INTRODUCTION
Soybean meal (SBM) is a prominent protein source in poultry diets and has been included in feed to prevent amino acid (AA) deficiency. However, the price of SBM is expected to soar as climate change disrupts production [1], even as the SBM demand increases alongside broiler meat and egg production [2]. In addition, excessive SBM in diets increases the excretion of nitrogen (N) that is not utilized by animals. The N from excreta is a primary source of environmental pollution in animal production related to land, water, and air contamination [3]. Therefore, low protein (LP) diets supplemented with crystalline AA, reducing SBM use in broiler diets, may contribute to both feed cost reduction and the environmental sustainability of poultry production.
In most cases, crystalline AA supplemented in an LP diet is indispensable AA to meet requirements, although dietary levels of dispensable AA also decrease as SBM dietary concentration decreases. Therefore, specific dispensable AA may be deficient in the LP diet and need to be supplemented to match the growth performance of a standard diet [4]. In previous studies, Hilliar et al. [5] reported that glycine (Gly) supplementation in an 18.5% crude protein (CP) diet improved body weight gain (BWG) and feed conversion ratio compared to an 18.5% CP diet without Gly supplementation. Hofmann et al. [6] reported that a 16% CP diet supplemented with Gly and glutamic acid (Glu) improved growth performance compared to a 16% CP diet without dispensable AA supplementation but had a lower growth performance than the 18% CP diet. However, Hussein et al. [7] illustrated that supplementing Glu in an LP diet did not affect growth performance. These inconsistent results indicate that effects of supplementing dispensable AA in the LP diets require further research for clarification. Therefore, the objective of the present study was to investigate the effects of supplementing indispensable AA as well as dispensable AA on growth performance and N excretion in LP diets.
MATERIALS AND METHODS
The protocols for this study were reviewed and approved by the Institutional Animal Care and Use Committee at Kyungpook National University (KNU 2021-0212).
Animals and management
A total of 175 day-old Ross 308 male broilers were housed in battery cages (60 cm length × 50 cm width × 60 cm height) and were fed a standard commercial pre-starter broiler diet (21% CP and 12.55 MJ/kg AMEn) for a 7-day pre-experimental period. On day 7, all birds were individually weighed and allocated to seven dietary treatments with five replicate cages in a randomized complete block design based on body weight (BW). From day 21 to 28, all birds were fed a standard broiler finisher diet (18% CP and 13.18 MJ/kg AMEn). All birds had ad libitum access to water and feed in an environmentally controlled room, with room temperature maintained at 33℃ for the first three days, then gradually decreased by 3℃ weekly to reach 24℃ by day 28.
Dietary treatments
Experimental diets consisted of seven diets, including one control diet and six LP diets (Table 1). The control diet was formulated to contain 20% CP, and two LP diets were prepared to contain 18.5% and 17.0% CP without crystalline AA supplementation. The other two LP diets were supplemented with indispensable AA, including arginine, histidine, leucine, lysine, methionine, cysteine, phenylalanine, threonine, tryptophan, and valine (11 AA), to meet indispensable AA requirements for broilers. The remaining two LP diets were supplemented with 11 AA, Glu, and Gly (13 AA) to investigate the effect of dispensable AA supplementation. The inclusion levels of Glu and Gly in the two LP diets with 13 AA were maintained at a constant ratio of 4:1 to achieve similar contents as the control diet. Analyzed CP and AA compositions in the experimental diets are presented in Table 2. The control diet and the LP diets, except for LP diets without crystalline AA, were formulated to meet nutrient and AA requirements based on standardized ileal digestible AA according to Hoehler et al. [8] and Aviagen [9] during the grower phase. All experimental diets included 0.5% chromium oxide as an indigestible index for calculating N excretion.
Table 1. Ingredient and chemical composition of the experimental diets
1)LP diet was not supplemented with AA, and overall AA were 14.5 % and 21.7% less compared to requirements in 18.5% CP and 17.0% CP diet, respectively.
2)LP diets supplemented with 11 AA (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, valine, and cysteine) were formulated to meet requirement. LP diets with 13 AA were obtained by supplementing glutamic acid and glycine to LP diets supplemented with 11 AA at the expense of corn-starch.
