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Lifelong Endurance Exercise as a Countermeasure Against Age-Related \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) Decline: Physiological Overview and Insights from Masters Athletes

Abstract

Maximum oxygen consumption (\(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\)) is not only an indicator of endurance performance, but also a strong predictor of cardiovascular disease and mortality. This physiological parameter is known to decrease with aging. In turn, physical exercise might attenuate the rate of aging-related decline in \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\), which in light of the global population aging is of major clinical relevance, especially at advanced ages. In this narrative review, we summarize the evidence available from masters athletes about the role of lifelong endurance exercise on aging-related \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) decline, with examples of the highest \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) values reported in the scientific literature for athletes across different ages (e.g., 35 ml·kg−1·min−1 in a centenarian cyclist). These data suggest that a linear decrease in \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) might be possible if physical exercise loads are kept consistently high through the entire life span, with \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) values remaining higher than those of the general population across all ages. We also summarize the main physiological changes that occur with inactive aging at different system levels—pulmonary and cardiovascular function, blood O2 carrying capacity, skeletal muscle capillary density and oxidative capacity—and negatively influence \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\), and review how lifelong exercise can attenuate or even prevent most—but apparently not all (e.g., maximum heart rate decline)—of them. In summary, although aging seems to be invariably associated with a progressive decline in \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\), maintaining high levels of physical exercise along the life span slows the multi-systemic deterioration that is commonly observed in inactive individuals, thereby attenuating age-related \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) decline.

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References

  1. 1.

    Joyner MJ, Coyle EF. Endurance exercise performance: the physiology of champions. J Physiol. 2008;586:35–44.

    CAS  PubMed  Google Scholar 

  2. 2.

    Ross R, Blair SN, Arena R, Church TS, Després JP, Franklin BA, 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:e653–99.

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Astrand I, Astrand P, Hallback I, Kilbom A. Reduction in maximal oxygen uptake with age. J Appl Physiol. 1973;35:649–54.

    CAS  PubMed  Google Scholar 

  4. 4.

    Fleg J, Morrell C, Bos A, Brant L, Talbot L, Wright J, et al. Accelerated longitudinal decline of aerobic capacity in healthy older adults. Circulation. 2005;112:674–82.

    PubMed  Google Scholar 

  5. 5.

    Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood J. Exercise capacity and mortality among men referred for exercise testing. N Engl J Med. 2002;346:793–801.

    PubMed  Google Scholar 

  6. 6.

    Mandsager K, Harb S, Cremer P, Phelan D, Nissen SE, Jaber W. Association of cardiorespiratory fitness with long-term mortality among adults undergoing exercise treadmill testing. JAMA Netw Open. 2018;1:e183605.

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Kodama S, Saito K, Tanaka S, Maki M, Yachi Y, Asumi M, et al. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events. J Am Med Assoc. 2009;301:2024–35.

    CAS  Google Scholar 

  8. 8.

    Lazarus NR, Izquierdo M, Higginson IJ, Harridge SDR. Exercise deiciency diseases of ageing: the primacy of exercise and muscle strengthening as irst line therapeutic agents to combat frailty. J Am Med Dir Assoc. 2018;19:741–3.

    PubMed  Google Scholar 

  9. 9.

    Clegg A, Young J, Iliffe S, Olde Rikkert M, Rockwood K. Frailty in elderly people. Lancet. 2013;381:752–62.

    Google Scholar 

  10. 10.

    Guthold R, Stevens GA, Riley LM, Bull FC. Worldwide trends in insuicient physical activity from 2001 to 2016: a pooled analysis of 358 population-based surveys with 1.9 million participants. Lancet Glob. Health. 2018;6:e1077–86.

    PubMed  Google Scholar 

  11. 11.

    Noakes T, Spedding M. Olympics: run for your life. Nature. 2012;487:295–6.

    CAS  PubMed  Google Scholar 

  12. 12.

    Harridge SDR, Lazarus NR. Physical activity, aging, and physiological function. Physiology. 2017;32:152–61.

