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

Effect of dietary energy intake on erythrocytic antioxidant defence in growing lambs fed a wheat straw-based diet

Vijay Kumar Singh A C , Ashok Kumar Pattanaik A D E , Kusumakar Sharma A and Mohini Saini B
+ Author Affiliations
- Author Affiliations

A Centre of Advanced Studies in Animal Nutrition, Indian Veterinary Research Institute, Izatnagar 243 122, India.

B Division of Biochemistry, Indian Veterinary Research Institute, Izatnagar 243 122, India.

C Present address: College of Veterinary Science and Animal Husbandry, Narendra Dev University of Agriculture and Technology, Kumarganj, Faizabad 224 229, India.

D Present address: School of Veterinary and Animal Sciences, University of Adelaide, Roseworthy, SA 5371, Australia.

E Corresponding author. Email: akpattanaik1@gmail.com

Animal Production Science 51(7) 642-649 https://doi.org/10.1071/AN10098
Submitted: 17 June 2010  Accepted: 24 March 2011   Published: 27 June 2011

Abstract

Twenty-four Muzaffarnagari lambs (~8 months, 26.56 ± 2.04 kg), consisting 12 each of male and female, were used for ascertaining the effect of dietary energy restriction on the erythrocytic antioxidant defence including lipid peroxidation. The lambs, allotted randomly into three equal groups, were fed on wheat straw-based diets to provide 100, 80 and 70% of calculated metabolisable energy (ME) requirements. Bodyweight gain and feed intake were recorded. Blood samples were collected at the start and thereafter at 60-day intervals during 180 days of experimental duration and analysed for malonyl dialdehyde (MDA), reduced glutathione (GSH) and total thiol groups in addition to catalase, superoxide dismutase (SOD), glutathione peroxidase (GSH-Px) and glutathione S-transferase. Dietary treatments imparted significant (P < 0.001) effects on feed intake and average daily gain. The haemoglobin and haematocrit contents in blood reduced significantly (P < 0.001) on reduction in dietary energy levels. The dietary alterations elicited no change in the activities of SOD, catalase and glutathione S-transferase, but reduced activities of GSH-Px (P < 0.001) and GSH (P = 0.133) were evident on feeding the diet with 70% ME. Concentrations of total thiols decreased (P < 0.001) with reduced energy level. Both the energy-restricted groups exhibited a significant (P < 0.001) increase in MDA, indicative of increased lipid peroxidation. It was concluded that long-term energy malnutrition on a wheat straw-based diet reduces the erythrocytic antioxidant defence in growing lambs.

Additional keywords: glutathione, lipid peroxidation, oxidative stress, sheep.


References

Aurousseau B (2002) Les radicaux libres dans l’organisme des animaux d’e’levage: conse’quences sur la reproduction, la physiologie et la qualite’ de leurs produits. Productions Animales 15, 67–82.

Bergmeyer HU (1983) ‘Methods of enzymatic analysis. Vol. III.’ (Verlag Chemic: Weinheim, Germany)

Bruinsma J (2003) ‘World agriculture: towards 2015/2030, an FAO perspective.’ (Food and Agriculture Organization of the United Nations: Rome, Earthscan: London)

Catoni C, Peters A, Schaefer HM (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Animal Behaviour 76, 1107–1119.
Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants.Crossref | GoogleScholarGoogle Scholar |

Celi P, Robinson A (2010) Effects of Yerba Mate (Ilex paraguariensis) supplementation on the performance of dairy calves. Animal Production Science 50, 376–381.
Effects of Yerba Mate (Ilex paraguariensis) supplementation on the performance of dairy calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1yrs70%3D&md5=6ae6c05c4c7a429f3e8b7740632c6974CAS |

Celi P, Di Trana A, Claps S (2010) Effects of plane of nutrition on oxidative stress in goats during the peripartum period. Veterinary Journal 184, 95–99.
Effects of plane of nutrition on oxidative stress in goats during the peripartum period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisFOiurs%3D&md5=02440aaccfad4297c5b90d3960b961e1CAS |

Colitti M, Stefanon B (2006) Effect of natural antioxidants on superoxide dismutase and glutathione peroxide mRNA expression in leukocytes from periparturient dairy cows. Veterinary Research Communications 30, 19–27.
Effect of natural antioxidants on superoxide dismutase and glutathione peroxide mRNA expression in leukocytes from periparturient dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnnsFaktQ%3D%3D&md5=f484a1edcb7671ebbb7e212cd630dc80CAS | 16362607PubMed |

