European Journal of Applied Physiology

, Volume 94, Issue 5–6, pp 558–568 | Cite as

Inverse relationship between exercise economy and oxidative capacity in muscle

  • Gary R. Hunter
  • Marcas M. Bamman
  • D. Enette Larson-Meyer
  • Denis R. Joanisse
  • John P. McCarthy
  • Tamilane E. Blaudeau
  • Bradley R. Newcomer
Original Article

Abstract

An inverse relationship has been shown between running and cycling exercise economy and maximum oxygen uptake \(\left(\dot{V}\hbox{O}_{2{\rm max}}\right).\) The purposes were: 1) determine the relationship between walking economy and \(\dot{V}\hbox{O}_{2{\rm max}};\) and 2) determine the relationship between muscle metabolic economy and muscle oxidative capacity and fiber type. Subjects were 77 premenopausal normal weight women. Walking economy \(\left(1/\dot{V}\hbox{O}_{2}\right)\) was measured at 3 mph and \(\dot{V}\hbox{O}_{2{\rm max}}\) during graded treadmill test. Muscle oxidative phosphorylation rate (OxPhos), and muscle metabolic economy (force/ATP) were measured in calf muscle using 31P MRS during isometric plantar flexion at 70 and 100% of maximum force, (HI) and (MI) respectively. Muscle fiber type and citrate synthase activity were determined in the lateral gastrocnemius. Significant inverse relationships (r from −0.28 to −0.74) were observed between oxidative metabolism measures and exercise economy (walking and muscle). Type IIa fiber distribution was inversely related to all measures of exercise economy (r from −0.51 to −0.64) and citrate synthase activity was inversely related to muscle metabolic economy at MI (r=−0.56). In addition, Type IIa fiber distribution and citrate synthase activity were positively related to \(\dot{V}\hbox{O}_{2{\rm max}}\) and muscle OxPhos at HI and MI (r from 0.49 to 0.70). Type I fiber distribution was not related to any measure of exercise economy or oxidative capacity. Our results support the concept that exercise economy and oxidative capacity are inversely related. We have demonstrated this inverse relationship in women both by indirect calorimetry during walking and in muscle tissue by 31P MRS.

Keywords

Muscle metabolism Maximum oxygen uptake Efficiency Muscle fiber types 

Notes

Acknowledgements

We thank Roland Weinsier, Harry Vaughn, Betty Darnell, Paul Zuckerman, David Fields, Robert Petri, and Nancy Davis for their invaluable assistance. Research was supported by NIH grants R01 DK 49779 and R01 DK 51684, DRR General Clinical Research Center grant RR-32, and Clinical Nutrition Research Unit grant P30-DK 56336. Stouffer’s Lean Cuisine entrees, Nestle Food Co, Solon, OH and Weight Watchers Smart Ones HJ Heinz Frozen Foods, Pittsburgh, PA kindly provided food for dietary control.