3)Supplies the following quantities per kilogram of diet: vitamin A, 31,500 IU; vitamin D3, 12,500 IU; vitamin E, 175 mg; vitamin K3, 8.75 mg; vitamin B1, 10 mg; vitamin B2, 30 mg; B5, 75 mg; vitamin B6 15 mg; vitamin B12, 0.065 mg; folic acid, 7.5 mg; niacin, 12 mg; biotin, 0.5 mg; proviox50, 10 mg.
4)Supplies the following quantities per kilogram of diet: Fe, 250 mg; Cu, 85 mg; Zn, 460 mg; Mn, 5,000 mg; Co, 0.75 mg; Se, 1.5 mg; I, 7.5 mg.
CP, crude protein; LP, low protein; AA, amino acid; AME, apparent metabolizable energy; P, phosphorus; SID, standardized ileal digestible.
Table 2. Analyzed crude protein and amino acid levels of the experimental diets
1)LP diet was not supplemented with AA, and overall AA were 14.5 % and 21.7% less compared to requirements in 18.5% CP and 17.0% CP diet, respectively.
2)LP diets supplemented with 11 AA (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, valine, and cysteine) were formulated to meet requirement. LP diets with 13 AA were obtained by supplementing glutamic acid and glycine to LP diets supplemented with 11 AA at the expense of corn-starch.
CP, crude protein; LP, low protein; AA, amino acid.
Sample collection
On day 21 and 28, individual BW and feed leftovers per cage were measured and the gain to feed ratio (G:F) was calculated. Excreta from birds fed experimental diets were collected four times every 12 hours from day 19 to 21 of age. Excreta within a cage were pooled and stored at −20℃, then dried in a forced-air oven (JS research, Gongju, Korea) at 50℃ for further analysis.
Chemical analysis and calculation
The experimental diets were ground and analyzed for AA composition following the AOAC International method 982.30E (a, b) [10] and CP concentrations using the Kjeldahl method (Foss Innovation Centre, Hillerød, Denmark). Chromium concentrations in diets were determined using the method described by Fenton and Fenton [11]. Excreta samples were also analyzed for CP and chromium concentration.
The index method was used to determine the N excretion coefficient with the following equations [12]:
N retention = [1 − (Cri ÷ Cro) × (No ÷ Ni)]
N excretion coefficient = 1 − N retention
N excretion (g) = Feed intake (g) × Dietary N concentration (%) × N excretion coefficient
where Cri and Cro represent the chromium concentrations (%) in the diet and excreta, respectively; Ni and No represent the nitrogen concentrations (%) in the diet and excreta, respectively.
Statistical analysis
The data were analyzed using the MIXED procedure of SAS software (SAS Institute, Cary, NC, USA). The dietary treatment was considered a fixed variable, and replication was considered a random variable. The experimental unit was a cage. Treatment means were separated using Tukey’s HSD, and a statistical significance was set at p < 0.05.
RESULTS
The analyzed concentrations of CP and AA in the experimental diets were equal to the calculated values (Table 2). The results of the growth performance and N excretion are presented in Table 3. All growth performances, excluding feed intake (FI) in the finisher period, and N excretion showed significant differences (p < 0.05) between dietary treatments.
Table 3. Growth performance and nitrogen excretion of experiment diets
1)LP diet was not supplemented with AA, and the overall AA were 14.5 % and 21.7% less compared to requirements in 18.5% CP and 17.0% CP diet, respectively.
2)LP diets supplemented with 11 AA (arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, valine, and cysteine) were formulated to meet requirement. LP diets with 13 AA were obtained by supplementing glutamic acid and glycine to LP diets supplemented with 11 AA at the expense of corn-starch.
3)Each mean represents five observations.
a–cMeans within a row without a common superscript differ (p < 0.05).
CP, crude protein; LP, low protein; AA; amino acid; BW, body weight; BWG, body weight gain; FI, feed intake; G:F, gain to feed ratio; N, nitrogen.
