HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Namroud, N. F. Articles by Zaghari, M. Search for Related Content PubMed PubMed Citation Articles by Namroud, N. F. Articles by Zaghari, M.

Effects of Fortifying Low Crude Protein Diet with Crystalline Amino Acids on Performance, Blood Ammonia Level, and Excreta Characteristics of Broiler Chicks

Department of Animal Science, University of Tehran, Karaj, Tehran, Iran

¹ Corresponding author: nebonidnamroud{at}hotmail.com or shivazad{at}ut.ac.ir

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A study was conducted in a completely randomized design to evaluate the performance, excreta characteristics, and some blood nitrogen metabolite concentrations of 28-d-old male broilers fed 4 experimental diets in which CP was decreased in a stepwise manner from 23 to 17%. The other 4 diets were formulated to have 19 and 17% CP, in which 2 of them contained an additional 10% of particular essential amino acids (EAA) and 2 were supplemented with Gly and Glu. Ileal digestible quantities of all EAA were almost equal in the diets, and total amount of each EAA was maintained at or above NRC requirements. Decreasing dietary CP below 19% depressed performance and appetite and increased fat deposition in the whole body and abdominal cavity significantly. Adding the Gly and Glu mixtures to low-CP diets improved performance and decreased fat deposition. Uric acid, moisture, and acidity of excreta were decreased by reduction of dietary CP; excretory ammonia level was increased in 17% CP diets. Blood ammonia level was increased and plasma uric acid was decreased with reduction of CP to 17%. Supplementing Gly and Glu increased plasma and excretory uric acid level in spite of decreasing blood ammonia concentration. The aminostatic hypothesis cannot explain the sharp reduction in appetite in this experiment, because alteration of dietary CP had no significant influence on most plasma free amino acid levels. Therefore, reduction of CP to 19% not only does not impair performance but also decrease nitrogen, ammonia, and pH of excreta that may improve upon litter and air quality. Adding large amounts of crystalline EAA to diets with low intact CP increased blood and excretory ammonia concentration, which due to its negative effects on tissue metabolism may be the main cause of retarded growth and appetite in decreased CP diets below 19%.

Key Words: crude protein • amino acid • ammonia • uric acid • broiler

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Attempts to decrease CP content of broiler diets have been successful to a point, but most researchers agree that reduction of CP has some noxious effects on performance and appetite. This failure is seen even with providing all requirements for those amino acids considered as essential. Failure to obtain optimum result in performance may be attributed to one or more of the following factors: lack of nitrogen pool to synthesize nonessential amino acids (NEAA); insufficiency of body capacity to meet all NEAA requirements especially Gly, Ser, Pro, and Glu; decreased level of potassium or altered ionic balance; and imbalances among certain amino acids such as Arg to Lys, Lys to Thr, between branched-chain amino acids, and Trp to large neutral amino acids. But, a majority of these factors cannot explain completely the main reason for failure in performance.

Based on the assumption that the nonessential amino nitrogen may likely become a limiting factor in the low-CP diets and the NEAA limitation is particularly significant in regard to the effects upon the carcass fatness, many researchers had added NEAA to low-CP diets. Fancher and Jensen (1989a) concluded that the decreased growth associated with low-CP diets was not due to insufficient NEAA. They further (Fancher and Jensen, 1989b,c) demonstrated that the performance of broilers was impaired when feeding a low-CP diet despite the fact that Met, Lys, Thr, Arg, Trp, and potassium content were equal to a high-CP diet. Waldroup et al. (2005) reported that supplemental Gly to a low-CP diet improved BW significantly, although not completely restoring performance equal to that of diets with 22 or 24% CP. Schutte et al. (1997) recommended 1.9% of total Gly and Ser when birds were fed low-CP diets fortified with essential amino acids (EAA). On the other hand, some researchers suggested that feeding a greater rate of EAA to NEAA in low-CP diets tends to improve performance and prevent excess fat deposition (Yamazaki et al., 1998); however, there are some antithetical findings that reject this positive influence (Yamazaki et al., 2006).

