A Review on the Effect of Arginine on Growth Performance, Meat Quality, Intestine Morphology, and Immune System of Broiler Chickens

Document Type : Review Article

Authors

Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

Abstract

For chickens, arginine considered an essential amino acid due to the lack of urea cycle in birds. Arginine deficiency causes growth retardation, higher prevalence of disease due to the malfunction of immune system, and lower gastrointestinal capacity. However, higher levels of arginine in the diet improved growth performance, muscle hypertrophy, and meat quality. Arginine reduces carcass fat accretion by reducing liver lipogenic enzyme expressions and activities, but it improves muscle fat content. As an immunonutrition, feeding arginine shows some immunostimulatory and thymotrophic role and improves both humoral and cellular immunity. Also, in ovo injection of arginine improves both growth and immune function of birds. Arginine also improves insulin, growth hormone, and thyroid hormone secretion and by which, improves growth in a dose dependent manner. Arginine also improves small intestine histomorphology and enzyme activity and then, improves bird digestive system capacity and efficiency. Accordingly, the aim of this review article was to focus on the effects of arginine on growth, immune system, and meat quality of broiler chickens.

Keywords


INTRODUCTION

In 1886, arginine was isolated and named; then, in 1895, its presence in animal protein was reported (Evoy et al. 1998). Also, the antagonistic effects of arginine and lysine were understood in the 1950’s and 1960’s (Balnave and Brake, 2002). The impact of arginine on the immune system was demonstrated from 1983 till now (Khajali and Wideman, 2010) and its impact on the carcass fat reduction was proved from 2005 up to now (Tan et al. 2011; Ebrahimi et al. 2014a). Also, in ovo injection of arginine was first used in broiler chickens as a treatment for pulmonary hypertension disease (Pordel et al. 2018) and then used as a method for improving the growth of poultry (Foye et al. 2006; Foye et al. 2007; Abdolalizadeh Alvanegh et al. 2017; Omidi, 2018). As urea cycle in birds is not functional due to the lack or low activity of key enzymes (lack of carbamoyl phosphate synthase I and low activity of arginase and ornithine transcarbamoylase); accordingly, arginine considered an essential amino acid for chickens (Khajali and Wideman, 2010). Also, due to the high growth rate, arginine requirement of broiler chickens is high to support the growth of broilers (Ball et al. 2007). Arginine requirement depends on the growth stage and health status (Morris, 2004). Arginine requirement was also affected by the antagonistic effect of arginine and lysine, which is due to the competence of these two amino acids in gastrointestinal absorption and renal reabsorption (Balnave and Brake, 2002). Although higher levels of lysine cause growth retardation (Balnave and Brake, 2002), increasing dietary arginine higher than suggested levels improved growth performance of broiler chickens (Kidd et al. 2001; Ebrahimi et al. 2014a). Past researches demonstrated the importance of arginine supplementation for chickens to support meat quality and growth performance (Ansari Pirsaraei et al. 2015; Abdolalizadeh Alvanegh et al. 2017; Ansari Pirsaraei et al. 2018). Also, the improving effect of arginine on the immune system and intestine histomorphology of chickens was proved (Ebrahimi et al. 2014b; Adibmoradi et al. 2015; Ebrahimi et al. 2016a). Based on our knowledge, there is no review article focused on the effects of using arginine in non-ruminant animals and especially broiler chickens. Therefore, this review article was focused on the effects of arginine on growth, immune system, and meat quality of broiler chickens.

 

