The Aging Athlete: Paradigm of Healthy Aging

Abstract

The Exercise Boom of the 1970’s resulted in the adoption of habitual exercise in a significant portion of the population. Many of these individuals are defying the cultural norms by remaining physically active and competing at a high level in their later years. The juxtaposition between masters athletes and non-exercisers demonstrate the importance of remaining physically active throughout the lifespan on physiological systems related to healthspan (years of healthy living). This includes ~50% improved maximal aerobic capacity (VO₂max) and enhanced skeletal muscle health (size, function, as well as metabolic and communicative properties) compared to non-exercisers at a similar age. By taking a reductionist approach to VO₂max and skeletal muscle health, we can gain insight into how aging and habitual exercise affects the aging process. Collectively, this review provides a physiological basis for the elite performances seen in masters athletes, as well as the health implications of lifelong exercise with a focus on VO₂max, skeletal muscle metabolic fitness, whole muscle size and function, single muscle fiber physiology, and communicative properties of skeletal muscle. This review has significant public health implications due to the potent health benefits of habitual exercise across the lifespan.

Key words

aging - maximal oxygen consumption - metabolic health - lifelong exercise - single muscle fiber - sarcopenia

Publication History

Received: 06 January 2022

Accepted: 01 February 2022

Accepted Manuscript online:
04 February 2022

Article published online:
08 April 2022

• References

• 1 Dionigi R. Competitive sport as leisure in later life: negotiations, discourse, and aging. Leisure Sciences 2006; 28: 181-196
• 2 Kundert AML, Di Gangi S, Nikolaidis PT. et al. Jumping and throwing performance in the World Masters’ Athletic Championships 1975-2016. Res Sports Med 2019; 27: 374-411
• 3 Lazarus NR, Harridge SDR. Declining performance of master athletes: silhouettes of the trajectory of healthy human ageing?. J Physiol 2017; 595: 2941-2948
• 4 Seals DR, Justice JN, LaRocca TJ. Physiological geroscience: targeting function to increase healthspan and achieve optimal longevity. J Physiol 2016; 594: 2001-2024
• 5 Vandam LD, Fox JA. Adolf Fick (1829-1901), physiologist: a heritage for anesthesiology and critical care medicine. Anesthesiology 1998; 88: 514-518
• 6 Joyner MJ, Coyle EF. Endurance exercise performance: the physiology of champions. J Physiol 2008; 586: 35-44
• 7 Harber MP, Kaminsky LA, Arena R. et al. Impact of cardiorespiratory fitness on all-cause and disease-specific mortality: advances since 2009. Prog Cardiovasc Dis 2017; 60: 11-20
• 8 Myers J, Prakash M, Froelicher V. et al. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med 2002; 346: 793-801
• 9 Kodama S, Saito K, Tanaka S. et al. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA 2009; 301: 2024-2035
• 10 Ross R, Blair SN, Arena R. et al. Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association. Circulation 2016; 134: e653-e699
• 11 Robinson S. Experimental studies of physical fitness in relation to age. Arbeitsphysiologie 1938; 10: 251-323
• 12 Kaminsky LA, Arena R, Myers J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing: data from the fitness registry and the importance of exercise national database. Mayo Clin Proc 2015; 90: 1515-1523
• 13 Loe H, Rognmo O, Saltin B. et al. Aerobic capacity reference data in 3816 healthy men and women 20-90 years. PLoS One 2013; 8: e64319
