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Effect of age on in vivo oxidative capacity in two locomotory muscles of the leg

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Abstract

To determine the effects of age and sex on in vivo mitochondrial function of distinct locomotory muscles, the tibialis anterior (TA) and medial gastrocnemius (MG), of young (Y; 24 ± 3 years) and older (O; 69 ± 4) men (M) and women (W) of similar overall physical activity (PA) was compared. In vivo mitochondrial function was measured using phosphorus magnetic resonance spectroscopy, and PA and physical function were measured in all subjects. Overall PA was similar among the groups, although O (n = 17) had fewer daily minutes of moderate-to-vigorous PA (p = 0.001), and slowed physical function (p < 0.05 for all variables), compared with Y (n = 17). In TA, oxidative capacity (V max; mM s−1) was higher in O than Y (p < 0.001; Y = 0.90 ± 0.12; O = 1.12 ± 0.18). There was no effect of age in MG (p = 0.5; Y = 0.91 ± 0.17; O = 0.96 ± 0.24), but women had higher oxidative capacity than men (p = 0.007; M = 0.84 ± 0.18; W = 1.03 ± 0.18). In vivo mitochondrial function was preserved in healthy O men and women, despite lower intensity PA and physical function in this group. The extent to which compensatory changes in gait may be responsible for this preservation warrants further investigation. Furthermore, women had higher oxidative capacity in the MG, but not the TA.

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References

  • Benjuya N, Melzer I, Kaplanski J (2004) Aging-induced shifts from a reliance on sensory input to muscle cocontraction during balanced standing. J Gerontol A Biol Sci Med Sci 59(2):166–171

    Article  PubMed  Google Scholar 

  • Brierley EJ, Johnson MA, James OF, Turnbull DM (1996) Effects of physical activity and age on mitochondrial function. QJM 89(4):251–258

    Article  PubMed  CAS  Google Scholar 

  • Brierley EJ, Johnson MA, James OF, Turnbull DM (1997) Mitochondrial involvement in the ageing process. Facts and controversies. Mol Cell Biochem 174(1–2):325–328

    Article  PubMed  CAS  Google Scholar 

  • Chilibeck PD, Paterson DH, McCreary CR, Marsh GD, Cunningham DA, Thompson RT (1998) The effects of age on kinetics of oxygen uptake and phosphocreatine in humans during exercise. Exp Physiol 83(1):107–117

    PubMed  CAS  Google Scholar 

  • Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, Holloszy JO (1992) Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J Gerontol 47(3):B71–76

    Article  PubMed  CAS  Google Scholar 

  • Conley KE, Jubrias SA, Esselman PC (2000) Oxidative capacity and ageing in human muscle. J Physiol 526 Pt 1:203–210

  • den Hoed M, Hesselink MK, van Kranenburg GP, Westerterp KR (2008) Habitual physical activity in daily life correlates positively with markers for mitochondrial capacity. J Appl Physiol 105(2):561–568. doi:10.1152/japplphysiol.00091.2008

    Article  Google Scholar 

  • Edgerton VR, Smith JL, Simpson DR (1975) Muscle fibre type populations of human leg muscles. Histochem J 7(3):259–266

    Article  PubMed  CAS  Google Scholar 

  • Essen–Gustavsson B, Borges O (1986) Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 126(1):107–114

    Article  PubMed  Google Scholar 

  • Forbes SC, Paganini AT, Slade JM, Towse TF, Meyer RA, Forbes SC, Paganini AT, Slade JM, Towse TF, Meyer RA (2009a) Phosphocreatine recovery kinetics following low- and high-intensity exercise in human triceps surae and rat posterior hindlimb muscles. Am J Physiol Regul Integr Comp Physiol 296(1):R161–170. doi:10.1152/ajpregu.90704.2008

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Forbes SC, Slade JM, Francis RM, Meyer RA (2009b) Comparison of oxidative capacity among leg muscles in humans using gated 31P 2-D chemical shift imaging. NMR Biomed 22(10):1063–1071. doi:10.1002/nbm.1413