Di Trana A, Celi P, Claps S, Fedele V, Rubino R (2006) The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation. Animal Science 82, 717–722.
The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFOitA%3D%3D&md5=ffd879c44d26967cc98a72f9b504c3f6CAS |

Elsayed NM (2001) Antioxidant mobilization in response to oxidative stress: a dynamic environmental–nutritional interaction. Nutrition 17, 828–834.
Antioxidant mobilization in response to oxidative stress: a dynamic environmental–nutritional interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvFKjtb8%3D&md5=bf478807a6d617af2f629b019a18f7f3CAS | 11684389PubMed |

Gaal T, Karsal F, Mezes M, Ribiczey P, Brydl E (1990) Blood lipid peroxidative parameters in dairy cows with various liver lipid contents. In ‘Radicals, ions and tissue damage’. (Eds L Matkovics, H Karmazsin, B Kalasz) pp. 95–98. (Akademiai: Kiado, Budapest)

Gaal T, Mezes M, Miskucza O, Ribiczey-Szabo P (1993) Effect of fasting on blood lipid peroxidation parameters of sheep. Research in Veterinary Science 55, 104–107.
Effect of fasting on blood lipid peroxidation parameters of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhtlejs78%3D&md5=261ee116e46ab05c7aba1de720400677CAS | 8397431PubMed |

Gabai G, Testoni S, Piccinini R, Marinelli L, Stradaioli G (2004) Oxidative stress in primiparous cows in relation to dietary starch and the progress of lactation. Animal Science 79, 99–108.

Godin DV, Wohaieb SA (1988) Nutritional deficiency, starvation and tissue antioxidant status. Free Radical Biology & Medicine 5, 165–176.
Nutritional deficiency, starvation and tissue antioxidant status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXls12hsbs%3D&md5=69da7b5238194b80587d433713af6fdcCAS | 3075949PubMed |

Gumieniczek A, Hopkala H, Wojtowicz Z, Wysocka M (2002) Changes in antioxidant status of lung tissue in experimental diabetes in rabbits. Clinical Biochemistry 35, 147–149.
Changes in antioxidant status of lung tissue in experimental diabetes in rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xktlykurc%3D&md5=fa1d38bdee3b7df2f1eb37934a629128CAS | 11983351PubMed |

Habig WH, Michael JP, Jucoby WB (1974) Glutathione-S-transferase, the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 7130–7139.

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

Kearl LC (1982) ‘Nutrient requirements of ruminants in developing countries.’ (International Feedstuff Institute, Utah Agriculture Experiment Station, Utah State University: Logan, UT)

Liu SM, Eady SJ (2005) Glutathione: its implications for animal health, meat quality, and health benefits of consumers. Australian Journal of Agricultural Research 56, 775–780.
Glutathione: its implications for animal health, meat quality, and health benefits of consumers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovVOnt7w%3D&md5=ceccdb31c67c51a5fc615b002d9deeb2CAS |

Madesh M, Balasubramanian KA (1998) Micro titer plate assay for superoxide dismutase using MTT reduction by superoxide. Indian Journal of Biochemistry & Biophysics 35, 184–188.

Malmezat T, Breuille D, Capitan P, Patureau Mirand P, Obled C (2000) Glutathione turnover is increased during the acute phase of sepsis in rats. Journal of Nutrition 130, 1239–1246.

Mandal A, Prasad H, Ashok K, Roy R, Sharma N (2007) Factors associated with lamb mortalities in Muzaffarnagari sheep. Small Ruminant Research 71, 273–279.
Factors associated with lamb mortalities in Muzaffarnagari sheep.Crossref | GoogleScholarGoogle Scholar |

Öztabak K, Civelek S, Özpinar A, Burcak G, Esen F (2005) The effects of energy restricted diet on the activities of plasma Cu-Zn SOD, GSH-Px, CAT and TBARS concentrations in late pregnant ewes. Turkish Journal of Veterinary and Animal Sciences 29, 1067–1071.

Paglia DE, Valantine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory and Clinical Medicine 70, 158–169.

Pechova A, Dvorak R, Drastich P, Lubojacka V, Pavlata L, Poul J (2006) Influence of increased lipid content in diet in the form of treated rapeseed meal on the metabolism and milk yield of dairy cows in the first third of lactation. Veterinarni Medicina 51, 346–355.

Pedernera M, Celi P, García SC, Salvin HE, Barchia I, Fulkerson WJ (2010) Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Veterinary Journal 186, 352–357.
Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFWqtrbN&md5=1f8ef0a125c3d1bfcc97333943bd628fCAS |

Piccione G, Borruso M, Giannetto C, Morgante M, Giudice E (2007) Assessment of oxidative stress in dry and lactating cows. Acta Agriculturæ Scandinavica Section A. Animal Science 57, 101–104.