The addition of crystalline amino acids often results in a reduction of feed intake (Han and Baker, 1993; Carew et al., 1998; Si et al., 2004). Some studies (Kumta and Harper, 1962; Peng and Harper, 1970) proposed an aminostatic hypothesis, namely that amino acid levels or patterns in plasma may serve as a signal to an appetite-controlling mechanism. It is possible that not only the levels of amino acids but also the levels of their metabolites serve as signals to regulate feed intake. In rats, the level of blood urea has no effect on feed intake (Kumta and Harper, 1961). Ammonia is inevitably liberated in protein metabolism, but it is very toxic to living cells, and the sensitive mechanism(s) in animals keep it below a toxic level. Excess or imbalanced dietary amino acids split into C-skeletons and ammonia, which is converted to uric acid by birds. Decreasing feed intake to limit the absorption and catabolism of excess amino acids may be one mechanism to decrease the intracellular concentration of ammonia. Another way is induction of activities of enzymes involved in ammonia detoxification (Noda, 1975). According to Noda (1975), the blood ammonia level is an important factor in regulation of appetite in rats, but there is no reliable research to investigate this controlling mechanism in broiler chicks or the effective dietary factors on blood ammonia level.

In the present study, we tried to stabilize all important dietary variables that usually tend to alter with decreasing CP including electrolyte balance, Lys:Arg ratio, and standardized ileal digestible EAA levels in the dietary treatments to examine the effects of CP reduction on quality and quantity of performance and excreta characteristics. In addition, to study the influence of dietary CP and amino acid levels on the rate of ammonia production, the blood and excreta ammonia level were measured. Another objective of this study was to check the validity of the aminostatic hypothesis under our experimental condition.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Birds and Housing

Day-old male Ross 308 broiler chicks obtained from a local hatchery were housed in electrically heated battery cages (0.197 m² per bird) and had free access to water and a commercial starter diet for 10 d. On d 10, birds (215 ± 15 g) were allotted to 1 of the 8 feeding treatments on the basis of BW. Each dietary treatment was applied to 8 replicates of 6 chicks, randomly. The experimental birds were given ad libitum access to water and diet. The ambient temperature was gradually decreased from 35 to 24°C over the period of 1 to 28 d of age. The birds were exposed to a 23L:1D cycle. All procedures were approved by the Animal Care and Welfare Committee of Tehran University.

Diet Formulation

Corn, dehulled soybean meal, and corn gluten meal were sampled before diet formulation to determine CP as Kjeldahl nitrogen x 6.25, moisture, and total amino acids content (Degussa AG, Rodenbacher Chaussee 4, Hanau-Wolfgang, Germany), after which the contents of true digestible amino acids were calculated from standardized ileal digestibility coefficients listed by Lemme et al. (2004). The amount of calcium (method 968.08), phosphorus (method 965.17), potassium (method 966.03), sodium (method 966.03), and chloride (method 943.01) was analyzed by AOAC (1995) procedures in all feeding ingredients. Each ingredient sample was analyzed in triplicate. The dietary electrolyte balance was set at 280 mEq/kg. All diets were formulated to be isoenergetic (3,175 kcal/kg of ME_n). The amount of dietary calcium, available phosphorus, and sodium was maintained equal in all treatments (Table 1). Four levels of CP were used in this study including 23, 21, 19, and 17% with almost equal ileal digestible amounts of all EAA. Total EAA concentrations in all treatments were maintained at or above NRC (1994) recommended levels (Table 2). In addition, one series of 19 and 17% CP diets were supplemented with Gly and Glu to bring them to the amount of high-CP diets. Another series of 19 and 17% CP diets were supplemented with 10% additional EAA (Lys, Thr, Arg, Trp). Diets were supplemented with complete vitamin and trace mineral mixes. The L-Lys HCl, DL-Met, and L-Thr used in the diets were feed grade, whereas all other crystal-line amino acids as well as K₂CO₃ were reagent grade (minimum 98% purity) and purchased from Degussa Iran AG (Tehran, Iran).