    PubMed  Google Scholar 

  13. 13.

    Valenzuela P, Castillo-García A, Morales J, Izquierdo M, Serra-Rexach J, Santos-Lozano A, et al. Physical exercise in the oldest old. Compr Physiol. 2019;9:1281–304.

    PubMed  Google Scholar 

  14. 14.

    Tanaka H, Seals DR. Dynamic exercise performance in Masters athletes: insight into the effects of primary human aging on physiological functional capacity. J Appl Physiol. 2003;95:2152–62.

    PubMed  Google Scholar 

  15. 15.

    Lazarus NR, Harridge SDR. Declining performance of master athletes: silhouettes of the trajectory of healthy human ageing? J Physiol. 2017;595:2941–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Lepers R, Stapley PJ. Master athletes are extending the limits of human endurance. Front Physiol. 2016;7:1–8.

    Google Scholar 

  17. 17.

    Tanaka H, Seals DR. Endurance exercise performance in Masters athletes: age-associated changes and underlying physiological mechanisms. J Physiol. 2008;586:55–63.

    CAS  PubMed  Google Scholar 

  18. 18.

    Dehn MM, Bruce RA. Longitudinal variations in maximal oxygen intake with age and activity. J Appl Physiol. 1972;33:805–7.

    CAS  PubMed  Google Scholar 

  19. 19.

    Wilson TM, Tanaka H. Meta-analysis of the age-associated decline in maximal aerobic capacity in men: relation to training status. Am J Physiol Circ Physiol. 2000;278:H829–34.

    CAS  Google Scholar 

  20. 20.

    Fitzgerald MD, Tanaka H, Tran ZV, Seals DR. Age-related declines in maximal aerobic capacity in regularly exercising vs. sedentary women: a meta-analysis. J Appl Physiol. 1997;83:160–5.

    CAS  PubMed  Google Scholar 

  21. 21.

    Eskurza I, Donato AJ, Moreau KL, Seals DR, Tanaka H. Changes in maximal aerobic capacity with age in endurance-trained women: 7-yr follow-up. J Appl Physiol. 2002;92:2303–8.

    PubMed  Google Scholar 

  22. 22.

    Pimentel AE, Gentile CL, Tanaka H, Seals DR, Gates PE. Greater rate of decline in maximal aerobic capacity with age in endurance-trained than in sedentary men. J Appl Physiol. 2003;94:2406–13.

    PubMed  Google Scholar 

  23. 23.

    Trappe SW, Costill DL, Vukovich MD, Jones J, Melham T. Aging among elite distance runners: a 22-yr longitudinal study. J Appl Physiol. 1996;80:285–90.

    CAS  PubMed  Google Scholar 

  24. 24.

    Katzel LI, Sorkin JD, Fleg JL. A comparison of longitudinal changes in aerobic fitness in older endurance athletes and sedentary men. J Am Geriatr Soc. 2001;49:1657–64.

    CAS  PubMed  Google Scholar 

  25. 25.

    Kasch FW, Van Camp S, Nettl F, Wallace JP. Cardiovascular changes with age and exercise: a 28-year longitudinal study. Scand J Med Sci Sports. 1995;5:147–51.

    CAS  PubMed  Google Scholar 

  26. 26.

    Rogers MA, Hagberg JM, Martin WH, Ehsani AA, Holloszy JO. Decline in VO2max with aging in master athletes and sedentary men. J Appl Physiol. 1990;68:2195–9.

    CAS  PubMed  Google Scholar 

  27. 27.

    Gries KJ, Raue U, Perkins RK, Lavin KM, Overstreet BS, D’Acquisto LJ, et al. Cardiovascular and skeletal muscle health with lifelong exercise. J Appl Physiol. 2018;125:1636–45.

    PubMed  PubMed Central  Google Scholar 

  28. 28.

    Trappe S, Hayes E, Galpin A, Jemiolo B, Fink W, Trappe T, et al. New records in aerobic power among octogenarian lifelong endurance athletes. J Appl Physiol. 2013;114:3–10.

