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Muscle-specific metabolic, histochemical and biochemical responses to a nutritionally induced discontinuous growth path

Published online by Cambridge University Press:  18 August 2016

I. Cassar-Malek ,
J. F. Hocquette ,
C. Jurie ,
A. Listrat ,
R. Jailler ,
D. Bauchart ,
Y. Briand  and
B. Picard
I. Cassar-Malek*
Affiliation:
Equipe Croissance et Métabolismes du Muscle
J. F. Hocquette
Affiliation:
Equipe Croissance et Métabolismes du Muscle
C. Jurie
Affiliation:
Equipe Croissance et Métabolismes du Muscle
A. Listrat
Affiliation:
Equipe Croissance et Métabolismes du Muscle
R. Jailler
Affiliation:
Equipe Croissance et Métabolismes du Muscle
D. Bauchart
Affiliation:
Equipe Nutriments et Métabolismes, Unité de Recherches sur les Herbivores, INRA, Centre de Clermont-Ferrand/Theix, 63122 Saint-Genès-Champanelle, France
Y. Briand
Affiliation:
Université Blaise Pascal, Laboratoire de Biochimie Associé INRA, 63174 Aubière, France
B. Picard
Affiliation:
Equipe Croissance et Métabolismes du Muscle
*
† E-mail: [email protected]
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Abstract

An experiment was conducted with 42 Montbéliard steers to determine if nutritionally induced interrupted growth could influence muscle characteristics of steers and hence meat quality. A restriction/refeeding path was designed in order to induce a discontinuous growth path. At 9 months of age, 21 steers were given a restricted amount of diet for 3 months and were then slaughtered (R steers; no. = 10; intake: 5·28 kg dry matter (DM) per day) or subjected to a 4-month ad libitum refeeding period (R/F steers; no. = 11; intake: 8·99 kg DM per day) with the same diet (11·03 to 11·12 MJ metabolizable energy (ME) per kg DM) prior to slaughter. An additional 21 control steers were offered the same diet but in amounts that allowed them to gain continuously between 9 and 12 months of age, and were then slaughtered (C steers; no. = 10; intake: 7·08 kg DM per day) or maintained on a continuous feeding protocol through to 16 months of age prior to slaughter (C/C steers; no. = 11; intake: 8·07 kg DM per day). M. semitendinosus (ST), m. longisssimus thoracis and m. triceps brachii (TB) were collected for biochemical and histochemical analyses. R steers had a lower average daily gain (ADG; P 0·001), a lower final weight (P 0·01) and a leaner carcass (P 0·01) than C steers. Upon refeeding, R/F steers had a higher ADG than C/C steers (P 0·05) and underwent compensatory growth resulting in compensation of body weight and composition at 16 months. In muscles, glycolytic lactate dehydrogenase activity was lower in R steers (P 0·01) and restored in R/F steers compared with control steers. Among oxidative enzymes, cytochrome-c oxidase activity was higher in the TB of R/F compared with C/C steers (P 0·001) indicating a muscle-specific metabolic adaptation to the feeding level. There was little effect of the nutritional treatment on muscle fibre size and type except for an increase in the frequency of hybrid fibres in R and R/F groups (P 0·05). Total and insoluble collagen content were affected by restriction (P 0·001) in a muscle-specific manner: insoluble collagen content was lower in ST, but total and insoluble collagen contents were higher in TB of R compared with C animals at 12 months of age. No differences were recorded in lipid contents nor in proteasome activities. The data suggest that an alternation of relatively mild nutritional restriction and ad libitumfeeding had only a small effect on muscle characteristics. However, muscles respond differentially to changes in feeding level.

Keywords

collagencompensatory growthenergy metabolismmuscle fibressteers
Type
Growth, development and meat science
Information
Animal Science , Volume 79 , Issue 1 , August 2004 , pp. 49 - 59
Copyright
Copyright © British Society of Animal Science 2004