• 14 Bouchard C, An P, Rice T. et al. Familial aggregation of VO₂max response to exercise training: results from the HERITAGE Family Study. J Appl Physiol (1985) 1999; 87: 1003-1008
• 15 Kokko S, Liveng A, Torp S. 20 years of health promotion research in the Nordic countries: Health, wellbeing and physical activity. Scand J Public Healt 2018; 46: 3-6
• 16 Dill DB, Robinson S, Ross JC. A longitudinal study of 16 champion runners. J Sports Med Phys Fitness 1967; 7: 4-27
• 17 Gries KJ, Raue U, Perkins RK. et al. Cardiovascular and skeletal muscle health with lifelong exercise. J Appl Physiol (1985) 2018; 125: 1636-1645
• 18 Heath GW, Hagberg JM, Ehsani AA. et al. A physiological comparison of young and older endurance athletes. J Appl Physiol Respir Environ Exerc Physiol 1981; 51: 634-640
• 19 Wiswell RA, Hawkins SA, Victoria SV. et al. Relationship between physiological loss, performance decrement, and age in master athletes. J Gerontol A Biol Sci Med Sci 2001; 56: 618-626
• 20 Tanaka H, Desouza CA, Jones PP. et al. Greater rate of decline in maximal aerobic capacity with age in physically active vs. sedentary healthy women. J Appl Physiol (1985) 1997; 83: 1947-1953
• 21 Pimentel AE, Gentile CL, Tanaka H. et al. Greater rate of decline in maximal aerobic capacity with age in endurance-trained than in sedentary men. J Appl Physiol (1985) 2003; 94: 2406-2413
• 22 Hawkins SA, Marcell TJ, Victoria JS. A longitudinal assessment of change in VO₂max and maximal heart rate in master athletes. Med Sci Sports Exerc 2001; 33: 1744-1750
• 23 Fitzgerald MD, Tanaka H, Tran ZV. et al. Age-related declines in maximal aerobic capacity in regularly exercising vs. sedentary women: a meta-analysis. J Appl Physiol (1985) 1997; 83: 160-165
• 24 Maud PJ, Pollock ML, Foster C. et al. Fifty years of training and competition in the marathon: Wally Hayward, age 70 – a physiological profile. S Afr Med J 1981; 59: 153-157
• 25 Faria I, Frankel M. Anthropometric and physiologic profile of a cyclist – age 70. Med Sci Sports 1977; 9: 118-121
• 26 Billat V, Dhonneur G, Mille-Hamard L. et al. Case Studies in Physiology: Maximal oxygen consumption and performance in a centenarian cyclist. J Appl Physiol (1985) 2017; 122: 430-434
• 27 Hill AV, Lupton H. Muscular exercise, lactic acid, and the supply and utilization of oxygen. Q J Med 1923; 16: 135-171
• 28 Andersen P, Saltin B. Maximal perfusion of skeletal muscle in man. J Physiol 1985; 366: 233-249
• 29 Mitchell JH, Blomqvist G. Maximal oxygen uptake. N Engl J Med 1971; 284: 1018-1022
• 30 Proctor DN, Beck KC, Shen PH. et al. Influence of age and gender on cardiac output-VO₂ relationships during submaximal cycle ergometry. J Appl Physiol (1985) 1998; 84: 599-605
• 31 Ogawa T, Spina RJ, Martin WH. et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 1992; 86: 494-503
• 32 Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol 2001; 37: 153-156
• 33 Carrick-Ranson G, Hastings JL, Bhella PS. et al. The effect of lifelong exercise dose on cardiovascular function during exercise. J Appl Physiol (1985) 2014; 116: 736-745
• 34 Coggan AR, Abduljalil AM, Swanson SC. et al. Muscle metabolism during exercise in young and older untrained and endurance-trained men. J Appl Physiol (1985) 1993; 75: 2125-2133
• 35 Rogers MA, Hagberg JM, Martin WH. et al. Decline in VO₂max with aging in master athletes and sedentary men. J Appl Physiol (1985) 1990; 68: 2195-2199
• 36 Everman S, Farris JW, Bay RC. et al. Elite distance runners: a 45-year follow-up. Med Sci Sports Exerc 2018; 50: 73-78
• 37 Trappe S, Hayes E, Galpin A. et al. New records in aerobic power among octogenarian lifelong endurance athletes. J Appl Physiol (1985) 2013; 114: 3-10
