Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Influence of dietary glutamine supplementation on performance, biochemical indices and enzyme activities in broilers with cold-induced ascites

Mokhtar Fathi A , Mohammad Heidari A , Ali Asghar Ahmadisefat B , Mahmood Habibian C E and Mohammad Mehdi Moeini D
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, College of Agriculture, Payam-e-Noor University, Tehran, PO Box 193953697, Iran.

B Department of Animal Science, Agricultural Office (Jahad-e-Keshavarzi) of Ravansar, Kermanshah, PO Box 6796135673, Iran.

C Department of Animal Science, Faculty of Agriculture, University of Kurdistan, Sanandaj, PO Box 416, Iran.

D Department of Animal Science, College of Agriculture and Natural Resources, Razi University, Kermanshah, PO Box 6715685418, Iran.

E Corresponding author. Email: mahmood_habibiyan@yahoo.com

Animal Production Science 56(12) 2047-2053 https://doi.org/10.1071/AN15300
Submitted: 24 March 2015  Accepted: 17 July 2015   Published: 4 September 2015

Abstract

This study was conducted to investigate the effects of dietary glutamine supplementation on performance and biochemical indices of broilers with cold-induced ascites. A total of 240 1-day-old male broiler chicks (Ross 308) were randomly allotted to three treatment groups, with four replicate pens per treatment and 20 birds per pen. The control birds were kept in a thermoneutral chamber and fed a basal diet, whereas the other two experimental groups were kept in a cold chamber to induce ascites and fed the basal diet supplemented with either 0 or 100 mg of glutamine/kg. The cold-treated birds consumed less (P < 0.05) feed and had lower (P < 0.05) weight gain compared with the control birds. Dietary glutamine supplementation had no effect (P > 0.05) on broiler performance. The cold-treated birds had higher (P < 0.05) right ventricle to total ventricle ratio and mortality due to ascites compared with the control birds. However, mortality due to ascites and right ventricle to total ventricle ratio was reduced (P < 0.05) by dietary glutamine supplementation. The cold-treated birds had higher (P < 0.05) red blood cell counts, haematocrit percentage and haemoglobin concentration compared with the control birds at 21 and 42 days of age. The activities of plasma lactate dehydrogenase, aspartate aminotransferase and alanine aminotransferase were increased (P < 0.05) in cold-treated birds compared with the control birds at 42 days of age, but dietary glutamine supplementation reduced (P < 0.05) the activities of alanine aminotransferase and aspartate aminotransferase near to the control levels. The plasma and liver glutathione peroxidase activities were increased (P < 0.05) in cold-treated birds compared with the control birds at 21 and 42 days of age, whereas the reverse was true for malondialdehyde concentrations. The glutathione peroxidase activity was increased (P < 0.05), whereas the malondialdehyde concentration was decreased (P < 0.05) by dietary glutamine supplementation compared with the cold-treated birds at 42 days of age. The results indicated that the beneficial effect of glutamine is probably related to its ability to maintain near to normal free radical scavenging enzymes and the level of glutathione peroxidase bioactivity, thereby protecting cell membranes from oxidative damage via decreased lipid peroxidation.

Additional keywords: oxidative stress, pulmonary hypertension.


References

Arab HA, Jamshidi R, Rassouli A, Shams G, Hassanzadeh MH (2006) Generation of hydroxyl radicals during ascites experimentally induced in broilers. British Poultry Science 47, 216–222.
Generation of hydroxyl radicals during ascites experimentally induced in broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVaks7o%3D&md5=d0e88e51871f0fb5471b44537b6703d9CAS | 16641033PubMed |

Askanazi J, Carpentier YA, Michelsen CB, Elwyn DH, Furst P, Kantrowitz LR, Gump FE, Kinney JM (1980) Muscle and plasma amino acids following injury: influence of intercurrent infection. Annals of Surgery 192, 78–85.
Muscle and plasma amino acids following injury: influence of intercurrent infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c3msVegtw%3D%3D&md5=7fa0fb6c65005f63f878a11f55111fb9CAS | 7406567PubMed |

Azizian M, Rahimi S, Kamali MA, Karimi Torshizi MA, Zobdeh MR (2013) Comparison of the susceptibility of six male broiler hybrids to ascites by using hematological and pathological parameters. Journal of Agricultural Science and Technology 15, 517–525.