    PubMed  Google Scholar 

  29. 29.

    Arbab-Zadeh A, Dijk E, Prasad A, Fu Q, Torres P, Zhang R, et al. Effect of aging and physical activity on left ventricular compliance. Circulation. 2004;110:1799–805.

    PubMed  Google Scholar 

  30. 30.

    Prasad A, Popovic ZB, Arbab-Zadeh A, Fu Q, Palmer D, Dijk E, et al. The effects of aging and physical activity on doppler measures of diastolic function. Am J Cardiol. 2007;99:1629–36.

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Bhella PS, Hastings JL, Fujimoto N, Shibata S, Carrick-Ranson G, Palmer MD, et al. Impact of lifelong exercise “dose” on left ventricular compliance and distensibility. J Am Coll Cardiol. 2014;64:1257–66.

    PubMed  PubMed Central  Google Scholar 

  32. 32.

    Carrick-Ranson G, Hastings JL, Bhella PS, Fujimoto N, Shibata S, Palmer MD, et al. The effect of lifelong exercise dose on cardiovascular function during exercise. J Appl Physiol. 2014;116:736–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Hieda M, Howden E, Sarma S, Tarumi T, Palmer D, Lawley J, et al. Impact of lifelong exercise training “dose” on ventricular-arterial coupling. Circulation. 2018;138:2638–47.

    PubMed  Google Scholar 

  34. 34.

    Mckendry J, Breen L, Shad BJ, Greig CA. Muscle morphology and performance in master athletes: a systematic review and meta-analyses. Ageing Res Rev. 2018;45:62–82.

    PubMed  Google Scholar 

  35. 35.

    Montero D, Díaz-Cañestro C. Maximal cardiac output in athletes: Influence of age. Eur J Prev Cardiol. 2015;22:1588–600.

    PubMed  Google Scholar 

  36. 36.

    Bacon AP, Carter RE, Ogle EA, Joyner MJ. VO2max trainability and high Intensity interval training in humans: a meta-analysis. PLoS ONE. 2013;8:e73182.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    MacInnis MJ, Gibala MJ. Physiological adaptations to interval training and the role of exercise intensity. J Physiol. 2017;595:2915–30.

    CAS  PubMed  Google Scholar 

  38. 38.

    ACSM. ACSM’s guidelines for exercise testing and prescription. 10th ed. Philadelphia: Lippincott Williams & Wilkins; 2010.

    Google Scholar 

  39. 39.

    Burtscher M, Nachbauer W, Wilber R. The upper limit of aerobic power in humans. Eur J Appl Physiol. 2011;111:2625–8.

    PubMed  Google Scholar 

  40. 40.

    Ronnestad BR, Hansen J, Stenlokken L, Joyner M, Lundby C. Case studies in physiology: temporal changes in determinants of aerobic performance in individual going from alpine skier to world champion time trial cyclist. J Appl Physiol. 2019;127:306–11.

    PubMed  Google Scholar 

  41. 41.

    Everman S, Farris JW, Bay RC, Daniels JT. Elite distance runners: a 45-year follow-up. Med Sci Sports Exerc. 2018;50:73–8.

    PubMed  Google Scholar 

  42. 42.

    Heath GW, Hagberg JM, Ehsani AA, Holloszy JO. A physiological comparison of young and older endurance athletes. J Appl Physiol. 1981;51:634–40.

    CAS  PubMed  Google Scholar 

  43. 43.

    Lepers R, Bontemps B, Louis J. Physiological profile of a 59-year-old male world record holder marathoner. Med Sci Sports Exerc. 2019. https://doi.org/10.1249/MSS.0000000000002181.

    Article  Google Scholar 

  44. 44.

    Maud PJ, Pollock ML, Foster C, Anholm JD, Guten G, Al-Nouri M, et al. Fifty years of training and competition in the marathon: Wally Hayward, age 70—a physiological profile. S Afr Med J. 1981;59:153–7.

