Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T07:40:54.310Z Has data issue: false hasContentIssue false
  • English
  • Français

Food restriction and refeeding in lambs influence muscle antioxidant status

Published online by Cambridge University Press:  15 April 2008

I. Savary-Auzeloux ,
D. Durand ,
D. Gruffat ,
D. Bauchart  and
I. Ortigues-Marty
I. Savary-Auzeloux*
Affiliation:
Unité de Recherche sur les Herbivores, INRA Clermont Ferrand Theix, 63122 St Genès Champanelle, France
D. Durand
Affiliation:
Unité de Recherche sur les Herbivores, INRA Clermont Ferrand Theix, 63122 St Genès Champanelle, France
D. Gruffat
Affiliation:
Unité de Recherche sur les Herbivores, INRA Clermont Ferrand Theix, 63122 St Genès Champanelle, France
D. Bauchart
Affiliation:
Unité de Recherche sur les Herbivores, INRA Clermont Ferrand Theix, 63122 St Genès Champanelle, France
I. Ortigues-Marty
Affiliation:
Unité de Recherche sur les Herbivores, INRA Clermont Ferrand Theix, 63122 St Genès Champanelle, France
*
E-mail: [email protected]
Get access

Abstract

Compensatory growth, a frequent phenomenon observed in ruminants due to seasonal variation in food availability, affects protein metabolism including protein oxidation. These oxidation processes may have an impact on animal health as well as on meat protein degradation during post mortem aging (ie meat maturation). Sixteen male lambs were randomly divided into four groups. One group was fed ad libitum (C) and one group was food-restricted to 60% of the intake of the C group (R). The last two groups were restricted similarly to the R group and refed either ad libitum (RAL) or similarly to the C group (pair-feeding) (RPF). Muscles samples were taken immediately after slaughter. The present study showed that the restriction/refeeding pattern had no effect on protein oxidation in the muscles studied (longissimus dorsi (LD), semitendinosus (ST) and supraspinatus (SP)). However, total antioxidant capacity decreased after food restriction (−51%, −43%, P < 0.01 for ST and LD muscles, respectively) and re-increased only after ad libitum refeeding. This alteration in the total antioxidant status can partially be explained by the similar pattern of change observed in the glutathione concentration of the muscles (−25%, P < 0.05 for ST muscle and NS for the other muscles). However, none of the concentrations of other water-soluble antioxidants studied (carnosine, anserine, glutathione peroxidase and superoxide dismutase) were altered during compensatory growth. This study showed that an inappropriate feeding level following a nutritional stress induced alterations in the total antioxidant status (particularly that of glutathione), which may have consequences on animal health. Other consequences of a decrease of the animal antioxidant status in vivo could be an alteration of the protein oxidation processes during meat maturation.