Baker FJ, Silverton RE (1985) ‘Introduction to medical laboratory technology.’ 6th edn. (Butterworth-Heinemann: Boston, MA)

Balog JM, Kidd BD, Huff WE, Huff GR, Rath NC, Anthony NB (2003) Effect of cold stress on broilers selected for resistance or susceptibility to ascites syndrome. Poultry Science 82, 1383–1387.
Effect of cold stress on broilers selected for resistance or susceptibility to ascites syndrome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svis1GmsA%3D%3D&md5=c42db0a6c13497d237923e581579a164CAS | 12967249PubMed |

Bottje WG, Wideman RF (1995) Potential role of free radicals in the pathogenesis of pulmonary hypertension syndrome. Poultry and Avian Biology Reviews 6, 211–231.

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=539ca880a9a715c7159044a1b77823f6CAS | 942051PubMed |

Burton RR, Besch EL, Smith AH (1968) Effect of chronic hypoxia on the pulmonary arterial blood pressure of the chicken. American Journal of Physiology–Legacy Content 214, 1438–1442.

Buys N, Scheele CW, Kwakernaak C, Decuypere E (1999) Performance and physiological variables in broiler chicken lines differing in susceptibility to the ascites syndrome: 2. Effect of ambient temperature on partial efficiencies of protein and fat retention and plasma hormone concentrations. British Poultry Science 40, 140–144.
Performance and physiological variables in broiler chicken lines differing in susceptibility to the ascites syndrome: 2. Effect of ambient temperature on partial efficiencies of protein and fat retention and plasma hormone concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivFSks7s%3D&md5=382bc847f852b5abd9d11b61cb1c7f49CAS | 10405051PubMed |

Daneshyar M, Kermanshahi H, Golian A (2007) Changes of blood gases, internal organ weights and performance of broiler chickens with cold induced ascites. Research Journal of Biological Sciences 2, 729–735.
Changes of blood gases, internal organ weights and performance of broiler chickens with cold induced ascites.Crossref | GoogleScholarGoogle Scholar |

Daneshyar M, Kermanshahi H, Golian A (2009) Changes of biochemical parameters and enzyme activities in broiler chickens with cold-induced ascites. Poultry Science 88, 106–110.
Changes of biochemical parameters and enzyme activities in broiler chickens with cold-induced ascites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlamt7g%3D&md5=12ea244ea0e9caecde29364c85041f87CAS | 19096064PubMed |

Denno R, Rounds JD, Faris R, Holejko LB, Wilmore DW (1996) Glutamine-enriched total parenteral nutrition enhances plasma glutathione in the resting state. The Journal of Surgical Research 61, 35–38.
Glutamine-enriched total parenteral nutrition enhances plasma glutathione in the resting state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xhslyls7o%3D&md5=5dba12057f113870a0ebf240c97a5946CAS | 8769939PubMed |

Enkvetchakul B, Bottje WG, Anthony N, Moore R, Huff W (1993) Compromised antioxidant status associated with ascites in broilers. Poultry Science 72, 2272–2280.
Compromised antioxidant status associated with ascites in broilers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7ktlalug%3D%3D&md5=4eea1ea868f5195d7ab7fb6b1ff6831aCAS | 8309876PubMed |

Fathi M, Nazer Adl K, Ebrahim Nezhad Y, Aghdam Shahryar H, Daneshyar M, Tanha T (2011) The role of oxidative stress in the development of congestive heart failure (CHF) in broilers with pulmonary hypertension syndrome (PHS). Journal of Cell and Animal Biology 5, 176–181.