Growth performance
Excluding FI, the two LP diets without crystalline AA exhibited lower (p < 0.05) growth performance during the grower period than the control diet. The LP diet containing 17.0% CP without crystalline AA supplementation yielded lower (p < 0.05) FI than the control diet. However, the supplementation of 11 AA in the two LP diets increased (p < 0.05) BW, BWG, FI, and G:F compared to the two LP diets without crystalline AA, and their growth performance did not differ from that of the control diet. The two LP diets with 13 AA were not different in terms of the growth performance from the two LP diets with 11 AA.
During the finisher period, the two LP diets without crystalline AA exhibited less (p < 0.05) BW than the control diet. The BWG of birds fed only the LP diet containing 17.0% CP without crystalline AA was lower (p < 0.05) than that of the control diet. For the G:F, birds fed the two LP diets without crystalline AA were not different from birds fed the control diet. However, supplementing 11 AA in the two LP diets increased (p < 0.05) BW compared to the two LP diets without crystalline AA, and it was not different from BW of birds fed the control diet. The two LP diets supplemented with 11 AA were not different from the control diet regarding growth performance. Supplementing 13 AA in the two LP diets did not differ from the two LP diets supplemented with 11 AA in terms of growth performance.
Overall, the two LP diets without crystalline AA yielded lower (p < 0.05) BWG than the control diet, and the LP diet containing 17.0% CP showed lower FI and G:F than the control diet. However, supplementing 11 AA in the two LP diets increased (p < 0.05) BW, BWG, and G:F, reaching a level that was not significantly different from the control diet. Growth performance from supplementing 13 AA in the two LP diets did not differ from the two LP diets with 11 AA.
Nitrogen excretion
The N excretion coefficients differed (p < 0.05) between groups. The two LP diets without crystalline AA resulted in higher (p < 0.05) N excretion coefficients than the control diet. Supplementing the 11 AA in LP diets reduced (p < 0.05) N excretion coefficients compared to the two LP diets without crystalline AA, and these reductions were not different from those observed in the control diet. The amount of N excretion of birds fed the 17.0% LP diet with 11 AA was lower (p < 0.05) than that of birds fed the 18.5% LP diet without crystalline AA. Supplementing 13 AA in the LP diets was not different from LP diets supplemented with 11 AA the N excretion coefficient and amount of N excretion.
DISCUSSION
LP diets can lower feed costs and environmental pollution. Previous studies have evaluated the effects of the LP diets on growth performance by supplementing indispensable AA or both indispensable and dispensable AA. Indispensable AA was supplemented in the LP diet to meet AA requirements [13–19], while dispensable AA, such as Asp, Gly, and Glu, were supplemented as N sources for dispensable AA synthesis [4–6, 20–24]. In the current study, Glu and Gly were supplemented in LP diets because Glu was considered an N source for dispensable AA synthesis in the LP diet [25–27], and Gly in LP diets was considered a potentially deficient AA [28–30]. The current study evaluated the effects of supplementing indispensable AA and dispensable AA in LP diets.
Supplementing 11 AA in the two LP diets improved BW, BWG, and G:F compared to the two LP diets without crystalline AA during the grower and overall periods. These results might be attributed to satisfying indispensable AA requirements to optimize growth performance. Regarding FI, the two LP diets supplemented with 11 AA were not different from the two LP diets without crystalline AA since the birds might be able to compensate for undernutrition through voluntary feed consumption [31]. During the finisher period, the two LP diets supplemented with 11 AA were not different from the two LP diets without crystalline AA in terms of growth performance, excluding BW. For BW, the two LP diets with 11 AA had a greater BW than the two LP diets without crystalline AA, even though the BWG of the two LP diets with 11 AA during the finisher period was not different from the two LP diets without crystalline AA. This finding is because the BW of the two LP diets supplemented with 11 AA was greater than that of the two LP diets without crystalline AA during the grower period. Regarding BWG, the two LP diets with 11 AA were not different from the two LP diets without crystalline AA since all birds were fed the same standard finisher diet. Additionally, FI was not different between dietary treatments for the same reason. Thus, supplementing of 11 AA in the two LP diets did not increase G:F because it did not alter BWG and FI.