    PubMed  CAS  Google Scholar 

  • Forbes SC, Slade JM, Meyer RA (2008) Short-term high-intensity interval training improves phosphocreatine recovery kinetics following moderate-intensity exercise in humans. Appl Physiol Nutr Metab 33(6):1124–1131. doi:10.1139/H08–099

    Article  PubMed  CAS  Google Scholar 

  • Freedson PS, Melanson E, Sirard J (1998) Calibration of the Computer Science and Applications, Inc. accelerometer. Med Sci Sports Exerc 30(5):777–781

    Article  PubMed  CAS  Google Scholar 

  • Gollnick PD, Armstrong RB, Saltin B, Saubert CW, Sembrowich WL, Shepherd RE (1973) Effect of training on enzyme activity and fiber composition of human skeletal muscle. J Appl Physiol 34(1):107–111

    PubMed  CAS  Google Scholar 

  • Gottschall JS, Kram R (2003) Energy cost and muscular activity required for propulsion during walking. J Appl Physiol 94(5):1766–1772. doi:10.1152/japplphysiol.00670.2002

    PubMed  Google Scholar 

  • Gregory CM, Vandenborne K, Dudley GA (2001) Metabolic enzymes and phenotypic expression among human locomotor muscles. Muscle Nerve 24 (3):387–393. doi:10.1002/1097–4598(200103)24:3<387::AID-MUS1010>3.0.CO;2-M [pii]

  • Grimby G, Danneskiold-Samsoe B, Hvid K, Saltin B (1982) Morphology and enzymatic capacity in arm and leg muscles in 78–81 year old men and women. Acta Physiol Scand 115(1):125–134

    Article  PubMed  CAS  Google Scholar 

  • Harris RC, Hultman E, Nordesjo LO (1974) Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand J Clin Lab Invest 33(2):109–120

    Article  PubMed  CAS  Google Scholar 

  • Hasson CJ, Caldwell GE (2012) Effects of age on mechanical properties of dorsiflexor and plantarflexor muscles. Ann Biomed Eng 40(5):1088–1101. doi:10.1007/s10439–011–0481–4

    Article  PubMed  Google Scholar 

  • Hasson CJ, Kent-Braun JA, Caldwell GE (2011) Contractile and non-contractile tissue volume and distribution in ankle muscles of young and older adults. J Biomech 44(12):2299–2306. doi:10.1016/j.jbiomech.2011.05.031

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasson CJ, Van Emmerik RE, Caldwell GE (2014) Balance decrements are associated with age-related muscle property changes. J Appl Biomech. doi:10.1123/jab.2013–0294

    PubMed  Google Scholar 

  • Hikida RS, Gollnick PD, Dudley GA, Convertino VA, Buchanan P (1989) Structural and metabolic characteristics of human skeletal muscle following 30 days of simulated microgravity. Aviat Space Environ Med 60(7):664–670

    PubMed  CAS  Google Scholar 

  • Hortobagyi T, Finch A, Solnik S, Rider P, DeVita P (2011) Association between muscle activation and metabolic cost of walking in young and old adults. J Gerontol A Biol Sci Med Sci 66(5):541–547. doi:10.1093/gerona/glr008

    Article  PubMed  Google Scholar 

  • Houmard JA, Weidner ML, Gavigan KE, Tyndall GL, Hickey MS, Alshami A (1998) Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J Appl Physiol 85(4):1337–1341

    PubMed  CAS  Google Scholar 

  • Hunter SK, Critchlow A, Shin IS, Enoka RM (2004) Men are more fatigable than strength-matched women when performing intermittent submaximal contractions. J Appl Physiol 96(6):2125–2132. doi:10.1152/japplphysiol.01342.2003

    Article  PubMed  Google Scholar 

  • Hutter E, Skovbro M, Lener B, Prats C, Rabol R, Dela F, Jansen-Durr P (2007) Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 6(2):245–256. doi:10.1111/j.1474–9726.2007.00282.x