At the end of the experiment, 2 blood samples were taken per replicate from the brachial vein and placed into evacuated heparinized tubes. Samples were put on ice immediately and processed within 1 h of collection. Plasma was obtained by centrifuging the blood samples at 3,000 x g for 15 min at 4°C. Plasma aliquots were kept frozen at –70°C until analyzed, and concentrations of free plasma amino acids were measured with a model 3A30 Carlo Erba Amino Analyzer (Carlo Erba-Fisons, Rodano, Milan, Italy) as described previously (Marchesini et al., 1987). Blood ammonia level was determined with coupled enzymatic assay (Ishihard et al., 1972) 1 h after sampling. Plasma uric acid was measured by the method of Liddle et al. (1959) by enzymatic (uricase) spectrophotometry. Briefly, this enzyme catalyzed the oxidation of uric acid to allantoin with subsequent production of H₂O₂. This method is based on the fact that uric acid has a ultraviolet absorbance peak at 293 nm, whereas allantoin does not. The difference in absorbance before and after incubation with uricase is proportional to the uric acid concentration.

Excreta Samples

At 22 d of age, excreta were collected by replicate for 8 h and homogenized using a PT 10/35 polytron mixer (Brinkmann Instruments, Westbury, NY). Before recording the pH values of the samples on a Sentron model 2001 pH meter (Sentron, Gig Harbor, WA), the electrode was rinsed with distilled water and dried with soft paper tissue.

The remaining sample per replicate was placed in a –30°C freezer. After 1 wk, the samples were freeze-dried and then milled using a 0.5-mm sieve. Nitrogen content of the samples was then determined using the procedure (Kjeldahl) described by AOAC (1995). A part of freeze-dried samples was prepared and extracted with lithium carbonate (Hevia and Clifford, 1977) in duplicate to use in determining uric acid content by enzymatic spectrophotometer (Spectrophotometer, Hitachi 0404-006, Hitachi Ltd., Tokyo, Japan; Liddle et al., 1959). To determine ammonia content of excreta, frozen samples were scanned in the near-infrared on a Foss NIRSystems model 6500 scanning monochromator (Foss NIRSystems, Silver Spring, MD; Reeves and VanKessel, 2000). Samples were thawed and then scanned in airtight polyethylene bags to determine ammonia concentration. All samples were scanned in duplicate.

Carcass Characteristics and Whole-Body Analyses

At the end of the experimental period (d 28), 2 birds per replicate (with a BW close to the replicate mean), were slaughtered by cervical dislocation. The birds were killed 22 h after their last meal (with free access to water). One of the slaughtered birds was used to determine carcass characteristics. The data on breast muscle, thigh muscle, abdominal fat, and organs weight (i.e., liver, intestine, proventriculus + gizzard) were recorded at this stage. The other killed chick per replicate was stored in an airtight polyethylene bag at –22°C for later determination of whole-body composition. The whole body of the killed chicks was thawed overnight at room temperature, homogenized with Waring blender (Waring Products Division, New Hartford, CT) for 2.5 min, and sampled according to procedures described by Barker and Sell (1994). Whole-body DM (Barker and Sell, 1994), nitrogen content, and fat content were analyzed in triplicate subsequently (Nutrition and Chemical Laboratory of Tehran University, Karaj, Iran). Whole-body CP was calculated as Kjeldahl nitrogen x 6.25.

Statistical Analysis

Data were analyzed using the general linear model ANOVA (SAS Institute, 2004) in a completely randomized design. Means were compared using Duncan’ multiple range test. In all cases, significance was set at P < 0.05 or P < 0.01.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
During the 10 to 19-d period, performance was significantly influenced by dietary CP (Table 3). Fortifying a low-CP diet with excess EAA resulted in more reduction in BW, feed intake, and less favorable feed conversion ratio (FCR). Adding Gly and Glu (diet 5 and 6) significantly improved BW and feed intake and did not influence FCR compared with the same treatments without balanced Gly and Glu (diet 3 and 4). During the period of 19 to 28 d of age, some kind of compensatory growth was activated in the birds given 19% CP with or without balanced Gly and Glu (diet 3 and 5). But the chicks on all other low-CP treatments (diets 4, 6, 7, and 8) had a lower performance versus 23 or 21% CP diets. At the end of experiment, the greatest BW were obtained with birds fed diets with at least 19% CP (diets 1, 2, 3, and 5) apart from a 19% CP diet with an excess amount of EAA. Addition of an excess amount of EAA to low-CP diets (diets 7 and 8) decreased performance compared with regular low-CP diets (diets 3 and 4). On the other hand, supplementing low-CP diets with Gly and Glu improved performance significantly.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Deficiency of dietary protein is known to increase the fat deposition in broilers. Many researchers have reported the effect of supplementing several amino acids such as Met + cystine (Bunchasak et al., 1996), Arg (Leclercq et al., 1994), Trp, and Glu on decreasing carcass and abdominal fat and hepatic lipid content. However, the decrease was not obvious when supplemented beyond the requirement level. In our study, mixture of excess amounts of Lys, Trp, Thr, and Arg caused no reduction in fat deposition in abdominal cavity and carcass. This result is in agreement with previous studies such as Yamazaki et al. (2006). Han et al. (1992) showed that NEAA nitrogen was necessary for optimal chick performance and body composition, because NEAA biosynthesis was also a limiting factor in a low-CP diet. A decrease in the liver triglyceride content and abdominal fat deposition due to supplementation of Gly and Glu to the low-CP diet has been reported by Bunchasak et al. (1998). Our results are in complete agreement with the above research; however, Moran and Stilborn (1996) noted that Glu supplementation had no decreasing effect on abdominal fat. One of the mechanisms involved in decreasing carcass fatness by feeding greater protein level diets is the associated increased heat increment involved in deamination and transamination of surplus amino acids to other metabolites and finally uric acid. Rosebrough et al. (2002) showed that increase of CP can dramatically decrease in vitro lipogenesis. They suggested that a combination of mRNA stability and posttranscriptional events interact to regulate lipogenesis in the chicken.