    CAS  PubMed  Google Scholar 

  45. 45.

    Karlsen T, Leinan IM, Bækkerud FH, Lundgren KM, Tari A, Steinshamn SL, et al. How to be 80 year old and have a VO2max of a 35 year old. Case Rep Med. 2015;2015:1–6.

    Google Scholar 

  46. 46.

    Cattagni T, Gremeaux V, Lepers R. The physiological characteristics of an 83-year-old champion female master runner. Int J Sports Physiol Perform. 2019. https://doi.org/10.1123/ijspp.2018-0879.

    Article  PubMed  Google Scholar 

  47. 47.

    Billat V, Dhonneur G, Mille-Hamard L, Le Moyec L, Momken I, Launay T, et al. Maximal oxygen consumption and performance in a centenarian cyclist. J Appl Physiol. 2017;122:430–4.

    PubMed  Google Scholar 

  48. 48.

    Lepers R, Cattagni T. Age-related decline in endurance running performance—an example of a multiple World records holder. Appl Physiol Nutr Metab. 2018;43:98–100.

    PubMed  Google Scholar 

  49. 49.

    Pollock RD, Carter S, Velloso CP, Duggal NA, Lord JM, Lazarus NR, et al. An investigation into the relationship between age and physiological function in highly active older adults. J Physiol. 2015;593:657–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Kaminsky LA, Imboden MT, Arena R, Myers J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing using cycle ergometry: Data from the Fitness Registry and the importance of Exercise National Database (FRIEND) Registry. Mayo Clin Proc. 2017;92:228–33.

    PubMed  Google Scholar 

  51. 51.

    Williams CJ, Williams MG, Eynon N, Ashton KJ, Little JP, Wisloff U, et al. Genes to predict VO2max trainability: a systematic review. BMC Genomics. 2017;18:831.

    PubMed  PubMed Central  Google Scholar 

  52. 52.

    Bouchard C. DNA sequence variations contribute to variability in fitness and trainability. Med Sci Sports Exerc. 2019;51:1781–5.

    CAS  PubMed  Google Scholar 

  53. 53.

    Joyner MJ. Limits to the evidence that DNA sequence diferences contribute to the variability in fitness and trainability. Med Sci Sports Exerc. 2019;51:1786–9.

    PubMed  Google Scholar 

  54. 54.

    Wagner PD. Determinants of maximal oxygen transport and utilization. Annu Rev Physiol. 1996;58:21–50.

    CAS  PubMed  Google Scholar 

  55. 55.

    Aalami O, Fang T, Song H, Nacamuli R. Physiological features of aging persons. Arch Surg. 2003;138:1068–76.

    PubMed  Google Scholar 

  56. 56.

    Lowery EM, Brubaker AL, Kuhlmann E, Kovacs EJ. The aging lung. Clin Interv Aging. 2013;8:1489–96.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Knudson R, Lebowitz M, Holberg C, Burrows B. Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis. 1983;127:725–34.

    CAS  PubMed  Google Scholar 

  58. 58.

    Sorbini C, Grassi V, Solinas E, Muisan G. Arterial oxygen tension in relation to age in healthy subjects. Respiration. 1968;25:3–13.

    CAS  PubMed  Google Scholar 

  59. 59.

    Thurlbeck W, Angus G. Growth and aging of the normal human lung. Chest. 1975;67:3S–7S.

    CAS  PubMed  Google Scholar 

  60. 60.

    Bassett D, Howley E. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32:70–84.

    PubMed  Google Scholar 

  61. 61.

    Hassel E, Stensvold D, Halvorsen T, Wisløff U, Langhammer A, Steinshamn S. Association between pulmonary function and peak oxygen uptake in elderly: the Generation 100 study. Respir Res. 2015;16:1–8.

    Google Scholar 

  62. 62.

    Rasch-Halvorsen Ø, Steinshamn S, Hassel E, Brumpton BM, Langhammer A. The association between dynamic lung function and peak oxygen uptake in a healthy general population. The HUNT Study. BMC Pulm Med. 2019;19:OA3190.