Geng AL, Guo YM, Yang Y (2004) Reduction of ascites mortality in broilers by coenzyme Q10. Poultry Science 83, 1587–1593.
Reduction of ascites mortality in broilers by coenzyme Q10.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Kjsbw%3D&md5=7e7afdf01a84eb4dcc9e897c3a463f8cCAS | 15384911PubMed |

Grobe AC, Wells SM, Benavidez E, Oishi P, Azakie A, Fineman JR, Black SM (2006) Increased oxidative stress in lambs with increased pulmonary blood flow and pulmonary hypertension: role of NADPH oxidase and endothelial NO synthase. American Journal of Physiology. Lung Cellular and Molecular Physiology 290, L1069–L1077.
Increased oxidative stress in lambs with increased pulmonary blood flow and pulmonary hypertension: role of NADPH oxidase and endothelial NO synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVeitrk%3D&md5=e0b88728cfc7eaf6773ca4daeba8c043CAS | 16684951PubMed |

Halliwell B, Gutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods in Enzymology 186, 1–85.
Role of free radicals and catalytic metal ions in human disease: an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVKrt7Y%3D&md5=c048f882ccf84708a072d17028dca04eCAS | 2172697PubMed |

Hassanzadeh Ladmakhi M, Buys N, Vanderpooten A, Decuypere E (1997) Myocardial β‐adrenergic receptor characteristics in T3‐induced ascites and in broiler lines differing in ascites susceptibility. Avian Pathology 26, 293–303.
Myocardial β‐adrenergic receptor characteristics in T3‐induced ascites and in broiler lines differing in ascites susceptibility.Crossref | GoogleScholarGoogle Scholar |

Havenstein GB, Ferket PR, Qureshi MA (2003) Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1509–1518.
Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3sritlKgug%3D%3D&md5=6533e400ae0cf04b4d5baee8eaf1a5efCAS | 14601726PubMed |

Hearse DJ (1979) Cellular damage during myocardial ischemia: metabolic changes leading to enzyme leakage. In ‘Enzymes in cardiology’. (Eds DJ Hearse, JD Leiris, D Loisance) pp. 1–21. (John Wiley and Sons Ltd: New York, NY)

Hong RW, Rounds JD, Helton WS, Robinson MK, Wilmore DW (1992) Glutamine preserves liver glutathione after lethal hepatic injury. Annals of Surgery 215, 114–119.
Glutamine preserves liver glutathione after lethal hepatic injury.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387ovFeltQ%3D%3D&md5=6443827a7767ac0c3ed0fd7076ff0596CAS | 1546897PubMed |

Huchzermeyer FW, De Ruyck AM (1986) Pulmonary hypertension syndrome associated with ascites in broilers. The Veterinary Record 119, 94
Pulmonary hypertension syndrome associated with ascites in broilers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28zhslGrsg%3D%3D&md5=6edd521443dbc0ac9cfdc12c28ef38fdCAS | 3750788PubMed |

Izadinia M, Nobakht M, Khajali F, Faraji M, Zamani F, Qujeq D, Karimi I (2010) Pulmonary hypertension and ascites as affected by dietary protein source in broiler chickens reared in cool temperature at high altitudes. Animal Feed Science and Technology 155, 194–200.
Pulmonary hypertension and ascites as affected by dietary protein source in broiler chickens reared in cool temperature at high altitudes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGqtbg%3D&md5=bf9e68ecd219b093568b96c510eb7841CAS |

Jain MC (1986) ‘Schalm’s veterinary haematology.’ 4th edn. (Lea and Febiger: Philadelphia, PA)

Julian RJ (1993) Ascites in poultry. Avian Pathology 22, 419–454.
Ascites in poultry.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cvptVGhsA%3D%3D&md5=09203783da6dc7b6a28c005d6adee05aCAS | 18671031PubMed |

Karinch AM, Pan M, Lin CM, Strange R, Souba WW (2001) Glutamine metabolism in sepsis and infection. The Journal of Nutrition 131, 2535S–2538S.