Arginine and growth performance

Previous researches demonstrated the importance of arginine supplementation on growth performance of chickens (Table 1). The dietary supplementation with arginine improved overall body growth with increasing lean deposition, though without increasing fat accretion of broiler chickens (Castro et al. 2018). Also, higher levels of arginine (100, 153, and 168% digestible L-arginine based on Ross recommendation) improved growth performance, feed efficiency, and thigh and breast muscles, while it reduced carcass fat accretion in broilers (Ebrahimi et al. 2013; Ebrahimi et al. 2014a; Ebrahimi et al. 2014c). In another study, with supplementing 0.45, 0.90, 1.35, and 1.80% arginine to the basal diet indicated that higher levels of arginine (NRC, 1994) improved daily weight gain and feed conversion ratio (Xu et al. 2018). Supplementing 10 g/kg arginine in a maize -soybean basal diet increased body weight gain and relative breast muscle weight, but it decreased carcass abdominal fat pad and skin of ducks (Wu et al. 2011). Fernandes et al. (2009) with increasing arginine levels (1.490, 1.590, 1.690, and 1.790%) reported a linear increase in breast and breast fillet weight and breast fillet thickness at d 7 of starter period. Al-Daraji and Salih (2012) with dietary adding 0.04% and 0.06% arginine reported an increase in carcass weight, carcass efficiency, and breast and thigh weights. In another study, supplementing arginine in the starter (0, 0.67, 1.37, 2.07, and 2.77%), grower (0, 0.53, 1.1, 1.68, and 2.25%), and finisher (0, 0.52, 1.04, 1.56, and 2.08%) diets increased body weight and feed intake (Emadi et al. 2010). Murakami et al. (2012) reported that dietary supplementation of arginine (1.390, 1.490, 1.590, 1.690, and 1.790% digestible arginine) in the diet of broiler chickens improved body weight and feed conversion ratio, while had no effect on feed intake of chickens. Kidd et al. (2001) reported that dietary supplementing with 120% arginine or lysine based on NRC (1994) recommendation increased body weight gain with adding arginine content of the diet (and without adding lysine content). Gao et al. (2017) reported that in ovo injection of L-arginine increased body weight gain of broiler chickens during 1-7 days. Though, Omidi (2018) with in ovo injection of 0.5% arginine reported no effect on body weight of 24 day-old chickens. Abdolalizadeh Alvanegh et al. (2017) with in ovo injection of 1 mL solution of different ratios of L-arginine to L-lysine [75.7 (20 mg L-lysine and 15.14 mg L-arginine), 80.7 (20 mg L-lysine and 16.14 mg L-arginine), 85.7 (20 mg L-lysine and 17.14.14 mg L-arginine), 90.7 (20 mg L-lysine and 18.14 mg L-arginine), and 95.7 (20 mg L-lysine and 19.14 mg L-arginine)] reported the improving effect of treatments (up to 90.7 ratio) on chick weight and their carcass traits. Arginine increases growth performance by several possible mechanisms: 1- arginine is necessary for protein synthesis and growth (Jahanian, 2009; Yao et al. 2008). 2- arginine stimulates the release of insulin, GH, and IGF-1, and by which improves feed intake, protein synthesis and growth (Newsholme et al. 2005; Jahanian, 2009; Xu et al. 2018). 3- polyamines (putrescine, spermidine, and spermine) as a product of arginine have some anabolic functions like improving cell uptake of amino acids and synthesis of proteins (Khajali and Wideman, 2010). 4- nitric oxide as another product of arginine (synthesized by the act of nitric oxide synthase on arginine) stimulate glucose uptake, glucose and fatty acid oxidation, and adipocyte lipolysis (Jobgen et al. 2006).

 

Arginine and meat quality traits

There are few studies in poultry evaluating the effect of arginine on meat quality (Table 1). It was indicated that increasing the dietary arginine levels improved breast muscle crude protein, dry matter, and fat contents (Ebrahimi et al. 2014a). Jiao et al. (2010) with evaluating four dietary levels of arginine (80, 100, 120, 140% of NRC recommendation) indicated that increasing dietary arginine improved meat lightness, while decreased meat shear force with no effect on collagen content. Wu et al. (2011) indicated that arginine supplementation enhanced intramuscular fat content of duck breast muscle. Also, reducing effect of arginine was observed on shear force and pH of broiler meat (Ebrahimi et al. 2015; Ebrahimi et al. 2016b). Results of gene expression indicated higher expression of lipogenic genes in muscles (fatty acid synthase and lipoprotein lipase), while lower expression of lipogenic enzymes in adipose tissue (fatty acid synthase and lipoprotein lipase) and liver (acetyl-coenzyme A carboxylase, fatty acid synthase, and malic enzyme), (Ebrahimi et al. 2014a; Ansari Pirsaraei et al. 2018).

 

Table 1 Effects of arginine on broiler chickens

P: stands for positive effect; N: stands for negative effects; L: stands for lacking effect and –: stands for not being evaluated in the article.

 

In another study, dietary arginine supplementation increased myofiber diameter of broiler chickens (Fernandes et al. 2009). On the other hand, in ovo injection of 0.5% arginine had no effect on breast meat pH, shear force, and meat color [a* (the index of meat redness), b* (the index of meat yellowness), L* (the index of meat lightness)], (Omidi, 2018). Also, in pig adding 1% arginine increased the antioxidative capacity of skeletal muscle along with increasing intramuscular fat content (Ma et al. 2010). Another study in pig indicated that arginine supplementation increased muscle pH and muscle protein, glycogen, and fat contents, while reduced muscle lactate content (Tan et al. 2009).