    Article  PubMed  Google Scholar 

  • Jacobs RA, Diaz V, Soldini L, Haider T, Thomassen M, Nordsborg NB, Gassmann M, Lundby C (2013) Fast-twitch glycolytic skeletal muscle is predisposed to age-induced impairments in mitochondrial function. J Gerontol a-Biol 68(9):1010–1022. doi:10.1093/gerona/gls335

    Article  CAS  Google Scholar 

  • Jacobs RA, Lundby C (2013) Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes. J Appl Physiol (1985) 114(3):344–350. doi:10.1152/japplphysiol.01081.2012

    Article  CAS  Google Scholar 

  • Johnson ML, Robinson MM, Nair KS (2013) Skeletal muscle aging and the mitochondrion. Trends Endocrin Met 24(5):247–256. doi:10.1016/j.tem.2012.12.003

    Article  CAS  Google Scholar 

  • Karakelides H, Irving BA, Short KR, O’Brien P, Nair KS, Karakelides H, Irving BA, Short KR, O’Brien P, Nair KS (2010) Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 59(1):89–97. doi:10.2337/Db09-0591

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kemp GJ, Radda GK (1994) Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q 10(1):43–63

    PubMed  CAS  Google Scholar 

  • Kent-Braun JA, Ng AV (1999) Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 87(1):22–29

    PubMed  CAS  Google Scholar 

  • Kent-Braun JA, Ng AV (2000) Skeletal muscle oxidative capacity in young and older women and men. J Appl Physiol 89(3):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(5):1813–1823. doi:10.1152/japplphysiol.00091.2002

    PubMed  CAS  Google Scholar 

  • Kent-Braun JA, Walker CH, Weiner MW, Miller RG (1998) Functional significance of upper and lower motor neuron impairment in amyotrophic lateral sclerosis. Muscle Nerve 21(6):762–768

    Article  PubMed  CAS  Google Scholar 

  • Konopka AR, Nair KS (2013) Mitochondrial and skeletal muscle health with advancing age. Mol Cell Endocrinol 379(1–2):19–29. doi:10.1016/j.mce.2013.05.008

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Konopka AR, Suer MK, Wolff CA, Harber MP (2014) Markers of human skeletal muscle mitochondrial biogenesis and quality control: effects of age and aerobic exercise training. J Gerontol A Biol Sci Med Sci 69(4):371–378. doi:10.1093/gerona/glt107

    Article  PubMed  CAS  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(5):1736–1744. doi:10.1152/japplphysiol.00566.2005

    Article  PubMed  CAS  Google Scholar 

  • Lanza IR, Bhagra S, Nair KS, Port JD (2011) Measurement of human skeletal muscle oxidative capacity by 31P-MR spectroscopy: a cross-validation with in vitro measurements. J Magn Reson Imaging 34(5):1143–1150. doi:10.1002/jmri.22733

    Article  PubMed  PubMed Central  Google Scholar 

  • Lanza IR, Larsen RG, Kent-Braun JA (2007) Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J Physiol 583(Pt 3):1093–1105. doi:10.1113/jphysiol.2007.138362

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lanza IR, Wigmore DM, Befroy DE, Kent-Braun JA (2006) In vivo ATP production during free-flow and ischaemic muscle contractions in humans. J Physiol 577(Pt 1):353–367. doi:10.1113/jphysiol.2006.114249

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Larsen RG, Befroy DE, Kent-Braun JA (2012a) High-intensity interval training increases in vivo oxidative capacity with no effect on Pi→ATP rate in resting human muscle. Am J Physiol Regul Integr Comp Physiol. doi:10.1152/ajpregu.00409.2012

    PubMed Central  Google Scholar 

  • Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA (2009) In vivo oxidative capacity varies with muscle and training status in young adults. J Appl Physiol 107(3):873–879. doi:10.1152/japplphysiol.00260.2009

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA (2012b) Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior. Appl Physiol Nutr Metab 37(1):88–99. doi:10.1139/h11–135

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Matthews CE, Chen KY, Freedson PS, Buchowski MS, Beech BM, Pate RR, Troiano RP (2008) Amount of time spent in sedentary behaviors in the United States, 2003–2004. Am J Epidemiol 167(7):875–881. doi:10.1093/aje/kwm390