Chicks fed the low-CP diets tend to excrete less nitrogen. Excreta nitrogen content as percentage of DM significantly decreased in a linear manner with reduction of dietary CP ranging from 17 to 23%. The regression model (R² = 0.91) is as follows:

where Y = excreta nitrogen content (% of DM) and X = dietary CP (%). This is in agreement with Si et al. (2004). The increased nitrogen excretion that resulted from the amino acid mixtures, especially EAA mixtures, suggests that the supplements were not totally used to support protein accretion.

The increase of excreta acidity observed in low-CP treatments (except the 17% CP diet) might associate with drier excreta. The increase in pH of the excreta observed in the 17% CP diet might contribute to the increase of ammonia excretion. The lower pH decreases the unionized ammonia available for volatilization. The ammonia gas concentration tends to increase with increasing moisture content of the excreta or litter (Elliott and Collins, 1982; Ferguson et al., 1998), because the generation of a majority of microbe species depends on water, and thus, the increase of litter moisture activates them. Litter pH has been shown to be correlated with litter moisture content (Ferguson et al., 1998). In our study, this correlation was observed between pH and moisture of excreta as well, other than 17% CP diets. Elliott and Collins (1982) concluded that pH and moisture regulate the release of ammonia gas in poultry houses. In terms of reduction in ammonia gas production, the effective factors are total nitrogen content, ammonia level, pH, and moisture content. Diminishing dietary CP from 23 to 19% while maintaining adequate EAA levels during 10 to 28 d of age results in not only a significant decline in nitrogen emission but also a probable reduction in the ammonia volatilization because of reduction in pH and moisture. Contrary to expectations, reduction of dietary CP below the minimum level (19%) resulted in more ammonia.

