Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles
Abstract
This study compared in vivo measurements of muscle metabolism in humans with magnetic resonance spectroscopy (MRS) and in vitro analysis of biopsies. Healthy subjects [4 young males, 28.2 +/- 6.8 (SD) yr, and 6 older subjects (5 males, 1 female), 66 +/- 6.0 yr] performed a maximal cycle ergometer test, and MRS measurements of the calf muscles and needle biopsies of the lateral gastrocnemius were performed. Biopsies were analyzed for fiber type and citrate synthase (CS) activity. MRS measurements of inorganic phosphate (Pi), phosphocreatine (PCr), ATP, and pH were made using a 1.8-T 78-cm clear-bore magnet-and-spectrometer system. Two or three 5-min bouts of plantar flexion were performed against variable resistance to deplete PCr levels to 50% of resting values (mean end pH 6.99). PCr values during recovery were fit to an exponential curve, and the rate constant (PCrrate) was calculated. PCrrate was used as an index of oxidative metabolism. Older subjects had lower peak O2 uptake (VO2 peak) values (19.2 +/- 5.6 vs. 49.5 +/- 8.1 ml O2.min-1 x kg-1), CS activities (16 +/- 2.8 vs. 25 +/- 2.6 mmol.kg wet wt-1 x min-1), and PCrrate values (25.3 +/- 8. vs. 37.5 +/- 5.3 mmol PCr.kg wet wt-1.min-1) than young subjects. PCrrate correlated with CS activity, and both PCrrate and CS activity correlated with VO2 peak (P < 0.05). No correlations were found between percent fiber type and PCrrate, CS activity, and VO2 peak. These results support studies that showed decreases in muscle metabolism with age in healthy humans and show a good correlation between in vivo and in vitro measurements of oxidative metabolism.
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Skeletal muscle from sedentary older adults exhibits reduced mitochondrial abundance and oxidative capacity.
“Skeletal muscle from sedentary older adults exhibits reduced mitochondrial abundance and oxidative capacity.”
From Combined Training Enhances Skeletal Muscle Mitochondrial Oxidative Capacity Independent of Age (2015) · cites this paper as [8]
Cites
THE SPECIFICITY OF THE HISTOCHEMICAL METHOD FOR ADENOSINE TRIPHOSPHATAS
Padykula, H. A., & Herman, E. (1955) · Journal of Histochemistry & Cytochemistry · doi:10.1177/3.3.170 · Cited by 1,201 · see citing works
Guidelines for Exercise Testing and Prescription
Sharp, N. C. C. (1993) · British Journal of Sports Medicine · doi:10.1136/bjsm.27.2.138-a · Cited by 1,190 · see citing works
Decline in skeletal muscle mitochondrial respiratory chain function: possible factor in ageing
Trounce, I., Byrne, E., & Marzuki, S. (1989) · The Lancet · doi:10.1016/s0140-6736(89)92143-0 · Cited by 730 · see citing works
The time course of phosphorylcreatine resynthesis during recovery of the quadriceps muscle in man
Harris, R. C., Edwards, R. H. T., Hultman, E., Nordesj�, L. O., Nylind, B., & Sahlin, K. (1976) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00585149 · Cited by 527 · see citing works
Cycling efficiency is related to the percentage of Type I muscle fibers
Coyle, E. F., Sidossis, L. S., Horowitz, J. F., & Beltz, J. D. (1992) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199207000-00008 · Cited by 524 · see citing works
Suction applied to a muscle biopsy maximizes sample size
Evans, W. J., Phinney, S. D., & Young, V. R. (1982) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198201000-00018 · Cited by 520 · see citing works
Self-citationA linear model of muscle respiration explains monoexponential phosphocreatine changes
Meyer, R. A. (1988) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1988.254.4.c548 · Cited by 514 · see citing works
Coggan, A. R., Spina, R. J., King, D. S., Rogers, M. A., Rogers, M. A., Brown, M., Nemeth, P. M., & Holloszy, J. O. (1992) · Journal of Gerontology · doi:10.1093/geronj/47.3.b71 · Cited by 456 · see citing works
Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training
Davies, K. J. A., Packer, L., & Brooks, G. A. (1981) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(81)90312-x · Cited by 430 · see citing works