Keywords

antioxidant statuscompensatory growthmusclesheep
Type
Full Paper
Information
animal , Volume 2 , Issue 5 , May 2008 , pp. 738 - 745
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agergaard, N, Thode Jensen, P 1982. Procedure for blood glutathione peroxidase determination in cattle and swine. Acta Veterinarian Scandinavian 23, 515–527.CrossRefGoogle ScholarPubMed
Alia, M, Horcajo, C, Bravo, L, Goya, L 2003. Effect of grape antioxidant dietary fiber on the total antioxidant capacity and the activity of liver antioxidant enzymes in rats. Nutrition Research Reviews 23, 1251–1567.CrossRefGoogle Scholar
Aristoy, MC, Toldra, F 1998. Concentration of free amino acids and dipeptides in porcine skeletal muscles with different oxidative patterns. Meat Science 50, 327–332.CrossRefGoogle ScholarPubMed
Aurousseau, B 2002. Les radicaux libres dans l’organisme des animaux d’élevage: conséquences sur la reproduction, la physiologie et la qualité de leurs produits. INRA Productions Animales 15, 67–82.CrossRefGoogle Scholar
Briand, M, Talmant, A, Briand, Y, Monin, G, Durand, R 1981a. Metabolic types of muscle in sheep: I. Myosin ATPase, glycolytic, and mitochondrial enzyme activities. European Journal of Applied Physiology 46, 347–358.CrossRefGoogle ScholarPubMed
Briand, M, Talmant, A, Birnad, Y, Monin, G, Durand, R 1981b. Metabolic types of muscle in sheep: II. Lactate dehydrogenase activity and LDH isoenzyme distribution. European Journal of Applied Physiology 46, 359–365.CrossRefGoogle ScholarPubMed
Bruce, HL, Ball, RO, Mowat, DN 1991. Effects of compensatory growth on protein metabolism and meat tenderness of beef steers. Canadian Journal of Animal Science 71, 659–668.CrossRefGoogle Scholar
Chan, KM, Decker, EA 1994. Endogenous skeletal muscle antioxidants. Critical Reviews in Food Science and Nutrition 4, 403–426.CrossRefGoogle Scholar
Cho, ES, Sahyoun, N, Stegink, LD 1981. Tissue glutathione as a cyst(e)ine reservoir during fasting and refeeding of rats. Journal of Nutrition 111, 914–922.CrossRefGoogle ScholarPubMed
Cornet, M, Bousset, J 1999. Free amino acids and dipeptides in porcine muscles: differences between “red” and “white” muscles. Meat Science 51, 215–219.CrossRefGoogle ScholarPubMed
Dandona, P, Mohanty, P, Ghanim, H, Aljada, A, Browne, R, Hamouda, W, Prabhala, A, Afzal, A, Garg, R 2001. The suppressive effect of dietary restriction and weight loss in the obese on the generation of reactive oxygen species by leukocytes, lipid peroxidation, and protein carbonylation. Journal of Clinical Endocrinology and Metabolism 86, 355–362.Google ScholarPubMed
Dröge, W 2002. Free radicals in the physiological control of cell function. Physiological Reviews 82, 47–95.CrossRefGoogle ScholarPubMed
Durand, D, Scislowski, V, Gruffat, D, Chilliard, Y, Bauchart, D 2005. High-fat rations and lipid peroxidation in ruminants: consequences on the health of animals and quality of their products. In Indicators of milk and beef quality, vol 112 (ed. JF Mhocquette and S Gigli), pp. 137–150. EAAP Publications, Wageningen Academic Publishers, Wageningen.CrossRefGoogle Scholar
Fang, YZ, Yang, S, Wu, G 2002. Free radicals, antioxidants, and nutrition. Nutrition 18, 872–879.CrossRefGoogle ScholarPubMed
Fano, G, Mecocci, P, Vecchiet, J, Belia, S, Fulle, S, Polidori, MC, Felzani, G, Senin, U, Vecchiet, L, Beal, MF 2001. Age and sex influence on oxidative damage and functional status in human skeletal muscle. Journal of Muscle Research and Cell Motility 22, 345–351.CrossRefGoogle ScholarPubMed
Girard, A, Madani, S, El Boustani, ES, Belleville, J, Prost, J 2005. Changes in lipid metabolism and antioxidant defense status in spontaneously hypertensive rats and Wistar rats fed a diet enriched with fructose and saturated fatty acids. Nutrition 21, 240–248.CrossRefGoogle ScholarPubMed
Gladine, C, Morand, C, Rock, E, Gruffat, D, Bauchart, D, Durand, D 2007. The antioxidative effect of plant extracts rich in polyphenols differs between liver and muscle tissues in rats fed n-3 PUFA rich diets. Animal Feed Science and Technology 139, 257–272.CrossRefGoogle Scholar
Griffiths, HR 2002. The influence of diet on protein oxidation. Nutrition Research Reviews 15, 3–17.CrossRefGoogle ScholarPubMed