When indispensable AA was supplemented in the LP diet to meet requirements, reducing dietary CP from 20.0% to 17.0% did not lower BW, BWG, FI, and G:F. Previous studies have demonstrated that dietary CP can be practically reduced by up to 3% without adversely affecting growth performance [4,32-35], corroborating this current finding. However, reducing dietary CP may be able to impair growth performance, even with indispensable AA supplementation in the LP diet. Dean et al. [30] found that average daily gain, final BW, and G:F linearly decrease with the reduction of dietary CP from 22% to 16%. Notably, the true digestible indispensable AA in the experimental diets, excluding Lysine, Threonine, Methionine, and Cysteine, were reduced as the dietary CP was curtailed. Furthermore, Bregendahl et al. [21] reported that despite formulating all diets to meet or exceed indispensable AA requirements based on true digestibility, 18.6% LP diets supplemented with indispensable AA led to less growth performance compared to the control diet (23% CP). These results may be attributed to an increase in ratio of unbound AA to protein-bound AA from a decrease in dietary SBM concentration and utilization differences between unbound AA and AA absorbed from protein in broiler chickens [36]. However, these effects are inconsistent, highlighting the need for further research.
On the other hand, supplementing 13 AA in the two LP diets did not improve growth performance compared to the 2 LP diets supplemented with 11 AA in the current study. This result proposes that dispensable AA was not deficient in the LP diets as long as the CP level was above 17.0% during the grower period. Hussein et al. [7] reported that dispensable AA was not deficient in 17.7% LP diets from day 7 to 21, as adding 5.5% Glu did not impact growth performance. Similarly, Bregendahl et al. [21] showed that adding 1% glutamine and asparagine as N sources to 18.6% LP diets did not affect growth performance. However, Namroud et al. [22] reported that supplementing 1.12% Glu and 0.26% Gly in a 19% LP diet improved growth performance as much as the control diet (23% CP). Corzo et al. [4] reported that all dispensable AA should be added to the 18% LP broiler diets to match the growth performance of the control diet (22% CP). In addition, Dean et al. [30] discovered that from day 0 to 17, 16.2% LP diets supplemented with Gly linearly increased G:F, with increasing concentrations of Gly + serine from 1.80% to 3.00%. The effect of dispensable AA supplementation on growth performance in LP diets may not be consistent with previous experiments due to differences in dispensable AA concentrations, AA precursors, and feed ingredients.
Supplementing 11 AA in the two LP diets resulted in a decrease in the N excretion coefficient compared to the two LP diets without crystalline AA in this study. This result agrees with Deschepper et al. [37] who demonstrated that a 16% LP diet with indispensable AA supplementation exhibited a greater protein accretion than a 21% LP diet with indispensable AA deficiency. These results may be attributed to an AA imbalance due to AA deficiency inhibiting protein synthesis [38]. The AA imbalance can lead to deamination, generating ammonia, which is then excreted via the Krebs cycle as uric acid [36]. Similarly, Macelline et al. [39] reported that supplementing indispensable AA in an LP diet decreased urea N in the plasma. Supplementing indispensable AA may mitigate the effect of the AA imbalance that increases deamination. However, further research is warranted to clarify the impact of reduced N metabolites in the plasma due to abated dietary CP concentration on the N excretion coefficient. Moreover, supplementing indispensable AA and reducing dietary CP might induce to decrease amount of N excretion by lowering N excretion coefficient and intake, primary factors that influence amount of N excretion. Previous research has demonstrated that reducing dietary CP decreased nitrogenous waste in litter [18,22,40,41] supporting current findings.
When indispensable AA was supplemented in LP diets to meet AA requirements for broilers, the 3% reduction in dietary CP did not affect the amount of N excretion and N excretion coefficient. Consistent with the current study, Chrystal et al. [42] demonstrated that there was no linear effect when dietary CP was reduced from 21% to 16.5% on N retention in broilers from day 33 to 35. Hernández et al. [14] also reported that reducing dietary CP from 23% to 20% and 21.5% to 18.5% did not influence N retention for male broilers from day 8 to 21 and day 22 to 35, respectively. These findings suggest that dietary CP level may be able to be reduced from 20.0% to 17.0% without affecting the N excretion coefficient during the grower phase, similar to the current growth performance results.