Effects of gender, age, and fitness level on response of VO2max to training in 60-71 yr olds
Kohrt, W. M., Malley, M. T., Coggan, A. R., Spina, R. J., Ogawa, T., Ehsani, A. A., Bourey, R. E., Martin, W. H., & Holloszy, J. O. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.71.5.2004 · Cited by 383 · see citing works
Chance, B., Eleff, S. M., Leigh, J. S., SOKOLOW, D. P., & Sapega, A. A. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.11.6714 · Cited by 318 · see citing works
Self-citationEnergetics of human muscle: Exercise‐induced ATP depletion
Taylor, D. J., Styles, P., Matthews, P. M., Arnold, D. L., Gadian, D. G., Bore, P. J., & Radda, G. K. (1986) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910030107 · Cited by 318 · see citing works
Mitochondrial citric acid cycle and related enzymes: Adaptive response to exercise
Holloszy, J. O., Oscai, L. B., Don, I., & Mole, P. A. (1970) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(70)90017-3 · Cited by 314 · see citing works
Peripheral effects of endurance training in young and old subjects
Meredith, C. N., Frontera, W. R., Fisher, E. C., HUGHES, V. A., Herland, J., Edwards, J. E., & Evans, W. J. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.66.6.2844 · Cited by 231 · see citing works
Self-citationVariability of fiber type distributions within human muscles
Elder, G. C. B., Bradbury, K., & Roberts, R. G. D. (1982) · Journal of Applied Physiology · doi:10.1152/jappl.1982.53.6.1473 · Cited by 226 · see citing works
Histochemical characteristics of human skeletal muscle during aging
LARSSON, L. (1983) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1983.tb00024.x · Cited by 219 · see citing works
Evidence for tissue diffusion limitation of VO2max in normal humans
Roca, J., Hogan, M. C., Story, D., Bebout, D. E., Haab, P., Gonzalez, R., Ueno, O., & Wagner, P. D. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.1.291 · Cited by 218 · see citing works
A critical assessment of methods of measuring metabolite concentrations by NMR spectroscopy
Tofts, P. S., & Wray, S. (1988) · NMR in Biomedicine · doi:10.1002/nbm.1940010103 · Cited by 163 · see citing works
A new double-tuned probed for concurrent 1H and 31P NMR
Schnall, M. D., Subramanian, V. H., Leigh, J. S., & Chance, B. (1985) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(85)90380-4 · Cited by 137 · see citing works
Self-citationHands, L. J., Bore, P. J., Galloway, G. J., Morris, P. J., & Radda, G. K. (1986) · Clinical Science · doi:10.1042/cs0710283 · Cited by 123 · see citing works
Nemeth, P. M., & Pette, D. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013935 · Cited by 119 · see citing works
Wrist flexor muscles of elite rowers measured with magnetic resonance spectroscopy
McCully, K. K., Boden, B. P., Tuchler, M., Fountain, M. R., & Chance, B. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.3.926 · Cited by 118 · see citing works
Self-citationZatina, M. A., Berkowitz, H. D., Gross, G. M., Maris, J. M., & Chance, B. (1986) · Journal of Vascular Surgery · doi:10.1016/0741-5214(86)90103-5 · Cited by 87 · see citing works
Keller, U., OBERHÄNSLI, R., HUBER, P., Widmer, L. K., Aue, W. P., Hassink, R., Müller, S., & Seelig, J. (1985) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1985.tb00289.x · Cited by 64 · see citing works
Muscle metabolism in track athletes, using 31P magnetic resonance spectroscopy
McCully, K. K., Vandenborne, K., DeMeirleir, K. L., Posner, J. D., & LEIGH, J. S. J. (1992) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y92-190 · Cited by 54 · see citing works
Self-citationMagnetic Resonance Spectroscopy Data Analysis
Prammer, M. G. (2005) · doi:10.1109/iembs.1990.690948 · Cited by 3 · see citing works
Comparison of Different Bicycle Ergometer Protocols in Elderly Males
Shaw, C., Gorman, K. M., McCully, K. K., & Posner, J. D. (1993) · Journal of Cardiopulmonary Rehabilitation · doi:10.1097/00008483-199303000-00010 · Cited by 2 · see citing works
Self-citation
Flagged first, then by citations
1 of the 28 references couldn’t be matched to a known paper.