Himmelfarb, J, McMonagle, E, McMenamin, E 2000. Plasma protein thiols oxidation and carbonyl formation in chronic renal failure. Kidney International 58, 2571–2578.CrossRefGoogle ScholarPubMed
Hipkiss, AR, Preston, JE, Himsworth, DT, Worthington, VC, Keown, M, Michaelis, J, Lawrence, J, Mateen, A, Allende, L, Eagles, PA, Abbott, NJ 1998. Pluripotent protective effects of carnosine, a naturally occurring dipeptide. Annals of the New York Academy of Sciences 854, 37–53.CrossRefGoogle ScholarPubMed
Hipkiss, AR, Brownson, C, Carrier, MJ 2001. Carnosine, the anti-ageing, anti-oxidant dipeptide, may react with protein carbonyl group. Mechanisms of Ageing and Development 122, 1431–1445.CrossRefGoogle Scholar
Hoch, T, Begon, C, Cassar-Malek, I, Picard, B, Savary-Auzeloux, I 2003. Mécanismes et conséquences de la croissance compensatrice chez les ruminants. INRA Productions Animales 16, 49–59.CrossRefGoogle Scholar
Hornick, JL, Van Eenaeme, C, Gérard, O, Dufrasne, I, Istasse, L 2000. Mechanisms of reduced and compensatory growth. Domestic Animal Endocrinology 19, 121–132.CrossRefGoogle ScholarPubMed
Leeuwenburgh, C, Heinecke, JW 2001. Oxidative stress and antioxidants in exercise. Current Medicinal Chemistry 8, 829–838.CrossRefGoogle ScholarPubMed
Levine, RL, Williams, JA, Stadtman, ER, Shacter, E 1994. Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology 233, 346–357.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Liu, Q, Lanari, MC, Schaefer, DM 1995. A review of dietary vitamin E supplementation for improvement of beef quality. Journal of Animal Science 73, 3131–3140.CrossRefGoogle ScholarPubMed
Lobley, G 2003. Protein turnover, what does that mean for animal production? Canadian Journal of Animal Science 83, 327–340.CrossRefGoogle Scholar
Malmezat, T, Breuillé, D, Pouyet, C, Patureau Mirand, P, Obled, C 1998. Metabolism of cysteine is modified during the acute phase sepsis in rats. Journal of Nutrition 128, 97–105.CrossRefGoogle ScholarPubMed
Malmezat, T, Breuillé, 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.CrossRefGoogle ScholarPubMed
Maltin, C, Balcerzak, D, Tilley, R, Delday, M 2003. Determinants of meat quality: tenderness. Proceedings of the Nutrition Society 62, 337–347.CrossRefGoogle ScholarPubMed
Marklund, SL, Marklund, G 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry 47, 469–474.CrossRefGoogle Scholar
Martinaud, A, Mercier, Y, Marinova, P, Tassy, C, Gatellier, P, Renerre, M 1997. Comparison of oxidative processes on myofibrillar proteins from beef during maturation and by different model oxidation systems. Journal of Agriculture and Food Chemistry 45, 2481–2487.CrossRefGoogle Scholar
Masella, R, Di Benedetto, R, Vari, R, Filesi, C, Giovannini, C 2005. Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. Journal of Nutritional Biochemistry 16, 577–586.CrossRefGoogle ScholarPubMed
Maynard, LM, Boissonneault, GA, Chow, CK, Bruckner, GG 2001. High levels of dietary carnosine are associated with increased concentrations of carnosine and histidine in rat soleus muscle. Journal of Nutrition 131, 287–290.CrossRefGoogle ScholarPubMed
Mei, L, Cromwell, GL, Crum, AD, Decker, EA 1998. Influence of dietary β-alanine and histidine on the oxidative stability in pork. Meat Science 49, 55–64.CrossRefGoogle ScholarPubMed
Mercier, Y, Gatellier, P, Viau, M, Remignon, H, Renerre, M 1998. Effect of dietary fat and vitamin E on colour stability and on lipid and protein oxidation in turkey meat during storage. Meat Science 48, 301–318.CrossRefGoogle ScholarPubMed
Mercier, Y, Gatellier, P, Renerre, M 2004. Lipid and protein oxidation in vitro, and antioxidant potential in meat from Charolais cows finished on pasture or mixed diet. Meat Science 66, 467–473.CrossRefGoogle ScholarPubMed
Miller, NJ, Rice-Evans, C, Davies, MJ, Gopinathan, V, Milner, A 1993. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clinical Science (London) 84, 407–412.CrossRefGoogle ScholarPubMed
Moya, VJ, Flores, M, Aristoy, MC, Toldra, F 2001. Pork meat quality affects peptide and amino acid profiles during the ageing process. Meat Science 58, 197–206.CrossRefGoogle ScholarPubMed
Nagai, M, Takahashi, R, Goto, S 2000. Dietary restriction initiated late in life can reduce mitochondrial protein carbonyls in rat livers: western blot studies. Biogerontology 1, 321–328.CrossRefGoogle ScholarPubMed