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References

Allingham, P. G., Harper, G. S., Hennessy, D. W. and Oddy, V. H. 2001. The influence of pre-weaning nutrition on biochemical and myofibre characteristics of bovine semitendinosus muscle. Australian Journal of Agricultural Research 52: 891–902.CrossRefGoogle Scholar
Allingham, P. G., Harper, G. S. and Hunter, R. A. 1998. Effect of growth path on the tenderness of the semitendinosus muscle of Braham-cross steers. Meat Science 48: 65–73.Google Scholar
Barlett, G. R. 1959. Phosphorus assay in column chromatography. Journal of Biological Chemistry 234: 466–469.CrossRefGoogle Scholar
Bauchart, D., Ortigues, I., Hocquette, J. F., Gruffat, D. and Durand, D. 1996. Energy and fat metabolism of the liver, the digestive tract and muscles: transport, processing, energy consumption, fixation by tissues. In Veal. Perspectives to the year 2000. Proceedings of the international symposium, pp. 255–290. Presse de Jouve, Le Mans.Google Scholar
Blum, J. W., Schnyder, W., Kunz, P. L., Blom, A. K., Bickel, H. and Schurch, D. 1985. Reduced and compensatory growth: endocrine and metabolic changes during food restriction and refeeding in steers. Journal of Nutrition 115: 417–424.Google Scholar
Boleman, S. J., Miller, R. K., Buyck, M. J., Cross, H. R. and Savell, J. W. 1996. Influence of realimentation of mature cows on maturity, color, collagen solubility, and sensory characteristics. Journal of Animal Science 74: 2187–2194.Google Scholar
Brandstetter, A. M., Picard, B. and Geay, Y. 1998a. Muscle fibre characteristics in four muscles of growing male cattle.I.Postnatal differentiation. Livestock Production Science 53: 15–23.CrossRefGoogle Scholar
Brandstetter, A. M., Picard, B. and Geay, Y. 1998b. Muscle fibre characteristics in four muscles of growing male cattle.II.Effect of castration and feeding level. Livestock Production Science 53: 25–26.CrossRefGoogle Scholar
Bruce, H. L., Ball, R. O. and Mowat, D. N. 1991. Effects of compensatory growth on protein metabolism and meat tenderness of beef steers. Canadian Journal of Animal Science 71: 659–668.Google Scholar
Cassar-Malek, I., Kahl, S., Jurie, C. and Picard, B. 2001. Influence of feeding level during postweaning growth on circulating concentrations of thyroid hormones and extrathyroidal 5’-deiodination in steers. Journal of Animal Science 79: 2679–2687.Google Scholar
Chilliard, Y., Doreau, M., Bocquier, F. and Lobley, G. E. 1995. Digestive and metabolic adaptions of ruminants to variations in food supply. In Recent developments in the nutrition of herbivores: IVth international symposium on nutrition of herbivores (ed.Journet, M. Grenet, E. Farce, M. -H. Theriez, M. and Demarquilly, C.), pp. 329–360. INRA, Paris.Google Scholar
Eenaeme, C. van, Clinquart, A., Uytterhaegen, L., Hornick, J. L., Demeyer, D. and Istasse, L. 1994. Postmortem protease activity in relation to protein turnover in Belgian Blue bulls with different growth rates. Sciences des Aliments 14: 475–483.Google Scholar
Etherington, D. J. 1987. Collagen and meat quality: effects of conditioning and growth rate. In Advance in meat research, vol. 4 (ed. Pearson, A. M. Dutson, T. R. and Bayley, A. J.), pp. 351–360. Van Nostrand Reinhold Co., New York.Google Scholar
Farout, L., Lamare, M., Cardozo, C., Harrisson, M., Briand, Y. and Briand, M. 2000. Distribution of proteasome and of the five proteolytic activities in rat tissues. Archives of Biochemistry and Biophysics 374: 207–212.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. and Slone-Stanley, H. S. 1957. A simple method for the isolation and purification of lipids from animal tissues. Journal of Biological Chemistry 226: 497–509.CrossRefGoogle ScholarPubMed
Geay, Y., Bauchart, D., Hocquette, J. F. and Culioli, J. 2001. Effect of nutritional factors on biochemical, structural and metabolic characteristics of muscles in ruminants; consequences on dietetic value and sensorial qualities of meat. Reproduction, Nutrition, Development 41: 1–26. Erratum, 41: 377.CrossRefGoogle ScholarPubMed