Cited by
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Sarcopenia: Aging-Related Loss of Muscle Mass and Function
Larsson, L., Degens, H., Li, M., Salviati, L., Lee, Y. I., Thompson, W., Kirkland, J. L., & Sandri, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00061.2017 · Cited by 1,797 · see citing works
Bogdanis, G. C., Nevill, M. E., Boobis, L. H., & Lakomy, H. K. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.3.876 · Cited by 691 · see citing works
Oxidative capacity and ageing in human muscle
Conley, K. E., Jubrias, S. A., & Esselman, P. C. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-1-00203.x · Cited by 651 · see citing works
Poole, D. C., & JONES, A. M. (2012) · Comprehensive physiology · doi:10.1002/cphy.c100072 · Cited by 533 · see citing works
Effects of Exercise and Aging on Skeletal MusclePreprint
Distéfano, G., & Goodpaster, B. H. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a029785 · Cited by 493 · see citing works
Gene expression profile of aging in human muscle
Welle, S. L., Brooks, A. I., Delehanty, J. M., Needler, N. A., & Thornton, C. A. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00049.2003 · Cited by 351 · see citing works
Kent‐Braun, J. A., Ng, A., Doyle, J., & Towse, T. F. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00091.2002 · Cited by 351 · see citing works
Coen, P. M., Jubrias, S. A., Distefano, G., Amati, F., Mackey, D. C., Glynn, N. W., Manini, T. M., Wohlgemuth, S. E., Leeuwenburgh, C., Cummings, S. R., et al. (2013) · The Journals of Gerontology: Series A · doi:10.1093/gerona/gls196 · Cited by 323 · see citing works
Mitochondrial dysfunction in aging: Much progress but many unresolved questions
Payne, B. A. I., & Chinnery, P. F. (2015) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2015.05.022 · Cited by 335 · see citing works
Hamaoka, T., McCully, K. K., Quaresima, V., Yamamoto, K., & Chance, B. (2007) · Journal of Biomedical Optics · doi:10.1117/1.2805437 · Cited by 329 · see citing works
Self-citationSkeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2availability
Haseler, L. J., Hogan, M. C., & Richardson, R. S. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.86.6.2013 · Cited by 326 · see citing works
Skeletal Muscle Mitochondria and Aging: A Review
Peterson, C. M., Johannsen, D. L., & Ravussin, É. (2012) · Journal of Aging Research · doi:10.1155/2012/194821 · Cited by 318 · see citing works
Oxidative capacity of human muscle fiber types: effects of age and training status
Proctor, D. N., Sinning, W. E., Walro, J. M., Sieck, G. C., & Lemon, P. W. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.6.2033 · Cited by 283 · see citing works
Sarcopenia of Aging and Its Metabolic Impact
Karakelides, H., & Nair, K. S. (2005) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(05)68005-2 · Cited by 264 · see citing works
Kamel, H. K. (2003) · Nutrition Reviews · doi:10.1301/nr.2003.may.157-167 · Cited by 265 · see citing works
Factors Affecting the Rate of Phosphocreatine Resynthesis Following Intense Exercise
McMahon, S., & Jenkins, D. G. (2002) · Sports Medicine · doi:10.2165/00007256-200232120-00002 · Cited by 262 · see citing works
Chilibeck, P., Kaviani, M., Candow, D., & Zello, G. A. (2017) · Open Access Journal of Sports Medicine · doi:10.2147/oajsm.s123529 · Cited by 235 · see citing works
Skeletal muscle aging and the mitochondrion
Johnson, M. L., Robinson, M. M., & Nair, K. S. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.12.003 · Cited by 233 · see citing works
RYAN, T. E., Erickson, M. L., Brizendine, J. T., Young, H., & McCully, K. K. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00319.2012 · Cited by 233 · see citing works