Administration of a low-CP diet with a high level of synthetic EAA resulted in increasing blood ammonia level and decreasing plasma uric acid. Noda (1975) reported that blood ammonia level may act as a signal to regulate appetite in rats. In addition, Lardy and Fedott (1950) observed that growth in rats was depressed after increasing the amount of ammonium salts added to the diet in place of NEAA. Russek (1971) reported that intraportal infusion of a small amount of ammonium salt strongly depressed the appetite of fasted dogs. Leung and Rogers (1969) in addition to Peng and Harper (1970) proposed the aminostatic hypothesis that associated appetite with pattern of plasma free amino acids. They suggested that imbalance pattern of blood amino acids may be detected in the brain and trigger some appetite-controlling mechanisms. But in our experiment, there was not a significant difference among plasma-limiting amino acid levels or ratio of EAA to NEAA. The aminostatic hypothesis had not been accepted thoroughly by Yoshida (1970) and Noda (1975), and the validity of this theory was questioned by them. In our research, the blood ammonia level of broilers fed the low-CP diets, especially those receiving excess amounts of EAA in their diet, was significantly greater than other treatments. Our conclusion is that a greater amount of synthetic amino acids in low-CP diets is the main cause of high blood ammonia level because of its high absorption rate in contrast to intact protein. In this circumstance, probably low capacity to utilize all digestible plasma-free EAA in protein synthesis or uric acid formation induces a deviation to ammonia production. In birds, ammonia is metabolized by conversion to uric acid; thus, enhancement of uric acid formation should be an effective factor in decreasing ammonia level. Formation of each molecule of uric acid represents a loss of 1 molecule of Gly for chicks (Sonne et al., 1946). Glycine not only participates in protein synthesis as a nonessential amino acid, but it is also required for DNA, RNA, creatine, and uric acid syntheses (Ngo et al., 1977). On this basis, the increasing level of plasma uric acid and reduction in blood ammonia in the birds fed the 17% CP diet that was supplemented with Gly and Glu may be due to greater amounts of Gly in the diet. In addition, feed intake was greater in treatments that were fortified with these NEAA. Therefore, Gly deficiency is probably one of the causes of an increase in blood ammonia level and reduction in appetite. Waldroup et al. (2005) reported that the 21-d BW and feed conversion of the broilers were severely influenced by dietary protein level and supplemental Gly, with a very significant interaction between protein level and Gly. They associated the failure in performance with the role of Gly in uric acid formation.

Ammonia has a small portion of total excretory nitrogen, but a significant shift was seen from uric acid to ammonia when the diet was low in protein. On the basis of previous research, excretory uric acid decreased with declining dietary CP. In our study, adding excess amount of EAA to the 17% CP diet increased nitrogen excretion but did not alter uric acid excretion rate. Our inference is that the low capacity of uric acid synthesis due to Gly deficiency and increased ammonia production deviate the nitrogen excretion pathway to excrete intact ammonia molecules. Nevertheless, there is a strong correlation between blood ammonia and excretory ammonia level.

Also in this experiment, liver percentage weight was increased in low-CP diets. Our conclusion is that increased blood ammonia level activates some mechanisms, one of which (conversion of ammonia to uric acid) mainly took place in the liver. Therefore, the increasing weight of liver might be due to adaptation to elevated ammonia production, but further work is needed to detect enzymes activity associated with uric acid synthesis, especially xanthine oxidase. In addition, low BW may be due partly to the increasing activities of enzymes involved in uric acid production. In mammals, increasing activity of urea cycle enzymes interferes with growth rate (Schimke, 1963). Noda (1975) reported that the capacity of the liver to detoxify ammonia may be a rate-limiting factor in the metabolism of imbalanced amino acid diets.

In summary, we have shown that feeding broiler chickens diets containing a high proportion of crystalline amino acids to maintain optimum recommended levels dramatically retarded growth and feed intake without changing the most plasma-free amino acid concentrations. On the other hand, increasing crystalline EAA proportion in low-CP diets elevates blood ammonia level. Therefore, the limitation on replacing intact protein with crystalline amino acids is partly due to increase of blood ammonia. The present results do not exclude the possibility that the pattern or concentration of plasma-free amino acids may be detected in the hypothalamus (Panksepp and Booth, 1971) and its likely regulatory effects on appetite, but ammonia that is the common product of amino acids imbalance and toxicity, because of its neurotoxic effects, may act as a signal to regulate some physiological mechanisms perhaps including appetite in chicks as well as rats. Nevertheless, adding Gly to low-CP diets with a high portion of crystalline amino acids, because of its important role in uric acid synthesis from ammonia in liver, may improve performance but not completely overcome the adverse effects of a high quantity of crystalline amino acids in low-CP diets.

	ACKNOWLEDGMENTS

 
We gratefully acknowledge Degussa AG and its technical service manager in Iran, Ali Afsar, for conducting the amino acid analyses of our feedstuffs and providing crystalline amino acids.

Received for publication December 8, 2007. Accepted for publication June 29, 2008.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
AOAC. 1995. Official Methods of Analysis. 16th ed. AOAC Int., Arlington, VA.

Barker, D. L., and J. L. Sell. 1994. Dietary carnitine did not influence performance and carcass composition of broiler chickens and young turkeys fed low or high-fat diets. Poult. Sci. 73:281–287.[Web of Science][Medline]

Bunchasak, C., K. Tanaka, and S. Ohtani. 1998. Effect of supplementing nonessential amino acids on growth performance and fat accumulation in broiler chicks fed a diet supplemented with Met + Cys. Jpn. Poult. Sci. 35:182–188.