Kumar SHS, Anandan R (2007) Biochemical studies on the cardioprotective effect of glutamine on tissue antioxidant defense system in isoprenaline-induced myocardial infarction in rats. Journal of Clinical Biochemistry and Nutrition 40, 49–55.
Biochemical studies on the cardioprotective effect of glutamine on tissue antioxidant defense system in isoprenaline-induced myocardial infarction in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSqurrO&md5=ba152ec3d20f62c0fc8da3e49a344671CAS |

Kumar SHS, Anandan R, Devaki T, Kumar MS (2001) Cardioprotective effects of Picrorhiza kurroa against isoproterenol-induced myocardial stress in rats. Fitoterapia 72, 402–405.
Cardioprotective effects of Picrorhiza kurroa against isoproterenol-induced myocardial stress in rats.Crossref | GoogleScholarGoogle Scholar |

Luger D, Shinder D, Rzepakovsky V, Rusal M, Yahav S (2001) Association between weight gain, blood parameters, and thyroid hormones and the development of ascites syndrome in broiler chickens. Poultry Science 80, 965–971.
Association between weight gain, blood parameters, and thyroid hormones and the development of ascites syndrome in broiler chickens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFKks7w%3D&md5=8c2410cc5557ba1c3bc00288ba774090CAS | 11469663PubMed |

Maulik N, Engelman DT, Watanabe M, Engelman RM, Rousou JA, Flack JE, Deaton DW, Gorbunov NV, Elsayed NM, Kagan VE, Das DK (1996) Nitric oxide/carbon monoxide. A molecular switch for myocardial preservation during ischemia. Circulation 94, II398–II406.

Maxwell MH, Robertson GW, Spence S (1986) Studies on an ascitic syndrome in young broilers. 1. Haematology and pathology. Avian Pathology 15, 511–524.
Studies on an ascitic syndrome in young broilers. 1. Haematology and pathology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1crnslyitw%3D%3D&md5=4984bff28fef31f3e6668febfd37c8ebCAS | 18766551PubMed |

Maxwell MH, Tullet SG, Burton FC (1987) Haematology and morphological changes in young broiler chicks with experimentally induced hypoxia. Research in Veterinary Science 43, 331–338.

Pan JQ, Tan X, Li JC, Sun WD, Wang XL (2005) Effects of early feed restriction and cold temperature on lipid peroxidation, pulmonary vascular remodelling and ascites morbidity in broilers under normal and cold temperature. British Poultry Science 46, 374–381.
Effects of early feed restriction and cold temperature on lipid peroxidation, pulmonary vascular remodelling and ascites morbidity in broilers under normal and cold temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXls1Slsbg%3D&md5=82fb83c692bb044f53539def52e8eb69CAS | 16050193PubMed |

Peacock AJ, Pickett C, Morris K, Reeves JT (1990) Spontaneous hypoxaemia and right ventricular hypertrophy in fast growing broiler chickens reared at sea level. Comparative Biochemistry and Physiology. Part A, Physiology 97, 537–541.
Spontaneous hypoxaemia and right ventricular hypertrophy in fast growing broiler chickens reared at sea level.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7jvVeisg%3D%3D&md5=000b5e8c42c46494c58e085552e8f001CAS |

Pratt DS, Kaplan MM (2000) Evaluation of abnormal liver-enzyme results in asymptomatic patients. The New England Journal of Medicine 342, 1266–1271.
Evaluation of abnormal liver-enzyme results in asymptomatic patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3ivVOlsQ%3D%3D&md5=e2aaa5a11d275b22b8225713b8175e5fCAS | 10781624PubMed |

Pullicino E (2012) Parenteral glutamine in critical illness: just what the gut needs. Malta Medical Journal 24, 2–7.