Self-citationl-Citrulline Supplementation: Impact on Cardiometabolic Health
Allerton, T. D., Proctor, D. N., Stephens, J. M., Dugas, T. R., Spielmann, G., & Irving, B. A. (2018) · Nutrients · doi:10.3390/nu10070921 · Cited by 235 · see citing works
Exercise: Kinetic Considerations for Gas Exchange
Rossiter, H. B. (2010) · Comprehensive physiology · doi:10.1002/cphy.c090010 · Cited by 231 · see citing works
Muscle buffer capacity and aerobic fitness are associated with repeated-sprint ability in women
Bishop, D. J., Edge, J., & Goodman, C. (2004) · European Journal of Applied Physiology · doi:10.1007/s00421-004-1150-1 · Cited by 230 · see citing works
Large energetic adaptations of elderly muscle to resistance and endurance training
Jubrias, S. A., Esselman, P. C., Price, L. B., Cress, M. E., & Conley, K. E. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.5.1663 · Cited by 213 · see citing works
Skeletal muscle gene expression profiles in 20–29 year old and 65–71 year old women
Welle, S., Brooks, A. I., Delehanty, J. M., Needler, N., Bhatt, K., Shah, B., & Thornton, C. A. (2004) · Experimental Gerontology · doi:10.1016/j.exger.2003.11.011 · Cited by 210 · see citing works
Ryan, T. E., Southern, W. M., Reynolds, M. A., & McCully, K. K. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00835.2013 · Cited by 192 · see citing works
Self-citationAge-related changes in ATP-producing pathways in human skeletal muscle in vivo
Lanza, I. R., Befroy, D. E., & Kent‐Braun, J. A. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00566.2005 · Cited by 192 · see citing works
Meckel, Y., Machnai, O., & Eliakim, A. (2009) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31818b9651 · Cited by 187 · see citing works
Skeletal muscle oxidative capacity in young and older women and men
Kent‐Braun, J. A., & Ng, A. V. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.3.1072 · Cited by 186 · see citing works
Linear dependence of muscle phosphocreatine kinetics on oxidative capacity
Paganini, A. T., Foley, J. M., & Meyer, R. A. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.2.c501 · Cited by 186 · see citing works
Noninvasive measurement of phosphocreatine recovery kinetics in single human muscles
Walter, G. A., Vandenborne, K., McCully, K. K., & Leigh, J. S. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.2.c525 · Cited by 185 · see citing works
Self-citation31P magnetic resonance spectroscopy in skeletal muscle: Experts' consensus recommendations
Meyerspeer, M., Boesch, C., Cameron, D., Dezortová, M., Forbes, S. C., Heerschap, A., Jeneson, J. A. L., Kan, H. E., Kent, J. A., Layec, G., et al. (2020) · NMR in Biomedicine · doi:10.1002/nbm.4246 · Cited by 177 · see citing works
Vascular and metabolic response to isolated small muscle mass exercise: effect of age
Lawrenson, L., Poole, J. G., Kim, J. H., Brown, C., Patel, P. M., & Richardson, R. S. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00135.2003 · Cited by 174 · see citing works
Predictors of repeated-sprint ability in elite female hockey players
Bishop, D. J., Lawrence, S. R., & Spencer, M. (2003) · Journal of science and medicine in sport · doi:10.1016/s1440-2440(03)80255-4 · Cited by 173 · see citing works
Methods for Assessing Mitochondrial Function in Diabetes
Perry, C. G. R., Kane, D. A., Lanza, I. R., & Neufer, P. D. (2013) · Diabetes · doi:10.2337/db12-1219 · Cited by 165 · see citing works
Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging
Houmard, J. A., Weidner, M. D., Gavigan, K. E., Tyndall, G. L., Hickey, M. S., & Alshami, A. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.4.1337 · Cited by 158 · see citing works
Skeletal Muscle Mitochondria in the Elderly: Effects of Physical Fitness and Exercise Training