 

Arginine and intestine morphology

L-arginine plays an important role in intestinal physiology (Table 1), (Rhoads and Wu, 2009). It was indicated that arginine has an improving effect on intestinal absorption and villous recovery after injury (Wang et al. 2009). Tan et al. (2014) reported that arginine enriched diets reduced damages induced by coccidia (intestinal villous damage, crypt dilation, and goblet cell depletion) in broiler chickens. Also, higher levels of dietary arginine improved small intestine weight and length, villous height, and crypt depth, but these levels decreased villous height to crypt depth ratio, epithelium thickness, and goblet cell number of small intestine of broiler chickens (Ebrahimi et al. 2014b; Adibmoradi et al. 2015; Ebrahimi et al. 2016a). Murakami et al. (2012) reported no effect of dietary arginine supplementation on weight and length of small intestine, but an increase in villous height to crypt depth ratio and a decrease in crypt depth of broiler chickens. In ovo injection of different L-arginine to L-lysine ratios also increased small intestine length, relative weight of small intestine, villous height, and villous height to crypt depth ratio, but it decreased crypt depth of a day old broiler chicks (Ebrahimi et al. 2018). Gao et al. (2017) with in ovo injection of 1% L-arginine reported higher duodenum villous height and villous height to crypt depth ratio, while lower crypt depth of broiler chicks. Also, they reported higher duodenal vasoactive intestinal peptide, ghrelin, and glucagon-like peptide 2 concentrations as well as higher duodenal mucosal enzyme activities (maltase, sucrose, alkaline phosphatase, and inducible nitric oxide synthase) of chicks (Gao et al. 2017). Omidi (2018) with in ovo injection of 0.5% L-arginine reported higher jejunum and duodenum villous height to crypt depth ratios of 24 days old broiler chickens. Other studies also indicated improving effect of in ovo injection of arginine on small intestine morphology parameters and intestine enzyme activities and so, on the digestive tract capacity of chickens (Foye et al. 2007; Edwards et al. 2016). Regardless, a study in rats indicated that dietary arginine supplementation reduced small intestine disaccharidase activity (Taboada et al. 2006). Higher villous height and villous height to crypt depth ratio are considered indicators for higher protein synthesis and cellular proliferation of intestinal epithelium (Chang et al. 2015). In pigs, Wu et al. (2010) reported higher small intestinal growth, villous height, crypt depth, and goblet cell number with feeding diets supplemented with 0.6% arginine. In another study, dietary supplementation of 1% L-arginine increased villous height and vascular endothelial growth factor in duodenal, jejunal, and ileal mucosae (Yao et al. 2011). Part of improving effects of arginine on small intestine morphology may be mediated by polyamines and their effect on protein synthesis, proliferation, and migration of intestinal cells and then, an increase in intestinal villous height and crypt depth (Ruemmele et al. 1999; Wang et al. 2009; Khajali and Wideman, 2010; Wu et al. 2010). Also, an increase in vascular endothelial growth factor in small intestine may improve the growth of gastrointestinal tract (Yao et al. 2011). Tan et al. (2010) reported the molecular mechanism by which arginine increases intestinal cells’ protein synthesis and reduces protein degradation through activating mammalian target of rapamycin (mTOR) and Toll-like receptor 4 (TLR4) signaling pathways. Pluske et al. (1997) reported that higher villous height and lower crypt depth increases performance by increasing the digestive and absorptive capacity of small intestine. Also, it was reported that arginine and nitrite oxide (as one of the arginine product) both stimulate intestinal epithelial cell proliferation and migration (Rhoads and Wu, 2009). Additionally, dietary arginine supplementation stimulated growth hormone, insulin-like growth factors-1, and insulin secretions, which in turn can improve intestinal growth (Xu et al. 2018). As intestinal development of broiler chickens occurs during the last stages of incubation, in ovo injection of nutrients per se can improve early gastrointestinal development and function of hatchlings, and then cause higher digestion and absorption during the growth period (Ebrahimi et al. 2017). Besides digestion and ingestion, another function of the gastrointestinal tract is a barrier against antigens within the lumen; then, an increase in intestinal permeability causes critical illnesses (Gatt et al. 2007). It was indicated that arginine reduced intestinal permeability, while improved intestinal barrier function (Schleiffer and Raul, 1996; Viana et al. 2010). Nutrition is an important modulator of gut microbial community structure. L-arginine supplementation had beneficial effects on gut mucosa by improving innate immunity, barrier function, and ileal microbial community, but it suppressed Clostridium perfringens colonization and gut injury inbroiler chickens (Zhang et al. 2017; Zhang et al. 2018), (Table 1). Feeding arginine in turkeys also improved Lactobacillus of cecum and Clostridium and Coliform of small intestine (Oso et al. 2017). In a study, it was indicated that in ovo injection of 0.5% arginine increased cecum Lactobacillus acidophilus (gram-positive bacteria), while decreased Coliforms and E. coli (cecum gram-negative bacteria), (Omidi, 2018).