Bunchasak, C., K. Tanaka, S. Ohtani, and C. M. Collado. 1996. Effect of Met+Cys supplementation to low-protein diet on the growth performance and fat accumulation of broiler chicks at starter period. Anim. Sci. Technol. (Jpn.) 67:956–966.

Carew, L. B., K. G. Evarts, and F. A. Alster. 1998. Growth, feed intake, and plasma thyroid hormone levels in chicks fed dietary excesses of essential amino acids. Poult. Sci. 77:295–298.[Abstract/Free Full Text]

Elliott, H. A., and N. E. Collins. 1982. Factors affecting ammonia release in broiler litter. Trans. ASAE 25:413–418, 424.[Web of Science]

Fancher, B. I., and L. S. Jensen. 1989a. Influence on performance of 3 to 6-wk-old broilers of varying dietary protein contents with supplementation of essential amino acid requirements. Poult. Sci. 68:113–123.[Web of Science][Medline]

Fancher, B. I., and L. S. Jensen. 1989b. Dietary protein level and essential amino acid content: Influence upon female broiler performance during the grower period. Poult. Sci. 68:897–908.[Web of Science][Medline]

Fancher, B. I., and L. S. Jensen. 1989c. Male broiler performance during the starting and growing period as affected by dietary protein, essential amino acids and potassium level. Poult. Sci. 68:1385–1395.[Web of Science][Medline]

Ferguson, N. S., R. S. Gates, J. L. Taraba, A. H. Cantor, A. J. Pescatore, M. L. Straw, M. J. Ford, and D. J. Burnham. 1998. The effect of dietary protein and phosphorus on ammonia concentration and litter composition in broilers. Poult. Sci. 77:1085–1093.[Abstract/Free Full Text]

Han, Y., and D. H. Baker. 1993. Effects of excess methionine or lysine for broilers fed a corn-soybean meal diet. Poult. Sci. 72:1070–1074.[Web of Science][Medline]

Han, Y., H. Suzuki, C. M. Parson, and D. H. Baker. 1992. Amino acid fortification of a low-protein corn and soybean meal diet for chicks. Poult. Sci. 71:1168–1178.[Web of Science][Medline]

Hevia, P., and A. J. Clifford. 1977. Protein intake, uric acid metabolism and protein efficiency ratio in growing chicks. J. Nutr. 107:959–964.[Abstract/Free Full Text]

Ishihard, A., K. Kurahasi, and H. Uihard. 1972. Enzymatic determination of ammonia in blood and plasma. Clin. Chem. Acta. 41:255–261.[CrossRef][Web of Science][Medline]

Kumta, U. S., and A. E. Harper. 1961. Amino acid balance and imbalance. 7. Effects of dietary additions of amino acids on feed intake and blood urea concentration of rats fed low-protein diets containing fibrin. J. Nutr. 74:139–147.[Abstract/Free Full Text]

Kumta, U. S., and A. E. Harper. 1962. Amino acid balance and imbalance. 4. Effect of amino acid imbalance on blood amino acid pattern. Proc. Soc. Exp. Biol. Med. 110:512–517.[CrossRef][Medline]

Lardy, H. A., and G. Fedott. 1950. The net utilization of ammonium nitrogen by the growing rat. J. Biol. Chem. 186:85–91.[Free Full Text]

Leclercq, B., A. M. Chagneau, T. Cochard, and J. Khoury. 1994. Parative responses of genetically lean and fat chickens to lysine, argentine and non-essential amino acid supply. Br. Poult. Sci. 35:687–696.[CrossRef][Web of Science][Medline]

Lemme, A., V. Ravindran, and W. L. Bryden. 2004. Ileal digestibility of amino acids in feed ingredients for broilers. World’s Poult. Sci. J. 60:423–437.[CrossRef][Web of Science]

Leung, P. M.-B., and Q. R. Rogers. 1969. Food intake: Regulation by plasma amino acid pattern. Life Sci. 8:1–9.[Medline]

Liddle, L., J. E. Seegmillu, and L. Loster. 1959. The enzymatic spectrophotometric method for the determination of uric acid. J. Lab. Clin. Med. 54:903–908.[Web of Science][Medline]