Broskey, N. T., Greggio, C., Boss, A., Boutant, M., Dwyer, A., Schlueter, L., Hans, D., Gremion, G., Kreis, R., Boesch, C., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-3983 · Cited by 157 · see citing works
Kemp, G. J., Ahmad, R., Nicolay, K., & Prompers, J. J. (2014) · Acta Physiologica · doi:10.1111/apha.12307 · Cited by 158 · see citing works
Mitochondrial Involvement and Impact in Aging Skeletal Muscle
Hepple, R. T. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00211 · Cited by 155 · see citing works
Charles‐Edwards, G., Amaral, N., Sleigh, A., Ayis, S. A., Catibog, N., McDonagh, T. A., Monaghan, M. J., Amin-Youssef, G. F., Kemp, G. J., Shah, A. M., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.038516 · Cited by 154 · see citing works
RYAN, T. E., Brophy, P. M., Lin, C., Hickner, R. C., & Neufer, P. D. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.274456 · Cited by 151 · see citing works
Mitochondrial function as a determinant of life span
Lanza, I. R., & Nair, K. S. (2009) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-009-0724-5 · Cited by 148 · see citing works
Ageing: Effects on oxidative function of skeletal muscle in vivo
Taylor, D. J., Kemp, G. J., Thompson, C. H., & Radda, G. K. (1997) · Springer eBooks · doi:10.1007/978-1-4615-6111-8_48 · Cited by 148 · see citing works
Effect of Recovery Mode on Repeated Sprint Ability in Young Basketball Players
Castagna, C., Abt, G., Manzi, V., Annino, G., Padua, E., & D'Ottavio, S. (2008) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31816a4281 · Cited by 141 · see citing works
Creatine supplementation and age influence muscle metabolism during exercise
Smith, S. A., Montain, S. J., Matott, R. P., Zientara, G. P., Jolesz, F. A., & Fielding, R. A. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.4.1349 · Cited by 140 · see citing works
Self-citationCombined Training Enhances Skeletal Muscle Mitochondrial Oxidative Capacity Independent of Age
Irving, B. A., Lanza, I. R., Henderson, G. C., Rao, R. R., Spiegelman, B. M., & Nair, K. S. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3081 · Cited by 139 · see citing works
Mitochondrial respiratory capacity and coupling control decline with age in human skeletal muscle
Porter, C., Hurren, N. M., Cotter, M. V., Bhattarai, N., Reidy, P. T., Dillon, E. L., Durham, W. J., Tuvdendorj, D., Sheffield-Moore, M., Volpi, E., et al. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00125.2015 · Cited by 134 · see citing works
Muscle strength mediates the relationship between mitochondrial energetics and walking performance
Zane, A. C., Reiter, D. A., Shardell, M., Cameron, D., Simonsick, E. M., Fishbein, K. W., Studenski, S. A., Spencer, R. G., & Ferrucci, L. (2017) · Aging Cell · doi:10.1111/acel.12568 · Cited by 134 · see citing works
Sako, T., Hamaoka, T., Higuchi, H., Kurosawa, Y., & Katsumura, T. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.1.338 · Cited by 131 · see citing works
Thomson, D. M., & Gordon, S. E. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00811.2004 · Cited by 131 · see citing works
Use of creatine in the elderly and evidence for effects on cognitive function in young and old
Rawson, E. S., & Venezia, A. C. (2011) · Amino Acids · doi:10.1007/s00726-011-0855-9 · Cited by 127 · see citing works
Franssen, F. M. E., Wouters, E. F. �., & Schols, A. M. W. J. (2002) · Clinical Nutrition · doi:10.1054/clnu.2001.0485 · Cited by 125 · see citing works
Ageing, muscle properties and maximal O2 uptake rate in humans
Conley, K. E., Esselman, P. C., Jubrias, S. A., Cress, M. E., Inglin, B., Mogadam, C., & Schoene, R. B. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00211.x · Cited by 124 · see citing works