    Article  PubMed  PubMed Central  Google Scholar 

  • McCully KK, Fielding RA, Evans WJ, Leigh JS Jr, Posner JD (1993) Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75(2):813–819

    PubMed  CAS  Google Scholar 

  • McCully KK, Forciea MA, Hack LM, Donlon E, Wheatley RW, Oatis CA, Goldberg T, Chance B (1991) Muscle metabolism in older subjects using 31P magnetic resonance spectroscopy. Can J Physiol Pharmacol 69(5):576–580

    Article  PubMed  CAS  Google Scholar 

  • Meyer RA (1988) A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Physiol 254(4 Pt 1):C548–553

    PubMed  CAS  Google Scholar 

  • Meyer RA (1989) Linear dependence of muscle phosphocreatine kinetics on total creatine content. Am J Physiol 257(6 Pt 1):C1149–1157

    PubMed  CAS  Google Scholar 

  • Pastoris O, Boschi F, Verri M, Baiardi P, Felzani G, Vecchiet J, Dossena M, Catapano M (2000) The effects of aging on enzyme activities and metabolite concentrations in skeletal muscle from sedentary male and female subjects. Exp Gerontol 35(1):95–104

    Article  PubMed  CAS  Google Scholar 

  • Picard M, Ritchie D, Wright KJ, Romestaing C, Thomas MM, Rowan SL, Taivassalo T, Hepple RT (2010) Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 9(6):1032–1046. doi:10.1111/j.1474–9726.2010.00628.x

    Article  PubMed  CAS  Google Scholar 

  • Proctor DN, Joyner MJ (1997) Skeletal muscle mass and the reduction of VO2max in trained older subjects. J Appl Physiol 82(5):1411–1415

    PubMed  CAS  Google Scholar 

  • Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PW (1995) Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 78(6):2033–2038

    PubMed  CAS  Google Scholar 

  • Purves-Smith FM, Sgarioto N, Hepple RT (2014) Fiber typing in aging muscle. Exerc Sport Sci Rev 42(2):45–52. doi:10.1249/JES.0000000000000012

    Article  PubMed  Google Scholar 

  • Rasmussen UF, Krustrup P, Kjaer M, Rasmussen HN (2003) Human skeletal muscle mitochondrial metabolism in youth and senescence: no signs of functional changes in ATP formation and mitochondrial oxidative capacity. Pflugers Arch 446(2):270–278. doi:10.1007/s00424–003–1022–2

    PubMed  CAS  Google Scholar 

  • Rooyackers OE, Adey DB, Ades PA, Nair KS (1996) Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc Natl Acad Sci U S A 93(26):15364–15369

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ruby BC, Robergs RA (1994) Gender differences in substrate utilisation during exercise. Sports Med 17(6):393–410

    Article  PubMed  CAS  Google Scholar 

  • Russ DW, Kent-Braun JA (2003) Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol 94(6):2414–2422. doi:10.1152/japplphysiol.01145.2002

    PubMed  Google Scholar 

  • Russ DW, Kent-Braun JA (2004) Is skeletal muscle oxidative capacity decreased in old age? Sports Med 34(4):221–229

    Article  PubMed  Google Scholar 

  • Russ DW, Lanza IR, Rothman D, Kent-Braun JA (2005) Sex differences in glycolysis during brief, intense isometric contractions. Muscle Nerve 32(5):647–655. doi:10.1002/mus.20396

    Article  PubMed  CAS  Google Scholar 

  • Ryschon TW, Fowler MD, Wysong RE, Anthony A, Balaban RS (1997) Efficiency of human skeletal muscle in vivo: comparison of isometric, concentric, and eccentric muscle action. J Appl Physiol 83(3):867–874

    PubMed  CAS  Google Scholar 

  • Schmitz A, Silder A, Heiderscheit B, Mahoney J, Thelen DG (2009) Differences in lower-extremity muscular activation during walking between healthy older and young adults. J Electromyogr Kinesiol 19(6):1085–1091. doi:10.1016/j.jelekin.2008.10.008