 

Arginine and immune system

A practical solution for improving the immune system against pathogens is using nutrients in broiler chickens (Kidd, 2004). Recently, the immunomodulatory effects of arginine on the immune system were proved (Kirk et al. 1992), (Table 1). It was indicated that early arginine supplementation improves the development of the immune system (Corzo and Kidd, 2003). D’Amato and Humphrey (2010) reported that the addition of L-arginine in broiler diet improved peripheral blood B cells and the percentage of monocytes. Adding dietary L-arginine in poultry also prevented the impact of oxidative stress during heat stress conditions (Attia et al. 2011). It was indicated that high dietary arginine levels increased thymus and spleen relative weights, and skin reaction to phytohemagglutinin P in broiler chickens (Ebrahimi et al. 2014b; Ebrahimi et al. 2016a; Adibmoradi et al. 2015). Tan et al. (2007) reported that supplementing 1% arginine reduced the incidence of ascites in broilers exposed to low ambient temperature. Xu et al. (2018) reported that dietary arginine supplementation in broiler chickens increased serum concentrations of IgA, IFN-γ, thymus weight, lymphocyte proliferation, antibody titers to Newcastle disease, and serum IgM concentration. Deng et al. (2005) reported that high levels of arginine increased antibody levels against sheep red blood cells, while reduced relative bursa weight. Kwak et al. (2001) reported that arginine deficiency decreased nitric oxide production of macrophages. It was indicated that high levels of arginine increased CD8+ cells, the absolute number of heterophils, and the ratio of heterophils to lymphocytes in broiler chickens challenged with infectious bronchitis virus (Lee et al. 2002). Emadi et al. (2011) reported that higher levels of arginine increased interferon-α, interferon-γ, and immunoglobulin G. High levels of arginine also improved lymphoid organ weights, humoral immunity, and cellular mediated immune response of broiler chicks (Munir et al. 2009; Ruiz-Feria and Abdukalykova, 2009). Although in ovo injection of different ratios of L-arginine to L-lysine increased bursa of fabricius weight (Ebrahimi et al. 2018), in ovo injection of 0.5% arginine had no effect on immune system organs (thymus, spleen, and bursa of fabricius) or antibody titers against Newcastle (Omidi, 2018). Immunomodulatory actions of arginine mediated by two pathways: 1- arginase pathway, in which polyamines produced as one of the products of arginine; thus, polyamines increase lymphocyte mitogenesis and arginine-dependent macrophage-mediated tumor cell cytotoxicity (Evoy et al. 1998), and 2- nitric oxide pathway, which is a product of arginine as a result of nitric oxide synthase (Khajali and Wideman, 2010). Nitric oxide production of macrophages enhances by increasing arginine levels and causes an improvement in weight and function of thymus and mitogenesis of lymphocyte (Evoy et al. 1998; Sung et al. 1991). Nitric oxide improves coagulation, the immune system, the maintenance of vascular tone, sepsis, hypertension, and cirrhosis (Evoy et al. 1998; Jahanian, 2009).

 

Arginine and some blood parameters

Increasing dietary arginine causes some changes in blood parameters (Table 1). Arginine increases growth hormone (GH) release and stimulates the release of insulin from pancreas (Ebrahimi et al. 2013). A blood glucose level also increases with increasing arginine levels, which is as the result of higher gluconeogenesis (Corzo and Kidd, 2003). It was indicated that arginine reduced blood cholesterol, low-density lipoprotein (LDL), and also insulin resistance in diabetes (Mohan and Cas, 1998). Dietary arginine supplementation increased serum concentrations of growth hormone, insulin-like growth factors-I, and insulin of broiler chickens (Xu et al. 2018). Higher levels of arginine in the diet of broiler chickens increased plasma triiodothyronine, thyroxine, and the ratio of triiodothyronine to thyroxine, but decreased plasma cholesterol, triglyceride, and urea concentrations (Ebrahimi et al. 2013; Ebrahimi et al. 2015; Ansari Pirsaraei et al. 2015; Ebrahimi et al. 2016b). Emadi et al. (2011) reported that arginine supplementation increased albumin and total protein, while decreased aspartate aminotransferase, lactic dehydrogenase, alkaline phosphatase, cholesterol, and triglyceride. Ansari Pirsaraei et al. (2018) with increasing dietary arginine levels (100, 124, 139, and 154%) reported higher blood glucose and high-density lipoprotein (HDL) levels, while lower cholesterol, triglyceride, and low-density lipoprotein (LDL) levels in Arian broilers. In ovo injection of different ratios of L-arginine to L-lysine improved serum total protein level, while decreased serum blood urea nitrogen of broiler chicks (Abdolalizadeh Alvanegh et al. 2017). On the other hand, 0.5% L-arginine in ovo injection had no effect on serum glucose, total protein, cholesterol, and blood urea nitrogen (Omidi, 2018).