Placer ZA, Cushman LL, Johnson B (1966) Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Analytical Biochemistry 16, 359–364.
Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XksFymsLs%3D&md5=ee9e6e02273ff136e352a58855e31618CAS | 6007581PubMed |

Prins HK, Loos JA (1969) Glutathione. In ‘Biochemical methods in red cell genetics’. (Ed. JJ Yunis) pp. 127–129. (Academic Press: London)

Reed DJ (1990) Glutathione: toxicological implications. Annual Review of Pharmacology and Toxicology 30, 603–631.
Glutathione: toxicological implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFekt7o%3D&md5=09b4770898c53a6929de6f42268d41bdCAS | 2188580PubMed |

Rollo CD (2002) Growth negatively impacts the life span of mammals. Evolution and Development 4, 55–61.
Growth negatively impacts the life span of mammals.Crossref | GoogleScholarGoogle Scholar | 11868658PubMed |

Rulquin H, Vérité R, Guinard-Flament J, Pisulewski PM (2001) Acides amine’s digestibles dans l’intestin. Origines des variations chez les ruminants et re’ percussions sur les prote’ines du lait. Productions Animales 14, 201–210.

Sahoo A, Pattanaik AK, Goswami TK (2009) Immunobiochemical status of sheep exposed to periods of experimental protein deficit and realimentation. Journal of Animal Science 87, 2664–2673.
Immunobiochemical status of sheep exposed to periods of experimental protein deficit and realimentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptV2gtLw%3D&md5=ce158ada8fd2bd0f994b59e9033f2622CAS | 19395513PubMed |

Sansinanea A, Cerone S, Verkel G, Streitenberger S, Gracia M, Auza N (2000) Nutritional condition affects the hepatic antioxidant systems in steers. Veterinary Research Communications 24, 517–525.
Nutritional condition affects the hepatic antioxidant systems in steers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvgvFygsg%3D%3D&md5=4c909a2f699f10e0821944e822bdc3faCAS | 11305743PubMed |

Savary-Auzeloux I, Durand D, Gruffat D, Bauchart D, Ortigues-Marty I (2008) Food restriction and refeeding in lambs influence muscle antioxidant status. Animal 2, 738–745.
Food restriction and refeeding in lambs influence muscle antioxidant status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFertbw%3D&md5=054bfc0b3c0409656fb00997b5fb70e9CAS |

Schroeder GF, Titgemeyer EC (2008) Interaction between protein and energy supply on protein utilization in growing cattle: a review. Livestock Science 114, 1–10.
Interaction between protein and energy supply on protein utilization in growing cattle: a review.Crossref | GoogleScholarGoogle Scholar |

Sedliak J, Lindsay R (1968) Estimation of total protein bound and non protein sulphydryl groups in tissue with Ellman’s reagent. Analytical Biochemistry 25, 195–205.

Sgorlon S, Stradaioli G, Zanin D, Stefanon B (2006) Biochemical and molecular responses to antioxidant supplementation in sheep. Small Ruminant Research 64, 143–151.
Biochemical and molecular responses to antioxidant supplementation in sheep.Crossref | GoogleScholarGoogle Scholar |

Sgorlon S, Stradaioli G, Gabai G, Stefanon B (2008) Variation of starch and fat in the diet affects metabolic status and oxidative stress in ewes. Small Ruminant Research 74, 123–129.
Variation of starch and fat in the diet affects metabolic status and oxidative stress in ewes.Crossref | GoogleScholarGoogle Scholar |

Snedecor GW, Cochran WG (1989) ‘Statistical methods.’ 8th edn. (The Iowa State University Press: Ames, IA)

Utley HG, Bernheim F, Hochsein P (1967) Effect of sulfhydryl reagents on peroxidation of microsomes. Archives of Biochemistry and Biophysics 118, 29–32.
Effect of sulfhydryl reagents on peroxidation of microsomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXmt1SisQ%3D%3D&md5=29870266d83a2ee9bd9ef67ebc2c0ac5CAS |

Yagi Y, Furunchi S, Takashi H, Koyama H (1989) Abnormality of osmotic fragility and morphological disorder of bovine erythrocytes infected with Theileria sergonti. Japanese Journal of Veterinary Science 51, 389–395.

Zhang XD, Chen WJ, Li CY, Liu JX (2009) Effects of protein-free energy supplementation on blood metabolites, insulin and hepatic PEPCK gene expression in growing lambs offered rice straw-based diet. Czech Journal of Animal Science 54, 481–489.