Geay, Y., Picard, B. and Renand, G. 1997. Variability in muscle fibre types during muscle development; effect of some hormones, muscle type and genotype. Proceedings of the 48th annual meeting of the European Association for Animal Production, 25th-28th August, Vienna. Satellite symposium I: beef production with special respect to beef quality.Google Scholar
Harper, G. S., Allingham, P. G. and LeFeuvre, R. P. 1999. Changes in connective tissue of M . semitendinosus as a response to different growth paths in steers. Meat Science 53: 107–114.Google Scholar
Hayden, J. M., Williams, J. E. and Collier, R. J. 1993. Plasma growth hormone, insulin-like growth factor, insulin, and thyroid hormone association with body protein and fat accretion in steers undergoing compensatory gain after dietary energy restriction. Journal of Animal Science 71: 3327–3338.Google Scholar
Henriksson, J. 1990. The possible role of skeletal muscle in the adaptation to periods of energy deficiency. European Journal of Clinical Nutrition 44: 55–64.Google ScholarPubMed
Hocquette, J. F., Ortigues-Marty, I., Pethick, D. W., Herpin, P. and Fernandez, X. 1998. Nutritional and hormonal regulation of energy metabolism in skeletal muscles of meat-producing animals. Livestock Production Science 56: 115–143.CrossRefGoogle Scholar
Hogg, B. W. 1991. Compensatory growth in ruminants. In Advances in meat research. Growth regulation in farm animals (ed. Pearson, A. M. and Dutson, T. R.), pp. 103–134. Elsevier Applied Science, London.Google Scholar
Institut National de la Recherche Agronomique. 1988. Alimentation des bovins, ovins et caprins. INRA Publications, Versailles, France.Google Scholar
Jones, S. J., Starkey, D. L., Calkins, C. R. and Crouse, J. D. 1990. Myofibrillar protein turnover in feed-restricted and realimented beef cattle. Journal of Animal Science 68: 2707–2715.Google Scholar
Jurie, C., Robelin, J., Picard, B., Renand, G. and Geay, Y. 1995. Inter-animal variation in the biological characteristics of muscle tissue in male Limousin cattle. Meat Science 39: 415–425.Google Scholar
Koohmaraie, M., Babiker, A. S., Schroeder, A. L., Merkel, R. A. and Dutson, T. R. 1988. Acceleration of postmortem tenderization in ovine carcasses through activation of Ca2 + -dependent proteases. Journal of Food Science 53: 1638–1641.Google Scholar
Koohmaraie, M., Kent, M. P., Shackelford, D. D., Veiseth, E. and Wheeler, T. L. 2002. Meat tenderness and muscle growth: is there any relationship? Meat Science 62: 345–352.Google Scholar
Lamare, M., Taylor, R. G., Farout, L., Briand, Y. and Briand, M. 2002. Changes in proteasome activity during postmortem aging of bovine muscle. Meat Science 61: 199–203.Google Scholar
Leplaix-Charlat, L., Durand, D. and Bauchart, D. 1996. Effects of tallow- and soybean oil-containing diets with and without cholesterol on hepatic metabolism of lipids and lipoproteins in the preruminant calf. Journal of Dairy Science 79: 1826–1835.Google Scholar
Listrat, A., Rakadjiyski, N., Jurie, C., Picard, B., Touraille, C. and Geay, Y. 1999. Effect of the diet on muscle characteristics and meat palatability of growing Salers bulls. Meat Science 53: 115–124.Google Scholar
McCormick, R. J. 1989. The influence of nutrition on collagen metabolism and stability. Reciprocal Meat Conference Proceedings 42: 137–148.Google Scholar
McCormick, R. J. 1994. The flexibility of the collagen compartment of muscle. Meat Science 36: 79–91.Google Scholar
McVeigh, J. and Tarrant, P. V. 1982. Glycogen content and repletion rates in beef muscle. Effects of feeding and fasting. Journal of Nutrition 112: 1306–1314.Google Scholar
Maltin, C. A., Lobley, G. E., Grant, C. M., Miller, L. A., Kyle, D. J., Horgan, G. W., Matthews, K. R. and Sinclair, K. D. 2001. Factors influencing beef eating quality. 2. Effects of nutritional regimen and genotype on muscle fibre characteristics. Animal Science 72: 279–287.Google Scholar
Morgan, J. B., Wheeler, T. L., Koohmaraie, M., Savell, J. W. and Crouse, J. D. 1993. Meat tenderness and the calpain proteolytic system in longissimus muscle of young bulls and steers. Journal of Animal Science 71: 1471–1476.Google Scholar
Muir, P. D., Smith, N. B., Dobbie, P. M., Smith, D. R. and Bown, M. D. 2001. Effects of growth pathway on beef quality in 18-month-old Angus and South Devon ✕ Angus pasture-fed steers. Animal Science 72: 297–308.Google Scholar