Marchesini, G., G. P. Bianchi, H. Vilstrup, G. A. Checchia, D. Patrono, and M. Zoli. 1987. Plasma clearances of branched-chain amino acids in control subjects and in patients with cirrhosis. J. Hepatol. 4:108–117.[CrossRef][Web of Science][Medline]

Moran, E. T. Jr., and H. L. Stilborn. 1996. Effect of glutamic acid on broilers given submarginal crude protein with adequate essential amino acids using feeds high and low in potassium. Poult. Sci. 75:120–129.[Web of Science][Medline]

Ngo, A., C. N. Coon, and G. R. Beecher. 1977. Dietary glycine requirement for growth and cellular development in chicks. J. Nutr. 107:1800–1808.[Abstract/Free Full Text]

Noda, K. 1975. Possible effect of blood ammonia on feed intake of rats fed amino acid imbalanced diets. J. Nutr. 105:508–516.[Abstract/Free Full Text]

NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC.

Panksepp, J., and D. A. Booth. 1971. Decreased feeding after injections of amino acids into the hypothalamus. Nature 233:341–342.[CrossRef][Web of Science][Medline]

Parr, J. F., and J. D. Summers. 1991. The effects of minimizing amino acid excesses in broiler diets. Poult. Sci. 70:1540–1549.[Web of Science][Medline]

Peng, Y., and A. E. Harper. 1970. Amino acid balance and food intake: Effect of different dietary amino acid patterns on the plasma amino acid pattern of rats. J. Nutr. 100:429–437.[Abstract/Free Full Text]

Reeves, J. B. III, and J. S. Van Kessel. 2000. Near-infrared spectroscopic determination of carbon, total nitrogen, and ammonium-N in dairy manures. J. Dairy Sci. 83:1829–1836.[Abstract]

Rosebrough, R. W., S. M. Poch, B. A. Russell, and M. P. Richards. 2002. Dietary protein regulates in vitro lipogenesis and lipogenic gene expression in broilers. Comp. Biochem. Physiol. 132A:423–432.[Medline]

Russek, M. 1971. Hepatic receptors and the neurophysiological mechanisms controlling feeding behavior. Neurosci. Res. 4:214–282.

SAS Institute. 2004. SAS Version 9.1. SAS Institute Inc., Cary, NC.

Schimke, R. T. 1963. Study on factors affecting the level of urea cycle enzymes in rat liver. J. Biol. Chem. 238:1012–1018.[Free Full Text]

Schutte, J. B., W. Smink, and M. Pack. 1997. Requirement of young broiler chicks for glycine + serine. Arch. Geflugelkd. 61:43–47.

Si, J., C. A. Fritts, P. W. Waldroup, and D. J. Burnham. 2004. Effects of tryptophan to large neutral amino acid ratios and overall amino acid levels on utilization of diets low in crude protein by broilers. J. Appl. Poult. Res. 13:570–578.[Abstract/Free Full Text]

Sonne, J. C., J. M. Buchanan, and A. M. Delluva. 1946. Biological precursors of uric acid carbon. J. Biol. Chem. 166:395–396.[Free Full Text]

Waldroup, P. W., Q. Jiang, and C. A. Fritts. 2005. Effects of glycine and threonine supplementation on performance of broiler chicks fed diets low in crude protein. Int. J. Poult. Sci. 4:250–257.

Yamazaki, M., H. Murakami, K. Nakashima, H. Abe, and M. Takemasa. 2006. Effect of excess essential amino acids in low protein diet on abdominal fat deposition and nitrogen excretion of the broiler chicks. Jpn. Poult. Sci. 43:150–155.[CrossRef]

Yamazaki, M., H. Murakami, and M. Takemasa. 1998. Effects of ratios of essential amino acids to nonessential amino acids in low protein diet on nitrogen excretion and fat deposition of broiler chicks. Jpn. Poult. Sci. 35:19–26.

Yoshida, A. 1970. Some aspects of recent advances in protein and amino acid nutrition. Eiyo To Shokuryo 23:583–597.

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Namroud, N. F. Articles by Zaghari, M. Search for Related Content PubMed PubMed Citation Articles by Namroud, N. F. Articles by Zaghari, M.