References

  1. Allor KM, Pivarnik JM, Sam LJ, Perkins CD (2000) Treadmill economy in girls and women matched for height and weight. J Appl Physiol 89:512–516PubMedGoogle Scholar
  2. Argov Z, De Stefano N, Arnold DL (1996) ADP recovery after a brief ischemic exercise in normal and diseased human muscle-a 31P MRS study. NMR Biomedicine 9:165–172CrossRefGoogle Scholar
  3. Bassett Jr DR, Howley ET (1997) Maximal oxygen uptake: “classical” versus “contemporary” viewpoints. Med Sci Sports Exerc 29:591–603PubMedGoogle Scholar
  4. Boska M (1991) Estimating the ATP cost of force production in the human gastrocnemius/soleus muscle group using P MRS and H MRI. NMR Biomed 4:173–181PubMedGoogle Scholar
  5. Boska M (1994) ATP production rates as a function of force level in the human gastrocnemius/soleus using P MRS. Magn Res Med 32:1–10Google Scholar
  6. Bouten CV, Westerterp KR, Verduin M, Janssen JD (1994) Assessment of energy expenditure for physical activity using a triaxial accelerometer. Med Sci Sports Exerc 26:1516–1523PubMedGoogle Scholar
  7. Conley Dl, Krahenbuhl GS (1980) Running economy and distance running performance of highly trained athletes. Med Sci Sports Exerc 12:357–360PubMedGoogle Scholar
  8. Coyle EF, Sidossis LS, Horowitz JF, Beltz JD (1992) Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sports Exerc 24:782–788Google Scholar
  9. Crouter SE, Schneider PL, Karabulut M, Bassett DR (2003) Validity of 10 electronic pedometers for measuring steps distance and energy cost. Med Sci Sports Exerc 35:1455–1460PubMedGoogle Scholar
  10. Crow MT, Kushmerick MJ (1982) Chemical energetics of slow-and fast-twitch muscle of the mouse. J Gen Physiol 79:147–166CrossRefPubMedGoogle Scholar
  11. Donovan CM, Brooks GA (1977) Muscular efficiency during steady-rate exercise. II Effects of walking speed and work rate. J Appl Physiol 43:431–439PubMedGoogle Scholar
  12. Gottschall JS, Kram R (2003) Energy cost and muscular activity required for propulsion during walking. J Appl Physiol 94:1766–1772PubMedGoogle Scholar
  13. Hopkins WG (2001) Generalizing to a population. In: A new view of statistics (at http//sportsci.org/stats/.: On line text)Google Scholar
  14. Howald H, Pette D, Simoneau J-A, Uber A, Hoppeler H, Cerretelli PI (1990) Effects of chronic hyposia on muscle enzyme activities. Int J Sports Med 11:S10–S14PubMedGoogle Scholar
  15. Hunter GR, Newcomer BR, Larson-Meyer DE, Bamman MM, Weinsier RL (2001) Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 24:654–661Google Scholar
  16. Hunter GR, Weinsier RL, McCarthy JP, Larson-Meyer DE, Newcomer BR (2001) Hemoglobin muscle oxidative capacity and VO2max in African-American and Caucasian women. Med Sci Sports Exerc 33:1739–1743CrossRefPubMedGoogle Scholar
  17. Larsen HB (2003) Kenyan dominance in distance running. Comp Biochem Physiol A Comp Physiol 136:161–170CrossRefGoogle Scholar
  18. Larson-Meyer DE, Newcomer BR, Hunter GR, Hetherington HP, Weinsier R (2000) 31P MRS measurement of mitochondrial function in skeletal muscle: reliability force-level sensitivity and relation to whole body maximal oxygen uptake. NMR in Biomedicine 13:14–17CrossRefGoogle Scholar
  19. Larson-Meyer DE, Newcomer BR, Hunter GR, Joanisse DR, WR L, Bamman MM (2001) Relation between in-vivo and in-vitro measurements of skeletal muscle oxidative metabolism. Muscle Nerve 24:1665-1676Google Scholar
  20. Lucia A, Rivero J-LL, Perez M, Serrano AL, Calbet JA. L, Santalla A, Chicharro JL (2002) Determinants of VO2 kinetics at high power outputs during a ramp exercise procol. Med Sci Sports Exerc 34:326–331PubMedGoogle Scholar
  21. Lucia A, Hoyos J, Perez M, Santalla A, Chicharro JL (2002) Inverse relationship between VO2max and economy/efficiency in world-class cyclists. Med Sci Sports Exerc 34:2079–2084PubMedGoogle Scholar
  22. Malatesta D, Simar D, Dauvilliers Y, Candau R, Borrani F, Prefaut C, Caillaud C (2003) Energy cost of walking and gait instability in healthy 65- and 80-yr-olds. J Appl Physiol 95:2248–2256PubMedGoogle Scholar
  23. McCully K, Fielding RA, Evans WJ, Leigh JS, Posner JD (1993) Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75:813–819PubMedGoogle Scholar
  24. Morgan D, Martin P, Krahenbuhl GS, Baldini FD (1991) Variability in running economy and mechanics among trained male runners. Med Sci Sports Exerc 23:378–383PubMedGoogle Scholar