    Google Scholar 

  63. 63.

    Babb TG. Ventilatory response to exercise in subjects breathing CO2 or HeO2. J Appl Physiol. 1997;82:746–54.

    CAS  PubMed  Google Scholar 

  64. 64.

    Babb TG, DeLorey DS, Wyrick BL. Ventilatory response to exercise in aged runners breathing He-O2 or inspired CO2. J Appl Physiol. 2003;94:685–93.

    CAS  PubMed  Google Scholar 

  65. 65.

    Babb TG. Ventilation and respiratory mechanics during exercise in younger subjects breathing CO2 or HeO2. Respir Physiol. 1997;109:15–28.

    CAS  PubMed  Google Scholar 

  66. 66.

    Roman MA, Rossiter HB, Casaburi R. Exercise, ageing and the lung. Eur Respir J. 2016;48:1471–86.

    PubMed  Google Scholar 

  67. 67.

    Bathgate KE, Bagley JR, Jo E, Talmadge RJ, Tobias IS, Brown LE, et al. Muscle health and performance in monozygotic twins with 30 years of discordant exercise habits. Eur J Appl Physiol. 2018;118:2097–110.

    CAS  PubMed  Google Scholar 

  68. 68.

    Johnson BD, Reddan WG, Seow KC, Dempsey JA. Mechanical constraints on exercise hyperpnea in a fit aging population. Am Rev Respir Dis. 1991;143:968–77.

    CAS  PubMed  Google Scholar 

  69. 69.

    McClaran SR, Babcock MA, Pegelow DF, Reddan WG, Dempsey JA. Longitudinal effects of aging on lung function at rest and exercise in healthy active fit elderly adults. J Appl Physiol. 1995;78:1957–68.

    CAS  PubMed  Google Scholar 

  70. 70.

    Jakes RW, Day NE, Patel B, Khaw KT, Oakes S, Luben R, et al. Physical inactivity is associated with lower forced expiratory volume in 1 second: European prospective investigation into cancer-Norfolk prospective population study. Am J Epidemiol. 2002;156:139–47.

    PubMed  Google Scholar 

  71. 71.

    Pelkonen M, Notkola IL, Lakka T, Tukiainen HO, Kivinen P, Nissinen A. Delaying decline in pulmonary function with physical activity: a 25-year follow-up. Am J Respir Crit Care Med. 2003;168:494–9.

    PubMed  Google Scholar 

  72. 72.

    Degens H, Maden-Wilkinson TM, Ireland A, Korhonen MT, Suominen H, Heinonen A, et al. Relationship between ventilatory function and age in master athletes and a sedentary reference population. Age. 2013;35:1007–15.

    PubMed  Google Scholar 

  73. 73.

    Taylor BJ, Johnson BD. The pulmonary circulation and exercise responses in the elderly. Semin Respir Crit Care Med. 2010;31:528–38.

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Préfaut C, Anselme F, Caillaud C, Massé-Biron J. Exercise-induced hypoxemia in older athletes. J Appl Physiol. 1994;76:120–6.

    PubMed  Google Scholar 

  75. 75.

    Mills DE, Johnson MA, Barnett YA, Smith WHT, Sharpe GR. The effects of inspiratory muscle training in older adults. Med Sci Sports Exerc. 2015;47:691–7.

    CAS  PubMed  Google Scholar 

  76. 76.

    Hill A, Lupton H. Muscular exercise, lactic acid, and the supply and utilization of oxygen. Proc R Soc. 1924;97:135–71.

    Google Scholar 

  77. 77.

    Levine BD. VO2max: what do we know, and what do we still need to know? J Physiol. 2008;586:25–34.

    CAS  PubMed  Google Scholar 

  78. 78.