• 38 Fujimoto N, Hastings JL, Bhella PS. et al. Effect of ageing on left ventricular compliance and distensibility in healthy sedentary humans. J Physiol 2012; 590: 1871-1880
• 39 Arbab-Zadeh A, Dijk E, Prasad A. et al. Effect of aging and physical activity on left ventricular compliance. Circulation 2004; 110: 1799-1805
• 40 Song Y, Yao Q, Zhu J. et al. Age-related variation in the interstitial tissues of the cardiac conduction system; and autopsy study of 230 Han Chinese. Forensic Sci Int 1999; 104: 133-142
• 41 Bhella PS, Hastings JL, Fujimoto N. et al. Impact of lifelong exercise “dose” on left ventricular compliance and distensibility. J Am Coll Cardiol 2014; 64: 1257-1266
• 42 Wooten SV, Moestl S, Chilibeck P. et al. Age- and sex-differences in cardiac characteristics determined by echocardiography in masters athletes. Front Physiol 2020; 11: 630148
• 43 Carrick-Ranson G, Sloane NM, Howden EJ. et al. The effect of lifelong endurance exercise on cardiovascular structure and exercise function in women. J Physiol 2020; 598: 2589-2605
• 44 Hagberg JM, Allen WK, Seals DR. et al. A hemodynamic comparison of young and older endurance athletes during exercise. J Appl Physiol (1985) 1985; 58: 2041-2046
• 45 Carrick-Ranson G, Hastings JL, Bhella PS. et al. The effect of age-related differences in body size and composition on cardiovascular determinants of VO₂max. J Gerontol A Biol Sci Med Sci 2013; 68: 608-616
• 46 Murias JM, Kowalchuk JM, Paterson DH. Time course and mechanisms of adaptations in cardiorespiratory fitness with endurance training in older and young men. J Appl Physiol (1985) 2010; 108: 621-627
• 47 Coggan AR, Spina RJ, King DS. et al. Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J Gerontol 1992; 47: 71-76
• 48 Ryan NA, Zwetsloot KA, Westerkamp LM. et al. Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol (1985) 2006; 100: 178-185
• 49 Croley AN, Zwetsloot KA, Westerkamp LM. et al. Lower capillarization, VEGF protein, and VEGF mRNA response to acute exercise in the vastus lateralis muscle of aged vs. young women. J Appl Physiol (1985) 2005; 99: 1872-1879
• 50 Proctor DN, Sinning WE, Walro JM. et al. Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol (1985) 1995; 78: 2033-2038
• 51 Haas TL, Nwadozi E. Regulation of skeletal muscle capillary growth in exercise and disease. Appl Physiol Nutr Metab 2015; 40: 1221-1232
• 52 Simoneau JA, Kelley DE. Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol (1985) 1997; 83: 166-171
• 53 Marin P, Andersson B, Krotkiewski M. et al. Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 1994; 17: 382-386
• 54 Coggan AR, Spina RJ, Rogers MA. et al. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol (1985) 1990; 68: 1896-1901
• 55 Trappe SW, Costill DL, Fink WJ. et al. Skeletal muscle characterstics among distance runners: a 20-yr follow-up study. J Appl Physiol (1985) 1995; 78: 823-829
• 56 Pollock RD, O’Brien KA, Daniels LJ. et al. Properties of the vastus lateralis muscle in relation to age and physiological function in master cyclists aged 55-79 years. Aging Cell 2018; 17
• 57 Lanza IR, Short DK, Short KR. et al. Endurance exercise as a countermeasure for aging. Diabetes 2008; 57: 2933-2942
• 58 Murgia M, Toniolo L, Nagaraj N. et al. Single muscle fiber proteomics reveals fiber-type-specific features of human muscle aging. Cell Rep 2017; 19: 2396-2409
• 59 Short KR, Bigelow ML, Kahl J. et al. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci U S A 2005; 102: 5618-5623
• 60 Conley KE, Jubrias SA, Esselman PC. Oxidative capacity and ageing in human muscle. J Physiol 2000; 526: 203-210