Oddy, V. H., Harper, G. S., Greenwood, P. L. and McDonagh, M. B. 2001. Nutritional and developmental effects on the intrinsic properties of muscles as they relate to the eating quality of beef. Australian Journal of Experimental Agriculture 41: 921–942.Google Scholar
Ortigues-Marty, I., Hocquette, J.-F., Bertrand, G., Martineau, C., Vermorel, M. and Toullec, R. 2003. The incorporation of solubilized wheat proteins in milk replacers for veal calves: effects on growth performance and muscle oxidative capacity. Reproduction, Nutrition, Development 43: 57–76.Google Scholar
Pethick, D. W. and Dunshea, F. R. 1997. The partitioning of fat in farm animals. Proceedings of Nutrition Society of Australia 20: 3–13.Google Scholar
Picard, B., Gagnière, H., Robelin, J. and Geay, Y. 1995. Comparison of the foetal development of muscle in normal and double-muscled cattle. Journal of Muscle Research and Cell Motility 16: 629–639.Google Scholar
Piot, C., Veerkamp, J. H., Bauchart, D. and Hocquette, J.-F. 1998. Contribution of mitochondria and peroxisomes to palmitate oxidation in rat and bovine tissues. Comparative Biochemistry and Physiology. Part B: Biochemistry and Molecular Biology. 121: 185–194.Google Scholar
Purchas, R. W., Burnham, D. L. and Morris, S. T. 2002. Effects of growth potential and growth path on tenderness of beef longissimus muscle from bull and steers. Journal of Animal Science 80: 3211–3221.Google Scholar
Robelin, J. and Geay, Y. 1975. Estimation de la composition des carcasses de jeunes bovins à partir de la composition d’un morceau monocostal prélevé au niveau de la 11ème côte. I. composition anatomique de la carcasse. Annales de Zootechnie 24: 391–402.Google Scholar
Rompala, R. E. and Jones, S.D. M. 1984. Changes in the solubility of bovine intramuscular collagen due to nutritional regime. Growth 48: 466–472.Google Scholar
Smith, S. B., Prior, R. L., Koong, L. J. and Mersmann, H. J. 1992. Nitrogen and lipid metabolism in heifers fed at increasing level of intakes. Journal of Animal Science 70: 152–160.Google Scholar
Soukup, T. and Jirmanova, I. 2000. Regulation of myosin expression in developing and regenerating extrafusal and intrafusal muscle fibers with special emphasis on the role of thyroid hormones. Physiological Research 49: 617–633.Google Scholar
Statistical Analysis Systems Institute. 1996. SAS/STAT guide for personal computers. SAS Institute Inc., Cary, NC.Google Scholar
Taylor, R. G., Geesink, G. H., Thompson, V. F., Koohmaraie, M. and Goll, D. E. 1995. Is Z-disk degradation responsible for postmortem tenderization? Journal of Animal Science 73: 1351–1367.CrossRefGoogle ScholarPubMed
Therkildsen, M., Melchior Larsen, L., Bang, H. G. and Vestergaard, M. 2002a. Effect of growth rate on tenderness development and final tenderness of meat from Friesian calves. Animal Science 74: 253–264.CrossRefGoogle Scholar
Therkildsen, M., Melchior Larsen, L. and Vestergaard, M. 2002b. Influence of growth rate and muscle type on muscle fibre type characteristics, protein synthesis capacity and activity of the calpain system in Friesian calves. Animal Science 74: 243–251.CrossRefGoogle Scholar
Torrescano, G., Sánchez-Escalante, A., Giménez, B., Roncalés, P. and Beltrán, J. A. 2003. Shear values of raw samples of 14 bovine muscles and their relation to muscle collagen characteristics. Meat Science 64: 84–91.Google Scholar
Vestergaard, M., Oksbjerg, N. and Henckel, P. 2000. Influence of feeding intensity, grazing and finishing feeding on muscle fibre characteristics and meat colour of semitendinosus, longissimus dorsi and supraspinatus muscles of young bulls. Meat Science 54: 177–185.CrossRefGoogle ScholarPubMed
Xie, Y. R., Bubsboom, J. R., Cornforth, D. P., Shenton, H. T., Gaskin, C. T., Johnson, K. A., Reeves, J. J., Wright, R. W. and Conrath, J. D. 1996. Effects of time on feed and post-mortem aging on palatability and lipid composition of crossbred Wagyu beef. Meat Science 43: 157–166.CrossRefGoogle ScholarPubMed
Yambayamba, E. S. K. and Price, M. A. 1991. Fiber type proportions and diameters in the longissimus muscle of beef heifers undergoing catch-up (compensatory) growth. Canadian Journal of Animal Science 71: 1013–1035.Google Scholar