    Lye M, Donnellan C. Heart disease in the elderly. Heart. 2000;84:560–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Fujimoto N, Hastings JL, Bhella PS, Shibata S, Gandhi NK, Carrick-Ranson G, et al. Effect of ageing on left ventricular compliance and distensibility in healthy sedentary humans. J Physiol. 2012;590:1871–80.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Francis Stuart SD, Wang L, Woodard WR, Ng GA, Habecker BA, Ripplinger CM. Age-related changes in cardiac electrophysiology and calcium handling in response to sympathetic nerve stimulation. J Physiol. 2018;596:3977–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Vaitkevicius PV, Fleg JL, Engel JH, O’Connor FC, Wright JG, Lakatta LE, et al. Effects of age and aerobic capacity on arterial stiffness in healthy adults. Circulation. 1993;88:1456–62.

    CAS  PubMed  Google Scholar 

  82. 82.

    Tschakovsky ME, Sujirattanawimol K, Ruble SB, Valic Z, Joyner MJ. Is sympathetic neural vasoconstriction blunted in the vascular bed of exercising human muscle? J Physiol. 2002;541:623–35.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Mortensen SP, Nyberg M, Winding K, Saltin B. Lifelong physical activity preserves functional sympatholysis and purinergic signalling in the ageing human leg. J Physiol. 2012;590:6227–36.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Racine M, Dinenno F. Reduced deformability contributes to impaired deoxygenation-induced ATP release from red blood cells of older adult humans. J Physiol. 2019;597:4503–19.

    CAS  PubMed  Google Scholar 

  85. 85.

    Howden EJ, Carrick-Ranson G, Sarma S, Hieda M, Fujimoto N, Levine BD. Effects of sedentary aging and lifelong exercise on left ventricular systolic function. Med Sci Sports Exerc. 2018;50:494–501.

    PubMed  Google Scholar 

  86. 86.

    Hagberg JM, Allen WK, Seals DR, Hurley BF, Ehsani AA, Holloszy JO. A hemodynamic comparison of young and older endurance athletes during exercise. J Appl Physiol. 1985;58:2041–6.

    CAS  PubMed  Google Scholar 

  87. 87.

    Hawkins SA, Marcell TJ, Jaque SV, et al. A longitudinal VO2max and maximal heart rate in master athletes. Med Sci Sports Exerc. 2001;33:7.

    Google Scholar 

  88. 88.

    Nybo L, Schmidt JF, Fritzdorf S, Nordsborg NB. Physiological characteristics of an aging olympic athlete. Med Sci Sports Exerc. 2014;46:2132–8.

    PubMed  Google Scholar 

  89. 89.

    Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, et al. Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol. 1998;85:68–75.

    CAS  PubMed  Google Scholar 

  90. 90.

    Franzoni F, Ghiadoni L, Galetta F, Plantinga Y, Lubrano V, Huang Y, et al. Physical activity, plasma antioxidant capacity, and endothelium-dependent vasodilation in young and older men. Am J Hypertens. 2005;18:510–6.

    CAS  PubMed  Google Scholar 

  91. 91.

    Montero D, Padilla J, Diaz-Cañestro C, Muris DMJ, Pyke KE, Obert P, et al. Flow-mediated dilation in athletes: influence of aging. Med Sci Sports Exerc. 2014;46:2148–58.

    PubMed  Google Scholar 

  92. 92.

    Shibata S, Fujimoto N, Hastings JL, Carrick-Ranson G, Bhella PS, Hearon CM, et al. The effect of lifelong exercise frequency on arterial stiffness. J Physiol. 2018;596:2783–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  93. 93.

    Groot H, Rossman M, Garten R, Wang E, Hoff J, Helgerud J, et al. The effect of physical activity on passive leg movement-induced vasodilation with age. Med Sci Sports Exerc. 2016;48:1548–57.

    PubMed  PubMed Central  Google Scholar 

  94. 94.

    Nyberg M, Blackwell JR, Damsgaard R, Jones AM, Hellsten Y, Mortensen SP. Lifelong physical activity prevents an age-related reduction in arterial and skeletal muscle nitric oxide bioavailability in humans. J Physiol. 2012;590:5361–70.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Munch GDW, Svendsen JH, Damsgaard R, Secher NH, González-Alonso J, Mortensen SP. Maximal heart rate does not limit cardiovascular capacity in healthy humans: insight from right atrial pacing during maximal exercise. J Physiol. 2014;592:377–90.