• 61 Lanza IR, Nair KS. Muscle mitochondrial changes with aging and exercise. Am J Clin Nutr 2009; 89: 467S-471S
• 62 Dubé JJ, Broskey NT, Despines AA. et al. Muscle characteristics and substrate energetics in lifelong endurance athletes. Med Sci Sports Exerc 2016; 48: 472-480
• 63 Toth MJ, Gardner AW, Ades PA. et al. Contribution of body composition and physical activity to age-related decline in peak VO₂ in men and women. J Appl Physiol (1985) 1994; 77: 647-652
• 64 Fleg JL, Lakatta EG. Role of muscle loss in the age-associated reduction in VO₂max. J Appl Physiol (1985) 1988; 65: 1147-1151
• 65 Chambers TL, Burnett TR, Raue U. et al. Skeletal muscle size, function, and adiposity with lifelong aerobic exercise. J Appl Physiol (1985) 2020; 128: 368-378
• 66 Tzankoff SP, Norris AH. Effect of muscle mass decrease on age-related BMR changes. J Appl Physiol Respir Environ Exerc Physiol 1977; 43: 1001-1006
• 67 Reed RL, Pearlmutter L, Yochum K. et al. The relationship between muscle mass and muscle strength in the elderly. J Am Geriatr Soc 1991; 39: 555-561
• 68 Pisciottano MV, Pinto SS, Szejnfeld VL. et al. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging 2014; 18: 554-558
• 69 Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr 2006; 84: 475-482
• 70 Cosqueric G, Sebag A, Ducolombier C. et al. Sarcopenia is predictive of nosocomial infection in care of the elderly. Br J Nutr 2006; 96: 895-901
• 71 de Hoogt PA, Reisinger KW, Tegels JJW. et al. Functional Compromise Cohort Study (FCCS): sarcopenia is a strong predictor of mortality in the intensive care unit. World J Surg 2018; 42: 1733-1741
• 72 Toth MJ, Callahan DM, Miller MS. et al. Skeletal muscle fiber size and fiber type distribution in human cancer: Effects of weight loss and relationship to physical function. Clin Nutr 2016; 35: 1359-1365
• 73 Callahan DM, Toth MJ. Skeletal muscle protein metabolism in human heart failure. Curr Opin Clin Nutr Metab Care 2013; 16: 66-71
• 74 Kunz HE, Port JD, Kaufman KR. et al. Skeletal muscle mitochondrial dysfunction and muscle and whole-body functional deficits in cancer patients with weight loss. J Appl Physiol (1985) 2021;
• 75 Hughes VA, Frontera WR, Wood M. et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci 2001; 56: B209-B217
• 76 Silva AM, Shen W, Heo M. et al. Ethnicity-related skeletal muscle differences across the lifespan. Am J Hum Biol 2010; 22: 76-82
• 77 Goodpaster BH, Park SW, Harris TB. et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 2006; 61: 1059-1064
• 78 Janssen I, Heymsfield SB, Wang ZM. et al. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985) 2000; 89: 81-88
• 79 Lauretani F, Russo CR, Bandinelli S. et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985) 2003; 95: 1851-1860
• 80 Mitchell WK, Williams J, Atherton P. et al. Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 2012; 3: 260
• 81 Reimers CD, Harder T, Saxe H. Age-related muscle atrophy does not affect all muscles and can partly be compensated by physical activity: an ultrasound study. J Neurol Sci 1998; 159: 60-66
• 82 Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 1988; 84: 275-294
• 83 Roberts BM, Lavin KM, Many GM. et al. Human neuromuscular aging: sex differences revealed at the myocellular level. Exp Gerontol 2018; 106: 116-124
• 84 Trappe S, Gallagher P, Harber M. et al. Single muscle fibre contractile properties in young and old men and women. J Physiol 2003; 552: 47-58
• 85 Mitsiopoulos N, Baumgartner RN, Heymsfield SB. et al. Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol (1985) 1998; 85: 115-122
• 86 Wroblewski AP, Amati F, Smiley MA. et al. Chronic exercise preserves lean muscle mass in masters athletes. Phys Sportsmed 2011; 39: 172-178