Pamplona, R, Portero-Otin, M, Requena, J, Gredilla, R, Barja, G 2002. Oxidative, glycoxidative and lipoxidative damage to rat heart mitochondrial proteins is lower after 4 months of caloric restriction than in age-matched controls. Mechanisms of Ageing and Development 123, 1437–1446.CrossRefGoogle ScholarPubMed
Park, YJ, Volpe, SL, Decker, EA 2005. Quantification of carnosine in human plasma after dietary consumption of beef. Journal of Agriculture and Food Chemistry 53, 4736–4739.CrossRefGoogle Scholar
Pennathur, S, Ido, Y, Heller, JI, Byun, J, Danda, R, Pergola, P, Williamson, JR, Heinecke, JW 2005. Reactive carbonyls and polyunsaturated fatty acids produce hydroxyl radical-like species. Journal of Biological Chemistry 280, 22706–22714.CrossRefGoogle ScholarPubMed
Petzke, KJ, Elsner, A, Proll, J, Thielecke, F, Metges, CC 2000. Long-term high protein intake does not increase oxidative stress in rats. Journal of Nutrition 130, 2889–2896.CrossRefGoogle Scholar
Potter, DW, Tran, TB 1993. Apparent rates of glutathione turnover in rat tissues. Toxicology and Applied Pharmacology 120, 186–192.CrossRefGoogle ScholarPubMed
Reznick, AZ, Packer, L 1994. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in Enzymology 233, 357–363.CrossRefGoogle ScholarPubMed
Rowe, LJ, Maddocks, KR, Lonergan, SM, Huff-Lonergan, E 2004a. Influence of early post-mortem protein oxidation on beef quality. Journal of Animal Science 82, 785–793.CrossRefGoogle Scholar
Rowe, LJ, Maddocks, KR, Lonergan, SM, Huff-Lonergan, E 2004b. Oxidative environments decrease tenderization of beef steaks through inactivation of μcalpain. Journal of Animal Science 82, 3254–3266.CrossRefGoogle ScholarPubMed
Rulquin, H, Vérité, R, Guinard-Flament, J, Pisulewski, PM 2001. Acides aminés digestibles dans l’intestin. Origines des variations chez les ruminants et répercussions sur les protéines du lait. INRA Productions Animales 14, 201–210.CrossRefGoogle Scholar
Savary-Auzeloux I, Micol D, Dozias D and Ortigues-Marty I 2001. Oxydation des protéines hépatiques et musculaires chez le bouvillon engraissé par un régime à base d’herbe. 8èmes Rencontres Recherches Ruminants, p. 107.Google Scholar
Sewell, DA, Harris, RC, Marlin, DJ, Dunnett, M 1992. Estimation of the carnosine content of different fibre types in the middle gluteal muscle of the thoroughbred horse. Journal of Physiology 455, 447–453.CrossRefGoogle ScholarPubMed
Stadtman, ER, Levine, RL 2000. Protein oxidation. Annals of the New York Academy of Sciences 899, 191–208.CrossRefGoogle ScholarPubMed
Tamaki, N, Tsunemori, F, Wakabayashi, M, Hama, T 1977. Effect of histidine-free and -excess diets on anserine and carnosine contents in rat gastrocnemius muscle. Journal of Nutritional Science and Vitaminology 23, 331–340.CrossRefGoogle ScholarPubMed
Tietze, F 1969. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Analytical Biochemistry 27, 502–522.CrossRefGoogle Scholar
Van Eenaeme, C, Evrard, M, Hornick, JL, Baldwin, P, Diez, M, Istasse, L 1998. Nitrogen balance and myofibrillar protein turnover in double muscled Belgian Blue bulls in relation to compensatory growth after different periods of restricted feeding. Canadian Journal of Animal Science 78, 549–559.CrossRefGoogle Scholar
Van Eijk, HM, Rooyakkers, DR, Deutz, NE 1993. Rapid routine determination of amino acids in plasma by high performance liquid chromatography with a 2-3 microns spherisorb ODS II column. Journal of Chromatography 620, 143–148.CrossRefGoogle ScholarPubMed
Wander, RC, Du, SH 2000. Oxidation of plasma proteins is not increased after supplementation with eicosapentaenoic and docosahexanoic acids. The American Journal of Clinical Nutrition 72, 731–737.CrossRefGoogle ScholarPubMed
Warner, RD, Dunshea, FR, Ponnampalam, EN, Cottrell, JJ 2005. Effects of nitric oxide and oxidation in vivo and post-mortem on meat tenderness. Meat Science 71, 205–217.CrossRefGoogle Scholar
Wood, JD, Enser, M 1997. Factors influencing fatty acids in meat and the role of antioxidants in improving meat quality. British Journal of Nutrition 78, S49–S60.CrossRefGoogle ScholarPubMed
Wood, JD, Richardson, RI, Nute, GR, Fisher, AV, Campo, MM, Kasapidou, E, Sheard, PR, Enser, M 2003. Effects of fatty acids on meat quality: a review. Meat Science 66, 21–32.CrossRefGoogle Scholar