Ageing: Effects on oxidative function of skeletal muscle in vivo
Taylor, D. J., Kemp, G. J., Thompson, C. H., & Radda, G. K. (1997) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006802602497 · Cited by 118 · see citing works
Conley, K. E., Kemper, W. F., & Crowther, G. J. (2001) · Journal of Experimental Biology · doi:10.1242/jeb.204.18.3189 · Cited by 117 · see citing works
DeLorey, D. S., Kowalchuk, J. M., & Paterson, D. H. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01179.2003 · Cited by 116 · see citing works
High-abundance mRNAs in human muscle: comparison between young and old
Welle, S. L., Bhatt, K. S., & Thornton, C. A. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.89.1.297 · Cited by 112 · see citing works
Lanza, I. R., Larsen, R. G., & Kent‐Braun, J. A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.138362 · Cited by 111 · see citing works
Skeletal Muscle Mitochondrial Function and Fatigability in Older Adults
Santanasto, A. J., Glynn, N. W., Jubrias, S. A., Conley, K. E., Boudreau, R. M., Amati, F., Mackey, D. C., Simonsick, E. M., Strotmeyer, E. S., Coen, P. M., et al. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu134 · Cited by 108 · see citing works
Puente‐Maestu, L., Tena, T., Trascasa, C., Pérez-Parra, J., Mayoral, R. G., García, J. M., & Stringer, W. W. (2003) · European Journal of Applied Physiology · doi:10.1007/s00421-002-0743-9 · Cited by 110 · see citing works
Oxygen uptake kinetics for moderate exercise are speeded in older humans by prior heavy exercise
Scheuermann, B. W., Bell, C., Paterson, D. H., Barstow, T. J., & Kowalchuk, J. M. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00186.2001 · Cited by 109 · see citing works
Determinants of team-sport performance: implications for altitude training by team-sport athletes
Bishop, D. J., & Girard, O. (2013) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-092950 · Cited by 114 · see citing works
Kemp, G. J., Roberts, N., Bimson, W. E., Bakran, A., Harris, P. L., Gilling-Smith, G. L., Brennan, J. M., Rankin, A., & Frostick, S. P. (2001) · Journal of Vascular Surgery · doi:10.1067/mva.2001.117152 · Cited by 108 · see citing works
Creatine supplementation and aging musculoskeletal health
Candow, D. G., Chilibeck, P. D., & Forbes, S. C. (2014) · Endocrine · doi:10.1007/s12020-013-0070-4 · Cited by 107 · see citing works
Abnormal Skeletal Muscle Oxidative Capacity After Lung Transplantation by 31P-MRS
Evans, A. B., Al-Himyary, A., Hrovat, M. I., Pappagianopoulos, P. P., Wain, J. C., Ginns, L. C., & Systrom, D. M. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.155.2.9032203 · Cited by 106 · see citing works
Helix-loop-helix transcription factors in electrically active and inactive skeletal muscles
Carlsen, H., & Gundersen, K. (2000) · Muscle & Nerve · doi:10.1002/1097-4598(200009)23:9 · Cited by 32 · see citing works
Lanza, I. R., Bhagra, S., Nair, K. S., & Port, J. D. (2011) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.22733 · Cited by 103 · see citing works
Oral creatine supplementation and skeletal muscle metabolism in physical exercise
Mesa, J. L. M., Ruiz, J. R., Gonz??lez-Gross, M. M., Guti??rrez S??inz, ?., & Castillo Garz??n, M. J. (2002) · Sports Medicine · doi:10.2165/00007256-200232140-00003 · Cited by 103 · see citing works
Poole, D. C., & Jones, A. (2012) · Comprehensive physiology · doi:10.1002/j.2040-4603.2012.tb00419.x · Cited by 104 · see citing works
Mitochondria’s Role in Skin Ageing
Stout, R., & Birch‐Machin, M. A. (2019) · Biology · doi:10.3390/biology8020029 · Cited by 100 · see citing works
