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Age, muscle fatigue, and walking endurance in pre-menopausal women

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Abstract

Aging is associated with loss of endurance; however, aging is also associated with decreased fatigue during maximal isometric contractions. The aims of this study were to examine the relationship between age and walking endurance (WE) and maximal isometric fatigue (MIF) and to determine which metabolic/fitness components explain the expected age effects on WE and MIF. Subjects were 96 pre-menopausal women. Oxygen uptake (walking economy) was assessed during a 3-mph walk; aerobic capacity and WE by progressive treadmill test; knee extension strength by isometric contractions, MIF during a 90-s isometric plantar flexion (muscle metabolism measured by 31P MRS). Age was related to increased walking economy (low VO2, r = −0.19, P < 0.03) and muscle metabolic economy (force/ATP, 0.34, P = 0.01), and reduced MIF (−0.26, P < 0.03). However, age was associated with reduced WE (−0.28, P < 0.01). Multiple regression showed that muscle metabolic economy explained the age-related decrease in MIF (partial r for MIF and age −0.13, P = 0.35) whereas walking economy did not explain the age-related decrease in WE (partial r for WE and age −0.25, P < 0.02). Inclusion of VO2max and knee endurance strength accounted for the age-related decreased WE (partial r for WE and age = 0.03, P > 0.80). In premenopausal women, age is related to WE and MIF. In addition, these results support the hypothesis that age-related increases in metabolic economy may decrease MIF. However, decreased muscle strength and oxidative capacity are related to WE.

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References

  • Bamman MM, Hill VJ, Adams GR, Haddad F, Wetzstein CJ, Gower BA, Ahmed A, Hunter GR (2003) Gender differences in resistance-training-induced myofiber hypertrophy among older adults. J Gerontol A Biol Sci Med Sci 58:108–116

    PubMed  Google Scholar 

  • Baudry S, Klass M, Pasquet B, Duchateau J (2007) Age-related fatigability of the ankle dorsiflexor muscle during concentric and eccentric contractions. Eur J Appl Physiol 100:515–525

    Article  PubMed  Google Scholar 

  • Boska M (1994) ATP production rates as a function of force level in the human gastrocnemius/soleus using P MRS. MRM 32:1–10

    CAS  Google Scholar 

  • Callahan DM, Foulis SA, Kent-Braun JA (2009) Age-related fatigue resistance in the knee extensor muscles is specific to contraction mode. Muscle Nerve 39:692–702

    Article  PubMed  Google Scholar 

  • Chung LH, Callahan DM, Kent-Braun JA (2007) Age-related resistance to skeletal muscle fatigue is preserved during ischemia. J Appl Physiol 103:1628–1635

    Article  PubMed  Google Scholar 

  • Coyle EF, Sidossis LS, Horowitz JF, Beltz JD (1992) Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sport Exerc 24:782–788

    CAS  Google Scholar 

  • Crow MT, Kushmerick MJ (1982) Chemical energetics of slow-and fast-twitch muscle of the mouse. J Gen Physiol 79:147–166

    Article  PubMed  CAS  Google Scholar 

  • Ditor DS, Hicks AL (2000) The effect of age and gender on the relative fatigability of the human adductor pollicis muscle. Can J Physiol Pharmacol 78:781–790

    Article  PubMed  CAS  Google Scholar 

  • Forbes SJ, Paganini AT, Slade JM, Towse TF, Meyer RA (2009) Phosphocreatine recovery kinetics following low-and high-intensity exercise in human triceps surae and rat posterior hindlimb muscles. Am J Physiol 296:161–170

    Google Scholar 

  • Frontera WR, Meredith CN, O’Reilly KP, Evans WJ (1990) Strength training and determinants of Vo2max in older men. J Appl Physiol 68:329–333

    PubMed  CAS  Google Scholar 

  • Hagberg JM, Allen WK, Seals DR, Hurley BF, Ehsani AA, Holloszy JO (1985) A hemodynamic comparison of young and older endurance athletes during exercise. J Appl Physiol 58:2041–2046

    PubMed  CAS  Google Scholar 

  • Hartman MJ, Fields DA, Byrne NM, Hunter GR (2007) Resistance training improves metabolic economy during functional tasks in older adults. J Strength Cond Res 21:91–95

    Article  PubMed  Google Scholar 

  • Hepple RT, Hagen JL, Krause DJ, Baker DJ (2004) Skeletal muscle aging in F344BN F1-hybrid rats. II. Imprved contractile economy in senescence helps compensate for reduced ATP-generating capacity. J Gerontol Biol Sci 59A:1111–1119