 

CONCLUSION

Arginine considered an essential amino acid for chickens due to the lack of urea cycle and high growth rate. Arginine requirement depends on the growth stage, health status, and dietary lysine level (because of the antagonistic effect of arginine and lysine). Arginine supplementation improved growth performance and meat production of chickens. Increasing the dietary arginine levels also improved meat quality traits (especially meat tenderness and meat fat content). Also, previous studies indicated the improving effect of arginine on intestinal growth, intestinal histology (especially villous height to crypt depth ratio), enzyme activities, and gut microflora community. Furthermore, the stimulatory effects of arginine on the immune system was proved. Arginine supplementation also increased blood GH, insulin, insulin-like growth factors-I, and thyroid hormones. Main effects of arginine mediated by stimulating hormonal secretion and producing polyamines and nitric oxide.

Abdolalizadeh Alvanegh F., Ebrahimi M. and Daghigh Kia H. (2017). Effect of in ovo injection of different ratios of L-arginine to L-lysine on body growth, muscle production, and blood metabolites concentration of day old Ross broiler chicks. Iranian J. Anim. Sci. 48, 207-217.
Adibmoradi M., Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z., Tebianian M. and Nourijelyani K. (2015). The effects of L-arginine on growth, small intestine, and immune system of broilers in starter period. Iranian J. Anim. Sci. 45, 223-233.
Al-Daraji H.J. and Salih A.M. (2012). Effect of dietary L-arginine on carcass traits of broilers. Res. Opin. Anim. Vet. Sci. 2, 40-44.
Ansari Pirsaraei Z., Ebrahimi M., Zare Shahneh A., Shivazad M. and Tebianian M. (2015). Determination of the best dietary level of L-arginine on improving growth performance, carcass traits and blood parameters in broiler chickens in the starter and grower periods. Res. Anim. Prod. 6, 87-95.
Ansari Pirsaraei Z., Rahimi A., Deldar H., Sayyadi A.J., Ebrahimi M., Zareh Shahneh A., Shivazad M. and Tebianian M. (2018). Effect of feeding arginine on the growth performance, carcass traits, relative expression of lipogenic genes, and blood parameters of Arian broilers. Brazilian J. Poult. Sci. 20, 363-370.
Attia Y.A, Hassan R.A., Tag El-Din A.E. and AbouShehema B.M. (2011). Effect of ascorbic acid or increasing metabolizable energy level with or without supplementation of some essential amino acids on productive and physiological traits of slow growing chicks exposed to chronic heat stress. J. Anim. Physiol. Anim. Nutr. 95, 744-755.
Ball R.O., Urschel K.L. and Pencharz P.B. (2007). Nutritional consequences of interspecies differences in arginine and lysine metabolism. J. Nutr. 137, 1626-1641.
Balnave D. and Brake J. (2002). Re-evaluation of the classical dietary arginine: lysine interaction for modern poultry diets: A review. World’s Poult. Sci. J. 58, 275-289.
Castro F.L.S., Su S., Choi H., Koo E. and Kim W.K. (2018). L-Arginine supplementation enhances growth performance, lean muscle, and bone density but not fat in broiler chickens. Poult. Sci. 98, 1716-1722.
Chang Y., Cai H., Liu G., Chang W., Zheng A., Zhang S., Liao R., Liu W., Li Y. and Tian J. (2015). Effects of dietary leucine supplementation on the gene expression of mammalian target of rapamycin signaling pathway and intestinal development of broilers. Anim. Nutr. 1, 313-319.
Corzo A. and Kidd M.T. (2003). Arginine needs of the chick and growing broiler. Int. J. Poult. Sci. 2, 379-382.
D’Amato J.L. and Humphrey B.D. (2010). Dietary arginine levels alter markers of arginine utilization in peripheral blood mononuclear cells and thymocytes in young broiler chicks. Poult. Sci. 89, 938-947.
Deng K., Wong C.W. and Nolan J.V. (2005). Long-term effects of early life L-arginine supplementation on growth performance, lymphoid organs and immune responses in Leghorn-type chickens. British Poult. Sci. 46, 318-324.
Ebrahimi M., Abdolalizadeh Alvanagh F., Adibmoradi M., Janmohammadi H. and Rajabi Z. (2018). The impact of in ovo feeding with different L-arginine to L-lysine ratios on small intestine histological characteristics and immune system organs in day-old chicks. Anim. Sci. Res. 2, 177-191.