Rathore N, John S, Kale M, Bhatnagar D (1998) Lipid peroxidation and antioxidant enzymes in isoproterenol induced oxidative stress in rat tissues. Pharmacological Research 38, 297–303.
Lipid peroxidation and antioxidant enzymes in isoproterenol induced oxidative stress in rat tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFGhu7g%3D&md5=b497d2af67a814811e9e2d1271976b31CAS | 9774493PubMed |

Ross (2007) ‘Broiler nutrition specification.’ (Aviagen: Midlothian, UK)

SAS Institute (2003) ‘User’s guide.’ Release 9.1. (SAS Institute Inc.: Cary, NC)

Walton JP, Julian RJ, Squires EJ (2001) The effect of dietary flax oil and antioxidants on ascites and pulmonary hypertension in broilers using a low temperature model. British Poultry Science 42, 123–129.

Wideman RF, Kirby YK, Ismail M, Bottje WG, Moore RW, Vardeman RC (1995) Supplemental L-arginine attenuates pulmonary hypertension syndrome (ascites) in broilers. Poultry Science 74, 323–330.
Supplemental L-arginine attenuates pulmonary hypertension syndrome (ascites) in broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXks1Slt7g%3D&md5=2307a44a85f36ce908ee35fd12acbfe6CAS | 7724455PubMed |

Wideman RF, Kirby YK, Forman M, Tacket CD, Marson NE, McNew RW (1996) Cardiopulmonary function during acute unilateral occlusion of pulmonary artery in broilers fed diets containing normal or high levels of arginine-HCl. Poultry Science 75, 1587–1602.
Cardiopulmonary function during acute unilateral occlusion of pulmonary artery in broilers fed diets containing normal or high levels of arginine-HCl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsFWmsg%3D%3D&md5=2470d5d130fb8231b6c8b0216e68da12CAS | 9000287PubMed |

Wideman RF, Wing T, Kirby YK, Forman MF, Marson N, Tackett CD, Ruiz-Feria CA (1998) Evaluation of minimally invasive indices for predicting ascites susceptibility in three successive hatches of broilers exposed to cool temperatures. Poultry Science 77, 1565–1573.
Evaluation of minimally invasive indices for predicting ascites susceptibility in three successive hatches of broilers exposed to cool temperatures.Crossref | GoogleScholarGoogle Scholar | 9776067PubMed |

Wink DA, Osawa Y, Darbyshire JF, Jones CR, Eshenaur SC, Nims RW (1993) Inhibition of cytochromes P450 by nitric oxide and a nitric oxide-releasing agent. Archives of Biochemistry and Biophysics 300, 115–123.
Inhibition of cytochromes P450 by nitric oxide and a nitric oxide-releasing agent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsV2gtQ%3D%3D&md5=ac3a1b390c71507ad819dd499da95e2eCAS | 8424643PubMed |

Wirz T, Brändle U, Soldati T, Hossle JP, Perriard JC (1990) A unique chicken B-creatine kinase gene gives rise to two B-creatine kinase isoproteins with distinct N termini by alternative splicing. The Journal of Biological Chemistry 265, 11656–11666.

Xiang RP, Sun WD, Wang JY, Wang XL (2002) Effect of vitamin C on pulmonary hypertension and muscularisation of pulmonary arterioles in broilers. British Poultry Science 43, 705–712.
Effect of vitamin C on pulmonary hypertension and muscularisation of pulmonary arterioles in broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslKksw%3D%3D&md5=927edd8f1408ae4f8441493caee7b951CAS | 12555895PubMed |

Yersin AG, Huff WE, Kubena LF, Elissalde MA, Harvey RB, Witzel DA, Giroir LE (1992) Changes in hematological, blood gas, and serum biochemical variables in broilers during exposure to simulated high altitude. Avian Diseases 36, 189–197.
Changes in hematological, blood gas, and serum biochemical variables in broilers during exposure to simulated high altitude.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zivVOjug%3D%3D&md5=c6f464d62b926cc30853e150e72c463dCAS | 1627093PubMed |

Zantop DW (1997) Biochemistries. In ‘Avian medicine: principles and applications’. (Eds BW Ritchie, GJ Harrison, LR Harrison) pp. 115–129. (Wingers Publishing Institute: Lake Worth, FL)