    CAS  Google Scholar 

  • Hickson RC, Dvorak BA, Gorostiaga EM, Kurowski TT, Foster C (1988) Potential for strength and endurance training to amplify endurance performance. J Appl Physiol 65:2285–2290

    PubMed  CAS  Google Scholar 

  • Holly RG (1988) Measurement of maximal rate of oxygen uptake. In: Blair SN, Painter P, Pate RR, Smith LK, Taylor CB (eds) Resource manual for guidelines for exercise testing and prescription. Lea & Febiger, Philadelphia, pp 171–177

    Google Scholar 

  • Hunter GR, Treuth MS, Weinsier RL, Kekes-Szabo T, Kell SH, Roth DL, Nicholson C (1995) The effects of strength conditioning on older women’s ability to perform daily tasks. J Am Geriatr Soc 43:756–760

    PubMed  CAS  Google Scholar 

  • 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 24:654–661

    Article  PubMed  CAS  Google Scholar 

  • Hunter GR, Newcomer BR, Weinsier RL, Karapondo DL, Larson-Meyer DE, Joanise DR, Bamman MM (2002) Age is independently related to muscle metabolic capacity in premenopausal women. J Appl Physiol 93:70–76

    PubMed  Google Scholar 

  • Hunter GR, McCarthy JP, Bamman MM (2004) Effects of resistance training on older adults. Sports Med 34:329–348

    Article  PubMed  Google Scholar 

  • Jacobsson A, Borg K, Edstrom L (1990) Fiber-type composition, structure and cytoskeletal protein location of fibers in the anterior tibial muscle. Acta Neuropathol 80:459–468

    Article  Google Scholar 

  • Katz A, Sahlin K, Henriksson J (1986) Muscle ATP turnover rate during isometric contraction in humans. J Appl Physiol 60:1839–1842

    Article  PubMed  CAS  Google Scholar 

  • Kent-Braun JA (2009) Skeletal Muscle fatigue in old age: whose advantage. Exerc Sport Sci Rev 37:3–9

    Article  PubMed  Google Scholar 

  • Kent-Braun JA, Ng AV (2000) Skeletal muscle oxidative capacity in young and older women and men. J Appl Physiol 89:1072–1078

    PubMed  CAS  Google Scholar 

  • Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823

    PubMed  CAS  Google Scholar 

  • Klass M, Baudry S, Duchateau J (2007) Voluntray activation during maximal contraction with advancing age: a brief review. Eur J Appl Physiol 100:543–551

    Article  PubMed  Google Scholar 

  • Landers KA, Hunter GR, Wetzstein CJ, Bamman MM, Weinsier RL (2001) The interrelationship among muscle mass, strength, and the ability to perform physical tasks of daily living in younger and older women. J Gerontol 56A:B443–B448

    Google Scholar 

  • Lanza IR, Towse TF, Caldwell GE, Wigmore DM, Kent-Braun JA (2003) Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol 95:2361–2369

    PubMed  CAS  Google Scholar 

  • Lanza IR, Russ DW, Kent-Braun JA (2004) Age-related enhancement of fatigue resistance in evident in men during both isometric and dynamic tasks. J Appl Physiol 97:967–975

    Article  PubMed  Google Scholar 

  • Lanza IR, Befroy DE, Kent-Braun JA (2005) Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J Appl Physiol 99:1736–1744

    Article  PubMed  CAS  Google Scholar 

  • Lanza IR, Wigmore DM, Belfroy DE, Kent-Braun JA (2006) In vivo ATP production during free-flow and ischaemic muscle contractions in humans. J Physiol 577:353–367

    Article  PubMed  CAS  Google Scholar 

  • Larew K, Hunter GR, Larson-Meyer EE, Newcomer BR, McCarthy JP, Weinsier RL (2003) Muscle metabolic function, exercise performance, and weight gain. Med Sci Sports Exerc 35:230–236

    Article  PubMed  Google Scholar 

  • 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 Biomed 13:14–17

    Article  PubMed  CAS  Google Scholar 

  • Lexell J (1995) Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50(Spec No.):11–1

    Google Scholar 

  • Lindstrom B, Lexell J, Gerdie B, Downham D (1997) Skeletal muscle fatigue and endurance in young and old men and women. J Gerontol A Biol Sci Med Sci 52:B59–B66

    PubMed  CAS  Google Scholar 

  • Makrides L, Heigenhauser GJF, Jones NL (1990) High intensity endurance training in 20 to 30 and 60 to 70 year old healthy men. J Appl Physiol 69:1792–1798

    PubMed  CAS  Google Scholar 

  • McCarthy JP, Hunter GR, Weinsier RL, Larson-Meyer DE, Bamman MM, Landers KA, Newcomer BR (2006) Ethnic differences in triceps surae muscle-tendon complex and walking economy. J Strength Cond Res 20:511–518