Ebrahimi M., Janmohammadi H., Daghigh Kia H., Moghaddam G., Rajabi Z., Rafat S.A. and Javanmard A. (2017). The effect of L-lysine in ovo feeding on body weight characteristics and small intestine morphology in a day-old Ross broiler chicks. Revue Méd. Vét. 168, 116-124.
Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z. and Ghafari Balesini M. (2016a). The effects of dietary L-arginine on some parameters of meat quality, intestine histology and immune system of 46-d old broiler chickens. Anim. Sci. Res. 26, 83-96.
Ebrahimi M., Zare Shahneh A., Shivazad M. and Ansari Pirsaraei Z. (2016b). Evaluation of 24 days feeding L-arginin on performance, meat quality and blood metabolites in broilers. Anim. Sci. Res. 25, 61-72.
Ebrahimi M., Zare Shahneh A., Shivazad M. and Ansari Pirsaraei Z. (2015). The effects of feeding high levels of L-arginine at the starter period on meat production and its quality, and blood parameters in broiler chicks. Iranian J. Anim. Sci. Res. 46, 169-179.
Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z., Tebianian M., Ruiz-Feria C.A., Adibmoradi M., Nourijelyani K. and Mohamadnejad F. (2014a). The effect of feeding excess arginine on lipogenic gene expression and growth performance in broilers. British Poult. Sci. 55, 81-88.
Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z., Tebianian M., Adibmoradi M. and Nourijelyani K. (2014b). The effects of high levels of L-arginine on performance, morphology of small intestine and immune system organs of broilers during the growth period. Anim. Sci. Res. 24, 95-107.
Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z., Tebianian M., Adibmoradi M. and Nourijelyani K. (2014c). The effects of L-arginine supplement on growth, meat production, and fat deposition in broiler chickens. Iranian J. Anim. Sci. Res. 5, 281-290.
Ebrahimi M., Zare Shahneh A., Shivazad M., Ansari Pirsaraei Z., Tebianian M., Adibmoradi M. and Nourijelyani K. (2013). Evaluation of the effect of feeding L-arginine on growth performance, carcass traits and blood parameters in broiler chickens. Iranian J. Anim. Sci. Res. 44, 157-166.
Edwards N.M., Heberle N.D. and Hynd P.I. (2016). The effect of in ovo administration of L-arginine on the hatchability and embryological development of broiler chicks. Pp. 24-28 in Proc. Aust. Soc. Anim. Prod.,Adelaide, Australia.
Emadi M., Jahanshiri F., Kaveh K., Hair-Bejo M., Ideris A. and Alimon A.R. (2011). Nutrition and immunity: The effects of the combination of arginine and tryptophan on growth performance, serum parameters and immune response in broiler chickens challenged with infectious bursal disease vaccine. Avian Pathol. 40, 63-72.
Emadi M., Kaveh K., Bejo M.H., Ideris A., Jahanshiri F., Ivan M. and Alimon R.A. (2010). Growth performance and blood parameters as influenced by different levels of dietary arginine in broiler chickens. J. Anim. Vet. Adv. 9, 70-74.
Evoy D., Lieberman M.D., Fahey III T.J. and Daly J.M. (1998). Immunonutrition: The role of arginine. Nutrition. 14, 611-617.
Fernandes J.I.M., Murakami A.E., Martins E.N., Sakamoto M.I. and Garcia E.R.M. (2009). Effect of arginine on the development of the pectoralis muscle and the diameter and the protein: deoxyribonucleic acid rate of its skeletal myofibers in broilers. Poult. Sci. 88, 1399-1406.
Foye O.T., Ferket P.R. and Uni Z. (2007). The effects of in ovo feeding arginine, β-hydroxy-β-methyl-butyrate, and protein on jejunal digestive and absorptive activity in embryonic and neonatal turkey poults. Poult. Sci. 86, 2343-2349.
Foye O.T., Uni Z., McMurty J.P. and Freket P.R. (2006). The effects of nutrient administration, "in ovo feeding" of arginine and / or β-hydroxy-β-methyle butyrate (HMB) on insulin–like growth factors, energy metabolism and growth in turkey poults. Int. J. Poult. Sci. 5, 309-317.
Gao T., Zhao M.M., Li Y.J., Zhang L., Li J.L., Yu L.L., Gao F. and Zhou G.H. (2017). Effects of in ovo feeding of L-arginine on the development of digestive organs, intestinal function and post-hatch performance of broiler embryos and hatchlings. J. Anim. Physiol. Anim. Nutr. 2017, 1-10.