• 87 Crane JD, Macneil LG, Tarnopolsky MA. Long-term aerobic exercise is associated with greater muscle strength throughout the life span. J Gerontol A Biol Sci Med Sci 2013; 68: 631-638
• 88 Tarpenning KM, Hamilton-Wessler M, Wiswell RA. et al. Endurance training delays age of decline in leg strength and muscle morphology. Med Sci Sports Exerc 2004; 36: 74-78
• 89 Trappe S, Godard M, Gallagher P. et al. Resistance training improves single muscle fiber contractile function in older women. Am J Physiol Cell Physiol 2001; 281: C398-C406
• 90 Bechshoft RL, Malmgaard-Clausen NM, Gliese B. et al. Improved skeletal muscle mass and strength after heavy strength training in very old individuals. Exp Gerontol 2017; 92: 96-105
• 91 Steele J, Raubold K, Kemmler W. et al. The effects of 6 months of progressive high effort resistance training methods upon strength, body composition, function, and wellbeing of elderly adults. Biomed Res Int 2017; 2017: 2541090
• 92 Snijders T, Leenders M, de Groot L. et al. Muscle mass and strength gains following 6months of resistance type exercise training are only partly preserved within one year with autonomous exercise continuation in older adults. Exp Gerontol 2019; 121: 71-78
• 93 Trappe S, Williamson D, Godard M. et al. Effect of resistance training on single muscle fiber contractile function in older men. J Appl Physiol (1985) 2000; 89: 143-152
• 94 Klitgaard H, Mantoni M, Schiaffino S. et al. Function, morphology and protein expression of ageing skeletal muscle: a cross-sectional study of elderly men with different training backgrounds. Acta Physiol Scand 1990; 140: 41-54
• 95 Gallagher D, Kuznia P, Heshka S. et al. Adipose tissue in muscle: a novel depot similar in size to visceral adipose tissue. Am J Clin Nutr 2005; 81: 903-910
• 96 Konopka AR, Wolff CA, Suer MK. et al. Relationship between intermuscular adipose tissue infiltration and myostatin before and after aerobic exercise training. Am J Physiol Regul Integr Comp Physiol 2018; 315: R461-R468
• 97 Coggan AR, Kohrt WM, Spina RJ. et al. Endurance training decreases plasma glucose turnover and oxidation during moderate-intensity exercise in men. J Appl Physiol (1985) 1990; 68: 990-996
• 98 Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol 1984; 56: 831-838
• 99 Jordy AB, Kiens B. Regulation of exercise-induced lipid metabolism in skeletal muscle. Exp Physiol 2014; 99: 1586-1592
• 100 Delmonico MJ, Harris TB, Visser M. et al. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 2009; 90: 1579-1585
• 101 Goodpaster BH, Chomentowski P, Ward BK. et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol (1985) 2008; 105: 1498-1503
• 102 Lynch NA, Metter EJ, Lindle RS. et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol (1985) 1999; 86: 188-194
• 103 Distefano G, Standley RA, Zhang X. et al. Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults. J Cachexia Sarcopenia Muscle 2018; 9: 279-294
• 104 Miljkovic-Gacic I, Gordon CL, Goodpaster BH. et al. Adipose tissue infiltration in skeletal muscle: age patterns and association with diabetes among men of African ancestry. Am J Clin Nutr 2008; 87: 1590-1595
• 105 Marcus RL, Addison O, Kidde JP. et al. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging 2010; 14: 362-366
• 106 Hunter SK, Pereira HM, Keenan KG. The aging neuromuscular system and motor performance. J Appl Physiol (1985) 2016; 121: 982-995
• 107 Clark BC, Taylor JL. Age-related changes in motor cortical properties and voluntary activation of skeletal muscle. Curr Aging Sci 2011; 4: 192-199