    PubMed  Google Scholar 

  • McNeil DJ, Rice CL (2007) Fatiguability is increased with age during velocity-depedent contractions of the dorsiflexors. J Gerontol A Biol Sci Med Sci 62:624–629

    PubMed  Google Scholar 

  • Narici MV, Bordini M, Cerretelli P (1991) Effect of aging on human adductor pollicis muscle function. J Appl Physiol 71:1277–1281

    PubMed  CAS  Google Scholar 

  • 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 20:336–346

    Article  PubMed  CAS  Google Scholar 

  • 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 25:1309–1315

    Article  CAS  Google Scholar 

  • Parker ND, Hunter GR, Treuth MS, Kekes-Szabo T, Kell SH, Weinsier R, White M (1996) Effects of strength training on cardiovascular responses during a submaximal walk and a weght-loaded walking test in older females. J Cardpulm Rehabil 16:56–62

    Article  CAS  Google Scholar 

  • Petrella JK, Kim J, Tuggle SC, Hall SR, Bamman MM (2005) Age differences in knee extension power, contratile velocity, and fatigability. J Appl Physiol 98:211–220

    Article  PubMed  Google Scholar 

  • Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PWR (1995) Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 78:2033–2038

    PubMed  CAS  Google Scholar 

  • Quistorff B, Johansen L, Sahlin K (1992) Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochemistry 291:681–686

    Google Scholar 

  • Russ DW, Towse TF, Wigmore DM, Lanza IR, Kent-Braun JA (2008) Contrasting influences of age and sex on muscle fatigue. Med Sci Sports Exerc 40:234–241

    Article  PubMed  Google Scholar 

  • Stone MH, Wilson GD, Blessing D, Rozenek R (1983) Cardiovascular responses to short-term olympic style weight training in young men. Can J Appl Sport Sci 8:134–139

    PubMed  CAS  Google Scholar 

  • Szentesi P, Zaremba R, van Mechelen W, Stienen M (2001) ATP utilization for calcium uptake and force production in different types of human skeletal muscle fibres. J Physiol 531:393–403

    Article  PubMed  CAS  Google Scholar 

  • Tevald MA, Foulis SA, Lanza IR, Kent-Braun JA (2009) Lower energy cost of skeletal muscle contractions in older humans. Am J Physiol Endocrinol Metab 298:P729–P739

    Google Scholar 

  • Woo JS, Derleth C, Stratton JR, Levy WC (2006) The influence of age, gender, and training on exercise efficiency. J Am Coll Cardiol 47:1049–1057

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge Bob Petri, David Bryan, Amy Thomas, and Betty Darnell for technical assistance and Paul Zuckerman for Program coordinating. We wish to thank our sources of support: NIH grants R01 DK 49779, R01 DK51684, R01 AG027084-S1, General Clinical Research Center grant M01-RR00032, Clinical Nutrition Research Unit grant P30-DK56336, and UAB University-Wide Clinical Nutrition Research Center grant. The Nestlé Food Co., Solon, OH, USA, and the Stouffer’s Lean Cuisine® provided food entrées. We have no professional relationships with companies or manufacturers who will benefit from the results of the present study.

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Authors and Affiliations

  1. Department of Human Studies, University of Alabama at Birmingham, 901 South 13th Street, Birmingham, AL, 35294-1250, USA

    Gary R. Hunter

  2. Department of Physical Therapy, University of Alabama at Birmingham, Birmingham, USA

    C. Scott Bickel

  3. Department of Nutrition Sciences, University of Alabama at Birmingham, Birmingham, USA

    Gary R. Hunter & Pedro Del Corral

  4. Department of Physiology and Biophysics, University of Alabama at Birmingham, Birmingham, USA

    Marcas M. Bamman

  5. Nuclear Medicine Technology Department, University of Alabama at Birmingham, Birmingham, USA

    Bradley R. Newcomer

  6. School of Movement Studies, Queensland University of Technology, Brisbane, QLD, Australia

    Nuala M. Byrne & Andrew P. Hills

  7. Department of Family and Consumer Sciences, University of Wyoming, Laramie, WY, USA

    D. Enette Larson-Meyer

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  1. Gary R. Hunter
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Correspondence to Gary R. Hunter.

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Communicated by Klaas Westerterp.

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Hunter, G.R., Bickel, C.S., Corral, P.D. et al. Age, muscle fatigue, and walking endurance in pre-menopausal women. Eur J Appl Physiol 111, 715–723 (2011). https://doi.org/10.1007/s00421-010-1694-1

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