Takahashi, H., Inaki, M., Fujimoto, K., Katsuta, S., Anno, I., N�tsu, M., & Itai, Y. (1995) · European Journal of Applied Physiology · doi:10.1007/bf00635872 · Cited by 97 · see citing works
Roussel, M., Bendahan, D., Mattei, J. P., Fur, Y. L., & Cozzone, P. J. (2000) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(99)00111-5 · Cited by 96 · see citing works
Skeletal Muscle Damage and Recovery
Kasper, C. E., Talbot, L. A., & Gaines, J. M. (2002) · AACN Clinical Issues: Advanced Practice in Acute and Critical Care · doi:10.1097/00044067-200205000-00009 · Cited by 96 · see citing works
Choi, S., Reiter, D. A., Shardell, M., Simonsick, E. M., Studenski, S., Spencer, R. G., Fishbein, K. W., & Ferrucci, L. (2016) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glw059 · Cited by 92 · see citing works
Forbes, S. C., Paganini, A. T., Slade, J. M., Towse, T. F., & Meyer, R. A. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90704.2008 · Cited by 95 · see citing works
Skeletal muscle energetics with PNMR: personal views and historic perspectives
Chance, B., Im, J., Nioka, S., & Kushmerick, M. J. (2006) · NMR in Biomedicine · doi:10.1002/nbm.1109 · Cited by 94 · see citing works
Hamaoka, T., & McCully, K. (2019) · Journal of Physiological Sciences · doi:10.1007/s12576-019-00697-2 · Cited by 86 · see citing works
Self-citationHaseler, L. J., Lin, A., & Richardson, R. S. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01321.2003 · Cited by 92 · see citing works
Mitochondrial DNA alterations and reduced mitochondrial function in aging
Hebert, S. L., Lanza, I. R., & Nair, K. S. (2010) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2010.03.007 · Cited by 90 · see citing works
Dietary quercetin supplementation is not ergogenic in untrained men
Cureton, K. J., Tomporowski, P. D., Singhal, A., Pasley, J. D., Bigelman, K. A., Lambourne, K., Trilk, J. L., McCully, K. K., Arnaud, M. J., & Zhao, Q. C. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00234.2009 · Cited by 88 · see citing works
Self-citationDeLorey, D. S., Kowalchuk, J. M., & Paterson, D. H. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00607.2004 · Cited by 88 · see citing works
Faster oxygen uptake kinetics during recovery is related to better repeated sprinting ability
Dupont, G., McCall, A., Prieur, F., Millet, G. P., & Berthoin, S. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1494-7 · Cited by 87 · see citing works
Larsen, R. G., Callahan, D. M., Foulis, S. A., & Kent‐Braun, J. A. (2012) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h11-135 · Cited by 87 · see citing works
Tian, Q., Mitchell, B. A., Zampino, M., Fishbein, K. W., Spencer, R. G., & Ferrucci, L. (2022) · Aging Cell · doi:10.1111/acel.13552 · Cited by 78 · see citing works
Regulation of skeletal muscle mitochondrial function: genes to proteins
Lanza, I. R., & Sreekumaran Nair, K. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02124.x · Cited by 83 · see citing works
Skeletal Muscle Metabolism in Endurance Athletes with Near-Infrared Spectroscopy
Brizendine, J. T., RYAN, T. E., Larson, R. D., & McCully, K. K. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31827e0eb6 · Cited by 83 · see citing works
Self-citationMitochondrial metabolic function assessed in vivo and in vitro
Lanza, I. R., & Nair, K. S. (2010) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32833cc93d · Cited by 82 · see citing works
Rasmussen, U. F., Krustrup, P., Kjær, M., & Rasmussen, H. (2003) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-003-1022-2 · Cited by 82 · see citing works
RYAN, T. E., Brizendine, J. T., & McCully, K. K. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01043.2012 · Cited by 77 · see citing works