• 108 Grosicki GJ, Standley RA, Murach KA. et al. Improved single muscle fiber quality in the oldest-old. J Appl Physiol (1985) 2016; 121: 878-884
• 109 Straight CR, Ades PA, Toth MJ. et al. Age-related reduction in single muscle fiber calcium sensitivity is associated with decreased muscle power in men and women. Exp Gerontol 2018; 102: 84-92
• 110 Sundberg CW, Hunter SK, Trappe SW. et al. Effects of elevated H(+) and Pi on the contractile mechanics of skeletal muscle fibres from young and old men: implications for muscle fatigue in humans. J Physiol 2018; 596: 3993-4015
• 111 Aagaard P, Magnusson PS, Larsson B. et al. Mechanical muscle function, morphology, and fiber type in lifelong trained elderly. Med Sci Sports Exerc 2007; 39: 1989-1996
• 112 Essén-Gustavsson B, Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 1986; 126: 107-114
• 113 Callahan DM, Bedrin NG, Subramanian M. et al. Age-related structural alterations in human skeletal muscle fibers and mitochondria are sex specific: relationship to single-fiber function. J Appl Physiol (1985) 2014; 116: 1582-1592
• 114 Aniansson A, Grimby G, Hedberg M. Compensatory muscle-fiber hypertrophy in elderly men. J Appl Physiol (1985) 1992; 73: 812-816
• 115 Frontera WR, Reid KF, Phillips EM. et al. Muscle fiber size and function in elderly humans: a longitudinal study. J Appl Physiol (1985) 2008; 105: 637-642
• 116 Power GA, Minozzo FC, Spendiff S. et al. Reduction in single muscle fiber rate of force development with aging is not attenuated in world class older masters athletes. Am J Physiol Cell Physiol 2016; 310: C318-C327
• 117 Widrick JJ, Trappe SW, Blaser CA. et al. Isometric force and maximal shortening velocity of single muscle fibers from elite master runners. Am J Physiol 1996; 271: C666-C675
• 118 Trappe S, Harber M, Creer A. et al. Single muscle fiber adaptations with marathon training. J Appl Physiol (1985) 2006; 101: 721-727
• 119 Harber M, Trappe S. Single muscle fiber contractile properties of young competitive distance runners. J Appl Physiol (1985) 2008; 105: 629-636
• 120 Sundstrup E, Jakobsen MD, Andersen JL. et al. Muscle function and postural balance in lifelong trained male footballers compared with sedentary elderly men and youngsters. Scand J Med Sci Sports 2010; 20: 90-97
• 121 Grosicki GJ, Gries KJ, Minchev K. et al. Single muscle fibre contractile characteristics with lifelong endurance exercise. J Physiol 2021; 599: 3549-3565
• 122 Zampieri S, Pietrangelo L, Loefler S. et al. Lifelong physical exercise delays age-associated skeletal muscle decline. J Gerontol A Biol Sci Med Sci 2015; 70: 163-173
• 123 Harber MP, Konopka AR, Douglass MD. et al. Aerobic exercise training improves whole muscle and single myofiber size and function in older women. Am J Physiol Regul Integr Comp Physiol 2009; 297: R1452-R1459
• 124 Luden N, Hayes E, Minchev K. et al. Skeletal muscle plasticity with marathon training in novice runners. Scand J Med Sci Sports 2012; 22: 662-670
• 125 Gries KJ, Minchev K, Raue U. et al. Single-muscle fiber contractile properties in lifelong aerobic exercising women. J Appl Physiol (1985) 2019; 127: 1710-1719
• 126 Trappe S, Luden N, Minchev K. et al. Skeletal muscle signature of a champion sprint runner. J Appl Physiol (1985) 2015; 118: 1460-1466
• 127 Klitgaard H, Zhou M, Schiaffino S. et al. Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol Scand 1990; 140: 55-62
• 128 Trappe S, Creer A, Slivka D. et al. Single muscle fiber function with concurrent exercise or nutrition countermeasures during 60 days of bed rest in women. J Appl Physiol (1985) 2007; 103: 1242-1250