Gatt M., Reddy B.S. and MacFie J. (2007). Review article: Bacterial translocation in the critically ill-evidence and methods of prevention. Aliment. Pharmacol. Therapeut. 25, 741-757.
Jahanian R. (2009). Immunological responses as affected by dietary protein and arginine concentrations in starting broiler chicks. Poult. Sci. 88, 1818-1824.
Jiao P., Guo Y., Yang X. and Long F. (2010). Effects of dietary arginine and methionine levels on broiler carcass traits and meat quality. J. Anim. Vet. Adv. 9, 1546-1551.
Jobgen W.S., Fried S.K., Fu W.J., Meininger C.J. and Wu G. (2006). Regulatory role for the arginine–nitric oxide pathway in metabolism of energy substrates. J. Nutr. Biochem. 17, 571-588.
Khajali F. and Wideman R.F. (2010). Dietary arginine: metabolic, environmental, immunological and physiological interrelationships. World's Poult. Sci. J. 66, 751-766.
Kidd M.T. (2004). Nutritional modulation of immune function in broilers. Poult. Sci. 83, 650-657.
Kidd M.T., Peebles E.D., Whitmarsh S.K., Yeatman J.B. and Wideman R.F. (2001). Growth and immunity of broiler chicks as affected by dietary arginine. Poult. Sci. 80, 1535-1542.
Kirk S.J., Regan M.C., Wasserkrug H.L., Sodeyama M. and Barbul A. (1992). Arginine enhances T-cell responses in athymic nude mice. J. Parenter. Enteral. Nutr. 16, 429-432.
Kwak H., Austic R.E. and Dietert R.R. (2001). Arginine-genotype interactions and immune status. Nutr. Res. 21, 1035-1044.
Lee J.E., Austic R.E., Naqi S.A., Golemboski K.A. and Dietert R.R. (2002). Dietary arginine intake alters avian leukocyte population distribution during infectious bronchitis challenge. Poult. Sci. 81, 793-798.
Ma X., Lin Y., Jiang Z., Zheng C., Zhou G., Yu D., Cao T., Wang J. and Chen F. (2010). Dietary arginine supplementation enhances antioxidative capacity and improves meat quality of finishing pigs. Amino Acids. 38, 95-102.
Mohan I. and Cas U. (1998). Effect of L-arginine nitric oxide system on chemical induced diabetes mellitus. Free Radic. Biol. Med. 25, 757-765.
Morris S.M. (2004). Enzymes of arginine metabolism. J. Nutr. 134, 2743-2747.
Munir K., Muneer M.A., Masaoud E., Tiwari A., Mahmud A., Chaudhry R.M. and Rashid A. (2009). Dietary arginine stimulates humoral and cell-mediated immunity in chickens vaccinated and challenged against hydropericardium syndrome virus. Poult. Sci. 88, 1629-1638.
Murakami A.E., Fernandes J.I., Hernandes L. and Santos T.C. (2012). Effects of starter diet supplementation with arginine on broiler production performance and on small intestine morphometry. Pesq. Vet. Bras. 32, 259-266.
Nayak N., Rajini R.A., Ezhilvalavan S., Sahu A.R. and Kirubaharan J.J. (2016). Influence of in ovo arginine feeding on post-hatch growth performance and economics of broilers. J. Anim. Res. 6, 585-591.‏
Newsholme P., Brennan L., Blanca R.U.B.I. and Maechler P. (2005). New insights into amino acid metabolism, β-cell function and diabetes. Clin. Sci. 108, 185-194.
NRC. (1994). Nutrient Requirements of Poultry, 9th Rev. Ed. National Academy Press, Washington, DC., USA.
Omidi S. (2018). The effect of in ovo injection with L-arginine on growth performance, meat quantity and quality, blood metabolites, and intestine histomorphology in broilers. MS Thesis. University of Tabriz, Tabriz, Iran.
Oso A.O., Williams G.A., Oluwatosin O.O., Bamgbose A.M., Adebayo A.O., Olowofeso O., Pirgozliev V., Adegbenjo A.A., Osho S.O., Alabi J.O. and Li F. (2017). Effect of dietary supplementation with arginine on haematological indices, serum chemistry, carcass yield, gut microflora, and lymphoid organs of growing turkeys. Livest. Sci. 198, 58-64.
Pluske J.R., Hampson D.J. and Williams I.H. (1997). Factors influencing the structure and function of the small intestine in the weaned pig-a review. Livest. Prod. Sci. 51, 215-236.
Pordel O., Khazali H., Rokni H. and Hosseini A. (2018). Administration of different levels of arginine and lysine coupled with copper for change the copper concentration of milk in the lactating Zandi’s ewes. Iranian J. Appl. Anim. Sci. 8(2), 241-246.
Rhoads J.M. and Wu G. (2009). Glutamine, arginine, and leucine signaling in the intestine. Amino Acids. 37, 111-122.