    Article  PubMed  PubMed Central  Google Scholar 

  • Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS (2005) Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci U S A 102(15):5618–5623. doi:10.1073/pnas.0501559102

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS (2003) Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52(8):1888–1896. doi:10.2337/diabetes.52.8.1888

    Article  PubMed  CAS  Google Scholar 

  • Simoneau E, Martin A, Van Hoecke J (2005) Muscular performances at the ankle joint in young and elderly men. J Gerontol A Biol Sci Med Sci 60(4):439–447

    Article  PubMed  Google Scholar 

  • Simonsick EM, Newman AB, Nevitt MC, Kritchevsky SB, Ferrucci L, Guralnik JM, Harris T, Health ABCSG (2001) Measuring higher level physical function in well-functioning older adults: expanding familiar approaches in the Health ABC study. J Gerontol A Biol Sci Med Sci 56(10):M644–649

    Article  PubMed  CAS  Google Scholar 

  • Tartaglia MC, Chen JT, Caramanos Z, Taivassalo T, Arnold DL, Argov Z (2000) Muscle phosphorus magnetic resonance spectroscopy oxidative indices correlate with physical activity. Muscle Nerve 23(2):175–181

    Article  PubMed  CAS  Google Scholar 

  • Taylor DJ, Styles P, Matthews PM, Arnold DA, Gadian DG, Bore P, Radda GK (1986) Energetics of human muscle: exercise-induced ATP depletion. Magn Reson Med 3(1):44–54

    Article  PubMed  CAS  Google Scholar 

  • Tevald MA, Foulis SA, Lanza IR, Kent-Braun JA (2010) Lower energy cost of skeletal muscle contractions in older humans. Am J Physiol Regul Integr Comp Physiol 298(3):R729–739. doi:10.1152/ajpregu.00713.2009

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Troiano RP, Berrigan D, Dodd KW, Masse LC, Tilert T, McDowell M (2008) Physical activity in the United States measured by accelerometer. Med Sci Sports Exerc 40(1):181–188. doi:10.1249/mss.0b013e31815a51b3

    Article  PubMed  Google Scholar 

  • Tucker JM, Welk GJ, Beyler NK (2011) Physical activity in U.S.: adults compliance with the Physical Activity Guidelines for Americans. Am J Prev Med 40(4):454–461. doi:10.1016/j.amepre.2010.12.016

    Article  PubMed  Google Scholar 

  • Winegard KJ, Hicks AL, Sale DG, Vandervoort AA (1996) A 12-year follow-up study of ankle muscle function in older adults. J Gerontol A Biol Sci Med Sci 51(3):B202–207

    Article  PubMed  CAS  Google Scholar 

  • Wolfson L, Judge J, Whipple R, King M (1995) Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 50 Spec No:64–67

  • Wray DW, Nishiyama SK, Monnet A, Wary C, Duteil SS, Carlier PG, Richardson RS (2009) Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics. Am J Physiol Heart Circ Physiol 297(5):H1870–1875. doi:10.1152/ajpheart.00709.2009

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

We thank Douglas Befroy, DPhil, for his expert technical assistance, John Buonaccorsi, PhD for his statistical advice, the members of the Muscle Physiology Lab for their insightful comments, and the study participants for their cheerful assistance with this project. Funding was provided by the National Institute on Aging (R01 AG21094 and K02 AG023582 to JKB), the New Investigator Fellowship Initiative from the Foundation for Physical Therapy (MAT), and the Keck Foundation.

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  1. Department of Kinesiology, University of Massachusetts, Amherst, MA, USA

    Stephen A. Foulis & Jane A. Kent

  2. Department of Rehabilitation Sciences, University of Toledo, 2801 W, Bancroft Street, MS 119, Toledo, OH, 43616, USA

    Michael A. Tevald

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  1. Michael A. Tevald
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Tevald, M.A., Foulis, S.A. & Kent, J.A. Effect of age on in vivo oxidative capacity in two locomotory muscles of the leg. AGE 36, 9713 (2014). https://doi.org/10.1007/s11357-014-9713-5

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