• 129 Fitts RH, Trappe SW, Costill DL. et al. Prolonged space flight-induced alterations in the structure and function of human skeletal muscle fibres. J Physiol 2010; 588: 3567-3592
• 130 Malisoux L, Jamart C, Delplace K. et al. Effect of long-term muscle paralysis on human single fiber mechanics. J Appl Physiol (1985) 2006; 102: 340-349
• 131 Trappe S, Trappe T, Gallagher P. et al. Human single muscle fibre function with 84 day bed-rest and resistance exercise. J Physiol 2004; 557: 501-513
• 132 Trappe S, Costill D, Gallagher P. et al. Exercise in space: human skeletal muscle after 6 months aboard the International Space Station. J Appl Physiol (1985) 2009; 106: 1159-1168
• 133 Stuart CA, McCurry MP, Marino A. et al. Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness. J Clin Endocrinol Metab 2013; 98: 2027-2036
• 134 Gollnick PD, Armstrong RB, Saltin B. Effect of training on enzyme activity and fiber composition of human skeletal muscle. J Appl Physiol 1973; 34: 107-111
• 135 Bottinelli R, Pellegrino MA, Canepari M. et al. Specific contributions of various muscle fibre types to human muscle performance: an in vitro study. J Electromyogr Kinesiol 1999; 9: 87-95
• 136 Brocca L, McPhee JS, Longa E. et al. Structure and function of human muscle fibres and muscle proteome in physically active older men. J Physiol 2017; 595: 4823-4844
• 137 Larsson L, Li X, Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 1997; 272: C638-C649
• 138 Raue U, Slivka D, Minchev K. et al. Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J Appl Physiol (1985) 2009; 106: 1611-1617
• 139 Miller MS, Bedrin NG, Ades PA. et al. Molecular determinants of force production in human skeletal muscle fibers: effects of myosin isoform expression and cross-sectional area. Am J Physiol Cell Physiol 2015; 308: C473-C484
• 140 Harber MP, Konopka AR, Undem MK. et al. Aerobic exercise training induces skeletal muscle hypertrophy and age-dependent adaptations in myofiber function in young and older men. J Appl Physiol (1985) 2012; 113: 1495-1504
• 141 Slivka D, Raue U, Hollon C. et al. Single muscle fiber adaptations to resistance training in old men: evidence for limited skeletal muscle plasticity. Am J Physiol Regul Integr Comp Physiol 2008; 295: R273-R280
• 142 Widrick JJ, Trappe SW, Costill DL. et al. Force-velocity and force-power properties of single muscle fibers from elite master runners and sedentary men. Am J Physiol 1996; 271: C676-C683
• 143 Trappe S, Costill D, Thomas R. Effect of swim taper on whole muscle and single muscle fiber contractile properties. Med Sci Sports Exerc 2000; 32: 48-56
• 144 Rome LC, Funke RP, Alexander RM. et al. Why animals have different muscle fibre types. Nature 1988; 335: 824-827
• 145 Altenburg TM, Degens H, van Mechelen W. et al. Recruitment of single muscle fibers during submaximal cycling exercise. J Appl Physiol (1985) 2007; 103: 1752-1756
• 146 Fitts RH, Costill DL, Gardetto PR. Effect of swim exercise training on human muscle fiber function. J Appl Physiol (1985) 1989; doi:10.1002/mus.23388
• 147 Luden N, Hayes E, Galpin A. et al. Myocellular basis for tapering in competitive distance runners. J Appl Physiol (1985) 2010; 108: 1501-1509
• 148 Neary JP, Martin TP, Quinney HA. Effects of taper on endurance cycling capacity and single muscle fiber properties. Med Sci Sports Exerc 2003; 35: 1875-1881
• 149 Luden N, Minchev K, Hayes E. et al. Human vastus lateralis and soleus muscles display divergent cellular contractile properties. Am J Physiol Regul Integr Comp Physiol 2008; 295: R1593-R1598
• 150 Harridge SDR, Bottinelli R, Canepari M. et al. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflügers Arch 1996; 432: 913-920
