.
• Reginatto MF, Ribeiro AMF, Penz Jr AM, Kessler AM, Krabe ELL. Suplementação de treonina em dietas de frangos de corte, variando a energia e as relações energia: proteína. Revista Brasileira de Ciência Avícola2000;2(3):239-247.
• Reis LH, Gama LT, Chaveiro Soares M. Effects of short storage conditions and broiler breeder age on hatchability, hatching time, and chick weights. Poultry Science1997;76:1459-1466.
• Rostagno HS, Albino IFT, Donzele JL, Gomes PC, Oliveira RF, Lopes DC, et al. Tabelas brasileiras para aves e suínos: composição de alimentos e exigências nutricionais. Viçosa: Editora UFV; 2005.
• Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RF, Lopes DC, et al. Composição de alimentos e exigências nutricionais de aves e suínos (Tabelas Brasileiras). Viçosa: UFV; 2011.
• Sá LM, Gomes PC, Cecon PR, Rostagno HS, D'agostini P. Exigência nutricional de treonina digestível para galinhas poedeiras no período de 34 a 50 semanas de idade. Revista Brasileira de Zootecnia2007;36(6):1846-1853.
• Sampaio IBM. Estatística aplicada à experimentação animal. 2ªed. Belo Horizonte: FEPMVZ; 2002.
• Silva D.J. Análise de alimentos (métodos químicos e biológicos).; Viçosa: UFV 1990.
• Sklan D, Plavnik I. Interactions between dietary crude protein and essential amino acid intake on performance in broilers. British Poultry Science 2002;43:442-449.
• Star L, Rovers M, Corrent E, Van der Klis JD. Threonine requeriment of broiler ckickens during subclinical intestinal clostridium infection. Poultry Science2012;91:643-652.
• Stringhini JH, Resende A, Café MB, Leandro NSM, Andrade MA. Efeito do peso inicial e do período de fornecimento da dieta pré-inicial sobre o desempenho de frangos de corte. Revista Brasileira de Zootecnia2003;32:353-360.
• Tona K, Onagbesan O, De Ketelaere B, Decuypere E, Bruggeman V. Effects of age of broiler breeders and egg storage on egg quality, hatchability, chick quality, chick weight, and chick posthatch growth to forty-two days. The Journal of Applied Poultry Research2004;13:10-18.
• Vieira SL, Moran Jr ET. Effects of egg and chick post-hatch nutrition on broiler live performance and meat yields. World's Poultry ScienceJournal 1999;55:125-142.
• Wilson HR. Interrelationships of egg size, chick size, post hatching growth and hatchability. World´s poultry of Science Journal 1991;47:5-20.
• Wu G. Intestinal mucosal amino acid catabolism. Journal of Nutrition1998;128:1249-1252.
• Yamauchi KE, Ishiki Y. Scanning electron microscopic observations on the intestinal villi in growing white leghorn and broiler chickens from 1 to 30 days of age. British Poultry Science 1991;32:67-78.

• Experiment conducted with CNPq financial support - Process n. 477385/2010

Publication Dates

• Publication in this collection
  Oct-Dec 2015

History

• Received
  Oct 2014
• Accepted
  June 2015