However, the supplementation of 13 AA in the two LP diets showed no difference in terms of the N excretion coefficient and the amount of N excretion when compared to the two LP diets supplemented with 11 AA. These results are consistent with Deschepper and deGroote [37], who showed that LP diets supplemented with indispensable AA following NRC recommendations [43] were not different from LP diets supplemented with indispensable AA, Glu, and Gly concerning protein accretion. Additionally, Hilliar et al. [23] established that adding Gly to a 19% LP diet did not affect N retention, similar to the current study.
In conclusion, this study demonstrated that supplementing indispensable AA in the LP diet preserved growth performance and N excretion in broilers as long as the CP level was above 17.0% during the grower period. Providing LP diets without supplementation of crystalline AA during the grower period can potentially have a negative impact on growth performance during the finisher period when feeding a standard diet. On the other hand, dispensable AA did not seem to be deficient in the LP diet during the grower period unless the dietary CP level was lower than 17.0%.
참고문헌
- Wheeler T, Reynolds C. Predicting the risks from climate change to forage and crop production for animal feed. Anim Front. 2013;3:36-41. https://doi.org/10.2527/af.2013-0006
- Masuda T, Goldsmith PD. China's meat and egg production and soybean meal demand for feed: an elasticity analysis and long-term projections. Int Food Agribusiness Manag Rev. 2012;15:35-53. https://doi.org/10.22004/ag.econ.132788
- Williams PEV. Animal production and european pollution problems. Anim Feed Sci Technol. 1995;53:135-44. https://doi.org/10.1016/0377-8401(95)02017-T
- Corzo A, Fritts CA, Kidd MT, Kerr BJ. Response of broiler chicks to essential and non-essential amino acid supplementation of low crude protein diets. Anim Feed Sci Technol. 2005;118:319-27. https://doi.org/10.1016/j.anifeedsci.2004.11.007
- Hilliar M, Hargreave G, Girish CK, Barekatain R, Wu SB, Swick RA. Using crystalline amino acids to supplement broiler chicken requirements in reduced protein diets. Poult Sci. 2020;99:1551-63. https://doi.org/10.1016/j.psj.2019.12.005
- Hofmann P, Siegert W, Naranjo VD, Rodehutscord M. Effects of supplemented nonessential amino acids and nonprotein nitrogen on growth and nitrogen excretion characteristics of broiler chickens fed diets with very low crude protein concentrations. Poult Sci. 2020;99:6848-58. https://doi.org/10.1016/j.psj.2020.09.003
- Hussein AS, Cantor AH, Pescatore AJ, Gates RS, Burnham D, Ford MJ, et al. Effect of low protein diets with amino acid supplementation on broiler growth. J Appl Poult Res. 2001;10:354-62. https://doi.org/10.1093/japr/10.4.354
- Hoehler D, Lemme A, Ravindran V, Bryden WL, Rostagno HS. Feed formulation in broiler chickens based on standardized ileal amino acid digestibility. In: Proceedings of Advances in Aquaculture Nutrition VIII. VIII International Symposium on Aquaculture Nutrition; 2006; Monterrey, Nuevo Leon, Mexico. p. 197-212.
- Aviagen. Ross 308 broiler nutrition specifications 2019 [Internet]. Aviagen Group. 2019 [cited 2021 Aug 15]. https://en.aviagen.com/assets/Tech_Center/Ross_PS/Ross308-PS-NS-2019-EN.pdf
- AOAC [Association of Official Analytical Chemists] International. Official methods of analysis of AOAC International. 20th ed. Gaithersburg, MD: AOAC International; 2016.