• 151 Power GA, Dalton BH, Behm DG. et al. Motor unit survival in lifelong runners is muscle dependent. Med Sci Sports Exerc 2012; 44: 1235-1242
• 152 Raue U, Trappe TA, Estrem ST. et al. Transcriptome signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J Appl Physiol (1985) 2012; 112: 1625-1636
• 153 Rubenstein AB, Smith GR, Raue U. et al. Single-cell transcriptional profiles in human skeletal muscle. Sci Rep 2020; 10: 229
• 154 Begue G, Raue U, Jemiolo B. et al. DNA methylation assessment from human slow- and fast-twitch skeletal muscle fibers. J Appl Physiol (1985) 2017; 122: 952-967
• 155 Tumasian RA, Harish A, Kundu G. et al. Skeletal muscle transcriptome in healthy aging. Nat Commun 2021; 12: 2014
• 156 Steensberg A, van Hall G, Osada T. et al. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 2000; 529: 237-242
• 157 Whitham M, Parker BL, Friedrichsen M. et al. Extracellular vesicles provide a means for tissue crosstalk during exercise. Cell Metab 2018; 27: 237-251
• 158 Severinsen MCK, Pedersen BK. Muscle-organ crosstalk: the emerging roles of myokines. Endocr Rev 2020; 41: 594-609 2020; 41: 594-609
• 159 Lavin KM, Perkins RK, Jemiolo B. et al. Effects of aging and lifelong aerobic exercise on basal and exercise-induced inflammation. J Appl Physiol (1985) 2020; 128: 87-99
• 160 Perkins RK, Lavin KM, Raue U. et al. Effects of aging and lifelong aerobic exercise on expression of innate immune components in human skeletal muscle. J Appl Physiol (1985) 2020; 129: 1483-1492
• 161 Santos-Lozano A, Pareja-Galeano H, Sanchis-Gomar F. et al. Physical activity and alzheimer disease: a protective association. Mayo Clin Proc 2016; 91: 999-1020
• 162 Nilsson MI, Bourgeois JM, Nederveen JP. et al. Lifelong aerobic exercise protects against inflammaging and cancer. PLoS One 2019; 14: e0210863
• 163 Pedersen BK, Steensberg A, Schjerling P. Muscle-derived interleukin-6: possible biological effects. J Physiol 2001; 536: 329-337
• 164 Lavin KM, Perkins RK, Jemiolo B. et al. Effects of aging and lifelong aerobic exercise on basal and exercise-induced inflammation in women. J Appl Physiol (1985) 2020; 129: 1493-1504
• 165 Murach KA, Dimet-Wiley AL, Wen Y. et al. Late-life exercise mitigates skeletal muscle epigenetic aging. Aging Cell 2022; 21: e13527
• 166 Hickson RC. Interference of strength development by simultaneously training for strength and endurance. Eur J Appl Physiol Occup Physiol 1980; 45: 255-263
• 167 Murach KA, Minchev K, Grosicki GJ. et al. Myocellular responses to concurrent flywheel training during 70 days of bed rest. Med Sci Sports Exerc 2018; 50: 1950-1960
• 168 Sanford JA, Nogiec CD, Lindholm ME. et al. Molecular Transducers of Physical Activity Consortium (MoTrPAC): mapping the dynamic responses to exercise. Cell 2020; 181: 1464-1474
• 169 Trappe SW, Costill DL, Vukovich MD. et al. Aging among elite distance runners: a 22-yr longitudinal study. J Appl Physiol (1985) 1996; 80: 285-290
• 170 Pollock RD, Carter S, Velloso CP. et al. An investigation into the relationship between age and physiological function in highly active older adults. J Physiol 2015; 593: 657-680 discussion 680
• 171 Larsson L, Sjodin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22--65 years. Acta Physiol Scand 1978; 103: 31-39
• 172 Lexell J, Taylor CC. Variability in muscle-fiber areas in whole human quadriceps muscle – effects of increasing age. J Anat 1991; 174: 239-249
• 173 Poggi P, Marchetti C, Scelsi R. Automatic morphometric analysis of skeletal muscle fibers in the aging man. Anat Rec 1987; 217: 30-34
• 174 Verdijk LB, Koopman R, Schaart G. et al. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 2007; 292: E151-E157