  25. Newcomer BR, Boska M (1997) Adenosine triphosphate production rates metabolic economy calculations ph phosphomonoesters phosphodiesters and force output during short-duration maximal isometric plantar flexion exercises and repeated maximal isometric plantar flexion exercises. Muscle Nerve 20:336–346CrossRefPubMedGoogle Scholar
  26. Newcomer BR, Larson DE, Bamman MM, Wetzstein CJ, Hunter GR (1999) Muscle injury’s effects on energy metabolism in a trained individual. Med Sci Sports Exerc 31:S70CrossRefGoogle Scholar
  27. Newcomer BR, Larson-Meyer DE, Hunter GR, Landers KL, Weinsier RL (2001) Skeletal muscle metabolism in overweight and post-overweight women: an isometric exercise study using 31P magnetic resonance spectroscopy. Int J Obes 25:1309–1315CrossRefGoogle Scholar
  28. Ogilvie RW, Feeback DL (1990) A metachromatic dye-ATPase method for the simultaneous identification of skeletal muscle fiber types I IIA IIB and IIC. Stain Tech 65:231–241Google Scholar
  29. Pate RR, Macera CA, Bailey SP, Bartoli WP, Powell KE (1992) Physiological anthropometric and training correlates of running economy. Med Sci Sports Exerc 24:1128–1133Google Scholar
  30. Pereira J, Wessels A, Moorman A, Sageant A. (1995) New methods for the accurate characterization of single human skeletal muscle fibres demonstrates a relation between mATPase and MyHC expression in pure and hybrid fibre types. J Mus Res Cell Motil 16:21–34CrossRefGoogle Scholar
  31. Perez M, Lucia A, Rivero JL, Serrano AL, Calbet JA, Delgado MA, Cicharro JL (2002) Effects of transcutaneous short-term electrical stimulation on M. vastus lateralis characteristics of healthy young men. Pflugers Archiv Europ J Physiol 443:866–874CrossRefGoogle Scholar
  32. Pollock ML (1977) Submaximal and maxima working capacity elite distance runners. Part I: cardiorespiratory aspects. An NY Acad Sci 301:310–322Google Scholar
  33. Rowland TW, Green GM (1988). Physiological responses to treadmill exercise in females: adult-child differences. Med Sci Sports Exerc 20:474–478PubMedGoogle Scholar
  34. Serrano AL, Perez M, Lucia ACJL, Quiroz-Rothe E, Rivero JL (2001) Immunolabelling histochemistry and in situ hybridization in human skeletal muscle fibres to detect myosin heavy chain expression at the protein and mRNA level. J Anat 199:329–337CrossRefPubMedGoogle Scholar
  35. Simoneau JA, Kelley DE (1997) Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 83:66–71Google Scholar
  36. Stal P, Eriksson PO, Schiaffino S, Butler-Browne GS, Thornell LE (1994) Differences in myosin composition between human oro-facial masticatory and limb muscles: enzyme-, immunohisto- and biochemical studies. J Mus Res Cell Mot 15:517–534CrossRefGoogle Scholar
  37. Staron RS (1991) Correlation between myofibrillar ATPase activity and myosin heavy chain composition in single human musclefibers. Histochem 96:21–24CrossRefGoogle Scholar
  38. Treuth MS, Hunter GR, Weinsier RL, Kell S (1995) Energy expenditure and substrate utilization in older women after strength training: 24 hour metabolic chamber. J Appl Physiol 78:2140–2146PubMedGoogle Scholar
  39. Weinsier RL, Hunter GR, Zuckerman PA, Redden DT, Darnell BE, Larson DE, Newcomer BR, Goran MI (2000) Energy expenditure and free-living physical activity in black and white women: comparison before and after weight loss. Am J Clin Nutr 71:1138–1146PubMedGoogle Scholar
  40. de Weir JB (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109:1–9PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Gary R. Hunter
    • 1
  • Marcas M. Bamman
    • 2
  • D. Enette Larson-Meyer
    • 3
  • Denis R. Joanisse
    • 4
  • John P. McCarthy
    • 5
  • Tamilane E. Blaudeau
    • 6
  • Bradley R. Newcomer
    • 7
  1. 1.Human Studies DepartmentUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Physiology and Biophysics DepartmentUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.Pennington Biomedical Research CenterBaton RougeUSA
  4. 4.Laval Hospital Research CenterSaint FoyCanada
  5. 5.Physical Therapy DepartmentUniversity of Alabama at BirminghamBirmingham
  6. 6.Human Studies DepartmentUniversity of Alabama at BirminghamBirmingham
  7. 7.Dept of Critical Care and Diagnostic CareUniversity of Alabama At BirminghamBirmingham

Personalised recommendations