- Fenton TW, Fenton M. An improved procedure for the determination of chromic oxide in feed and feces. Can J Anim Sci. 1979;59:631-4. https://doi.org/10.4141/cjas79-081
- Kong C, Adeola O. Evaluation of amino acid and energy utilization in feedstuff for swine and poultry diets. Asian-Australas J Anim Sci. 2014;27:917-25. http://dx.doi.org/10.5713/ajas.2014.r.02
- Darsi E, Shivazad M, Zaghari M, Namroud NF, Mohammadi R. Effect of reduced dietary crude protein levels on growth performance, plasma uric acid and electrolyte concentration of male broiler chicks. J Agric Sci Technol. 2012;14:789-97. http://dorl.net/dor/20.1001.1.16807073.2012.14.4.22.8 1001.1.16807073.2012.14.4.22.8
- Hernandez F, Lopez M, Martinez S, Megias MD, Catala P, Madrid J. Effect of low-protein diets and single sex on production performance, plasma metabolites, digestibility, and nitrogen excretion in 1- to 48-day-old broilers. Poult Sci. 2012;91:683-92. https://doi.org/10.3382/ps.2011-01735
- Malomo GA, Bolu SA, Olutade SG. Effects of dietary crude protein on performance and nitrogen economy of broilers. Sustain Agric Res. 2013;2:52-7. https://doi.org/10.5539/sar.v2n3p52
- Gou ZY, Jiang SQ, Jiang ZY, Zheng CT, Li L, Ruan D, et al. Effects of high peanut meal with different crude protein level supplemented with amino acids on performance, carcass traits and nitrogen retention of Chinese Yellow broilers. J Anim Physiol Anim Nutr. 2016;100:657-64. https://doi.org/10.1111/jpn.12420
- Belloir P, Meda B, Lambert W, Corrent E, Juin H, Lessire M, et al. Reducing the CP content in broiler feeds: impact on animal performance, meat quality and nitrogen utilization. Animal. 2017;11:1881-9. https://doi.org/10.1017/S1751731117000660
- Ullrich C, Langeheine M, Brehm R, Taube V, Siebert D, Visscher C. Influence of reduced protein content in complete diets with a consistent arginine-lysine ratio on performance and nitrogen excretion in broilers. Sustainability. 2018;10:3827. https://doi.org/10.3390/su10113827
- Lemme A, Hiller P, Klahsen M, Taube V, Stegemann J, Simon I. Reduction of dietary protein in broiler diets not only reduces n-emissions but is also accompanied by several further benefits. J Appl Poult Res. 2019;28:867-80. https://doi.org/10.3382/japr/pfz045
- Aletor VA, Hamid II, Niess E, Pfeffer E. Low-protein amino acid-supplemented diets in broiler chickens: effects on performance, carcass characteristics, whole-body composition and efficiencies of nutrient utilisation. J Sci Food Agric. 2000;80:547-54. https://doi.org/10.1002/(SICI)1097-0010(200004)80:5<547::AID-JSFA531>3.0.CO;2-C
- Bregendahl K, Sell JL, Zimmerman DR. Effect of low-protein diets on growth performance and body composition of broiler chicks. Poult Sci. 2002;81:1156-67. https://doi.org/10.1093/ps/81.8.1156
- Namroud NF, Shivazad M, Zaghari M. Effects of fortifying low crude protein diet with crystalline amino acids on performance, blood ammonia level, and excreta characteristics of broiler chicks. Poult Sci. 2008;87:2250-8. https://doi.org/10.3382/ps.2007-00499
- Hilliar M, Huyen N, Girish CK, Barekatain R, Wu S, Swick RA. Supplementing glycine, serine, and threonine in low protein diets for meat type chickens. Poult Sci. 2019;98:6857-65. https://doi.org/10.3382/ps/pez435
- Hofmann P, Siegert W, Kenez A, Naranjo VD, Rodehutscord M. Very low crude protein and varying glycine concentrations in the diet affect growth performance, characteristics of nitrogen excretion, and the blood metabolome of broiler chickens. J Nutr. 2019;149:1122-32. https://doi.org/10.1093/jn/nxz022
- Berres J, Vieira SL, Dozier WA 3rd, Cortes MEM, de Barros R, Nogueira ET, et al. Broiler responses to reduced-protein diets supplemented with valine, isoleucine, glycine, and glutamic acid. J Appl Poult Res. 2010;19:68-79. https://doi.org/10.3382/japr.2009-00085