Ruemmele F.M., Ruemmele C., Levy E. and Seidman E. (1999). Les mécanismes moléculaires de la régulation du renouvellement de cellules épithéliales intestinales par des nutriments. Gastroenterol. Clin. Biol. 23, 47-55.
Ruiz-Feria C.A. and Abdukalykova S.T. (2009). Arginine and vitamin E improve the antibody responses to infectious bursal disease virus (IBDV) and sheep red blood cells in broiler chickens. British Poult. Sci. 50, 291-297.
Schleiffer R. and Raul F. (1996). Prophylactic administration of L-arginine improves the intestinal barrier function after mesenteric ischaemia. Gut. 39, 194-198.
Sung Y.J., Hotchkiss J.H., Austic R.E. and Dietert R.R. (1991). L-arginine dependent production of a reactive nitrogen intermediate by macrophages of a uricotelic species. J. Leukoc. Biol. 50, 49-56.
Taboada M.C., Rodriguez B., Millán R. and Míguez I. (2006). Role of dietary L-arginine supplementation on serum parameters and intestinal enzyme activities in rats fed an excess-fat diet. Biomed. Pharmacother. 60, 10-13.
Tan J., Applegate T.J., Liu S., Guo Y. and Eicher S.D. (2014). Supplemental dietary L-arginine attenuates intestinal mucosal disruption during a coccidial vaccine challenge in broiler chickens. British J. Nutr. 112, 1098-1109.
Tan X., Sun W.D., Li J.C., Pan J.Q., Liu Y.J., Wang J.Y. and Wang X.L. (2007). L-arginine prevents reduced expression of endothelial nitric oxide synthase (NOS) in pulmonary arterioles of broilers exposed to cool temperatures. Vet. J. 173, 151-157.
Tan B., Yin Y., Kong X., Li P., Li X., Gao H., Li X., Huang R. and Wu G. (2010). L-arginine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids. 38, 1227-1235.
Tan B., Yin Y., Liu Z., Li X., Xu H., Kong X., Huang R., Tang W., Shinzato I., Smith S.B. and Wu G. (2009). Dietary L-arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids. 37, 169-175.
Tan B., Yin Y., Liu Z., Tang W., Xu H., Kong X., Li X., Yao K., Gu W., Smith S.B. and Wu G. (2011). Dietary L-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. J. Nutr. Biochem. 22, 441-445.
Tayade C., Koti M. and Mishra S.C. (2006). L-arginine stimulates intestinal intraepithelial lymphocyte functions and immune response in chickens orally immunized with live intermediate plus strain of infectious bursal disease vaccine. Vaccine. 24, 5473-5480.
Viana M.L., Santos R.G., Generoso S.V., Arantes R.M., Correia M.I.T. and Cardoso V.N. (2010). Pretreatment with arginine preserves intestinal barrier integrity and reduces bacterial translocation in mice. Nutrition. 26, 218-223.
Wang W.W., Qiao S.Y. and Li D.F. (2009). Amino acids and gut function. Amino Acids. 37, 105-110.
Wu L.Y., Fang Y.J. and Guo X.Y. (2011). Dietary L-arginine supplementation beneficially regulates body fat deposition of meat-type ducks. British Poult. Sci. 52, 221-226.
Wu X., Ruan Z., Gao Y., Yin Y., Zhou X., Wang L., Geng M., Hou Y. and Wu G. (2010). Dietary supplementation with L-arginine or N-carbamyl glutamate enhances intestinal growth and heat shock protein-70 expression in weanling pigs fed a corn- and soybean meal-based diet. Amino Acids. 39, 831-839.
Xu Y.Q., Guo Y.W., Shi B.L., Yan S.M. and Guo X.Y. (2018). Dietary arginine supplementation enhances the growth performance and immune status of broiler chickens. Livest. Sci. 209, 8-13.
Yao K., Guan S., Li T., Huang R., Wu G., Ruan Z. and Yin Y. (2011). Dietary L-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. British J. Nutr. 105, 703-709.
Yao K., Yin Y.L., Chu W., Liu Z., Deng D., Li T., Huang R., Zhang J., Tan B., Wang W. and Wu G. (2008). Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. J. Nutr. 138, 867-872.
Zhang B., Lv Z., Li H., Guo S., Liu D. and Guo Y. (2017). Dietary l-arginine inhibits intestinal Clostridium perfringens colonisation and attenuates intestinal mucosal injury in broiler chickens. British J. Nutr. 118, 321-332.
Zhang B., Lv Z., Li Z., Wang W., Li G. and Guo Y. (2018). Dietary L-arginine supplementation alleviates the intestinal injury and modulates the gut microbiota in broiler chickens challenged by clostridium perfringens. Front. Microbiol. 9, 1716-1716.