Self-citationGram, M., Vigelsø, A., Yokota, T., HANSEN, C. N., Helge, J. W., Hey‐Mogensen, M., & Dela, F. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.08.013 · Cited by 77 · see citing works
Bioenergetic basis for the increased fatigability with ageing
Sundberg, C. W., Prost, R. W., Fitts, R. H., & Hunter, S. K. (2019) · The Journal of Physiology · doi:10.1113/jp277803 · Cited by 76 · see citing works
Age-Related Alterations in Muscular Endurance
Bemben, M. G. (1998) · Sports Medicine · doi:10.2165/00007256-199825040-00004 · Cited by 76 · see citing works
Kestenbaum, B. R., Gamboa, J. L., Liu, S. Z., Ali, A. S., Shankland, E. G., Jue, T., Giulivi, C., Smith, L., Himmelfarb, J., de Boer, I. H., et al. (2020) · JCI Insight · doi:10.1172/jci.insight.133289 · Cited by 73 · see citing works
Layec, G., Bringard, A., Fur, Y. L., Vilmen, C., Micallef, J., Perrey, S., Cozzone, P. J., & Bendahan, D. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22085 · Cited by 75 · see citing works
Near-infrared assessments of skeletal muscle oxidative capacity in persons with spinal cord injury
Erickson, M. L., RYAN, T. E., Young, H., & McCully, K. K. (2013) · European Journal of Applied Physiology · doi:10.1007/s00421-013-2657-0 · Cited by 75 · see citing works
Self-citationMotobe, M., Murase, N., Osada, T., Homma, T., Ueda, C., Nagasawa, T., Kitahara, A., Ichimura, S., Kurosawa, Y., Katsumura, T., et al. (2004) · Dynamic Medicine · doi:10.1186/1476-5918-3-2 · Cited by 73 · see citing works
Welle, S. L., Brooks, A. I., & Thornton, C. A. (2001) · Physiological Genomics · doi:10.1152/physiolgenomics.2001.5.2.67 · Cited by 72 · see citing works
Beever, A. T., Tripp, T. R., Zhang, J., & MacInnis, M. J. (2020) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00017.2020 · Cited by 73 · see citing works
Skeletal muscle metabolism in individuals with spinal cord injury
McCully, K. K., Mulcahy, T. K., RYAN, T. E., & Zhao, Q. C. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00094.2011 · Cited by 70 · see citing works
Self-citationRasmussen, U. F., Rasmussen, H., Krustrup, P., Quistorff, B., Saltin, B., & Bangsbo, J. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.280.2.e301 · Cited by 69 · see citing works
Impact of aging on mitochondrial function in cardiac and skeletal muscle
Hepple, R. T. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.017 · Cited by 68 · see citing works
- Authors
- McCully, K. K., Fielding, R. A., Evans, W. J., Leigh, J. S., & Posner, J. D.
- Affiliations
- Department of Medicine, Medical College of Pennsylvania, Philadelphia 19129.
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1993-08-01
- Volume
- 75
- Issue
- 2
- Pages
- 813-819
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2273652180
- Cited by
- 288
- References
- 28
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 7 · 2023: 6 · 2022: 10 · 2021: 4 · 2020: 10 · 2019: 11 · 2018: 9 · 2017: 7 · 2016: 10 · 2015: 13 · 2014: 15 · 2013: 16 · 2012: 13
- FWCI
- 11.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5p01ag003934-14)
- National Institute on Aging (AG 03934)
- Topics
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- muscle metabolism, aging, oxidative metabolism, citrate synthase activity, triceps surae, lateral gastrocnemius, inorganic phosphate, muscle fiber type, peak oxygen uptake, plantar flexion, magnetic resonance spectroscopy, human skeletal muscle
- MeSH terms
- Adenosine Triphosphate, Adult, Aged, Aging, Citrate (si)-Synthase, Exercise Test, Female, Humans, Leg, Male, Middle Aged, Muscles, Magnetic Resonance Spectroscopy, Oxidation-Reduction, Oxygen Consumption, Phosphates, Phosphocreatine, In Vitro Techniques
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