- Bezerra RM, Perazzo FG, dos Santos RA. Glutamic acid and protein reduction for broilers and commercial laying hens. Appl Res Agrotechnol. 2013;6:101-9. https://doi.org/10.5935/PAeT.V6.N3.12
- Bezerra RM, Costa FGP, Givisiez PEN, Freitas ER, Goulart CC, Santos RA, et al. Effect of L-glutamic acid supplementation on performance and nitrogen balance of broilers fed low protein diets. J Anim Physiol Anim Nutr (Berl). 2016;100:590-600. https://doi.org/10.1111/jpn.12405
- Parr JF, Summers JD. The effect of minimizing amino acid excesses in broiler diets. Poult Sci. 1991;70:1540-9. https://doi.org/10.3382/ps.0701540
- Corzo A, Kidd MT, Burnham DJ, Kerr BJ. Dietary glycine needs of broiler chicks. Poult Sci. 2004;83:1382-4. https://doi.org/10.1093/ps/83.8.1382
- Dean DW, Bidner TD, Southern LL. Glycine supplementation to low protein, amino acid-supplemented diets supports optimal performance of broiler chicks. Poult Sci. 2006;85:288-96. https://doi.org/10.1093/ps/85.2.288
- Zubair AK, Leeson S. Compensatory growth in the broiler chicken: a review. Worlds Poult Sci J. 1996;52:189-201. https://doi.org/10.1079/Wps19960015
- Baker DH. Advances in protein-amino acid nutrition of poultry. Amino Acids. 2009;37:29-41. https://doi.org/10.1007/s00726-008-0198-3
- Cappelaere L, Le Cour Grandmaison J, Martin N, Lambert W. Amino acid supplementation to reduce environmental impacts of broiler and pig production: a review. Front Vet Sci. 2021;8:689259. https://doi.org/10.3389/fvets.2021.689259
- An SH, Kim KE, An BK, Kong C. Effects of reduced dietary crude protein diet with synthetic amino acid supplements on the growth performance and histochemical characteristics of the breast meat of male broilers. Korean J Poult Sci. 2022;49:33-43. https://doi.org/10.5536/KJPS.2022.49.1.33
- Wealleans A, Ashour R, Abu Ishmais M, Al-Amaireh S, Gonzalez-Sanchez D. Comparative effects of proteases on performance, carcass traits and gut structure of broilers fed diets reduced in protein and amino acids. J Anim Sci Technol. Forthcoming 2023. https://doi.org/10.5187/jast.2023.e20
- Liu SY, Macelline SP, Chrystal PV, Selle PH. Progress towards reduced-crude protein diets for broiler chickens and sustainable chicken-meat production. J Anim Sci Biotechnol. 2021;12:20. https://doi.org/10.1186/s40104-021-00550-w
- Deschepper K, deGroote G. Effect of dietary protein, essential and non-essential amino acids on the performance and carcase composition of male broiler chickens. Br Poult Sci. 1995;36:229-45. https://doi.org/10.1080/00071669508417772
- Salmon WD. The significance of amino acid imbalance in nutrition. Am J Clin Nutr. 1958;6:487-94. https://doi.org/10.1093/ajcn/6.5.487
- Macelline SP, Wickramasuriya SS, Cho HM, Kim E, Shin TK, Hong JS, et al. Broilers fed a low protein diet supplemented with synthetic amino acids maintained growth performance and retained intestinal integrity while reducing nitrogen excretion when raised under poor sanitary conditions. Poult Sci. 2020;99:949-58. https://doi.org/10.1016/j.psj.2019.10.035
- van Harn J, Dijkslag MA, van Krimpen MM. Effect of low protein diets supplemented with free amino acids on growth performance, slaughter yield, litter quality, and footpad lesions of male broilers. Poult Sci. 2019;98:4868-77. https://doi.org/10.3382/ps/pez229
- van Emous RA, Winkel A, Aarnink AJA. Effects of dietary crude protein levels on ammonia emission, litter and manure composition, N losses, and water intake in broiler breeders. Poult Sci. 2019;98:6618-25. https://doi.org/10.3382/ps/pez508
- Chrystal PV, Moss AF, Khoddami A, Naranjo VD, Selle PH, Liu SY. Impacts of reduced-crude protein diets on key parameters in male broiler chickens offered maize-based diets. Poult Sci. 2020;99:505-16. https://doi.org/10.3382/ps/pez573
- NRC [National Research Council]. Nutrient requirements of poultry. 9th rev. ed. Washington, DC: National Academies Press; 1994.