    CAS  PubMed  Google Scholar 

  96. 96.

    Calbet JAL, Lundby C, Koskolou M, Boushel R. Importance of hemoglobin concentration to exercise: acute manipulations. Respir Physiol Neurobiol. 2006;151:132–40.

    CAS  PubMed  Google Scholar 

  97. 97.

    Schmidt WF, Prommer N. Impact of alterations in total hemoglobin mass on VO2max. Exerc Sport Sci Rev. 2010;38:68–75.

    PubMed  Google Scholar 

  98. 98.

    Salive M, Cornoni-Huntley J, Guralnik J, Philips C, Wallace R, Ostfeld A, et al. Anemia and hemoglobin levels in older persons: relationship with age, gender, and health status. J Am Geriatr Soc. 1992;40:489–96.

    CAS  PubMed  Google Scholar 

  99. 99.

    Steensma DP, Tefferi A. Anemia in the elderly: how should we define it, when does it matter, and what can be done? Mayo Clin Proc. 2007;82:958–66.

    CAS  PubMed  Google Scholar 

  100. 100.

    Schmidt W, Maassen N, Trost F, Böning D. Training induced effects on blood volume, erythrocyte turnover and haemoglobin oxygen binding properties. Eur J Appl Physiol Occup Physiol. 1988;57:490–8.

    CAS  PubMed  Google Scholar 

  101. 101.

    Schmidt W, Heinicke K, Rojas J, Gomez JM, Serrato M, Mora M, et al. Blood volume and hemoglobin mass in endurance athletes from moderate altitude. Med Sci Sports Exerc. 2002;34:1934–40.

    CAS  PubMed  Google Scholar 

  102. 102.

    Rea IM, Gibson DS, McGilligan V, McNerlan SE, Denis Alexander H, Ross OA. Age and age-related diseases: role of inflammation triggers and cytokines. Front Immunol. 2018;9:1–28.

    Google Scholar 

  103. 103.

    Monteiro Junior RS, de Tarso Maciel-Pinheiro P, da Matta M Portugal E, da Silva Figueiredo LF, Terra R, Carneiro LSF, et al. Effect of exercise on inflammatory profile of older persons: systematic review and meta-analyses. J Phys Act Health. 2018;15:65–71.

    Google Scholar 

  104. 104.

    Macciò A, Madeddu C. Management of anemia of inflammation in the elderly. Anemia. 2012;2012:1–20.

    Google Scholar 

  105. 105.

    Nemeth E, Ganz T. Anemia of inflammation. Hematol Oncol Clin N Am. 2014;28:671–81.

    Google Scholar 

  106. 106.

    di Prampero P. Metabolic and circulatory limitations to VO2max at the whole animal level. J Exp Biol. 1985;115:319–31.

    PubMed  Google Scholar 

  107. 107.

    Groen B, Hamer HM, Snijders T, van Kranenburg J, Frijns D, Vink H, et al. Skeletal muscle capillary density and microvascular function are compromised with aging and type 2 diabetes. J Appl Physiol. 2014;116:998–1005.

    CAS  PubMed  Google Scholar 

  108. 108.

    Chistiakov DA, Sobenin IA, Revin VV, Orekhov AN, Bobryshev YV. Mitochondrial aging and age-related dysfunction of mitochondria. Biomed Res Int. 2014;2014:238463.

    PubMed  PubMed Central  Google Scholar 

  109. 109.

    Conley KE, Jubrias SA, Esselman PC. Oxidative capacity and ageing in human muscle. J Physiol. 2000;526(Pt 1):203–10.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Proctor DN, Parker BA. Vasodilation and vascular control in contracting muscle of the aging human. Microcirculation. 2006;13:325–37.

    Google Scholar 

  111. 111.

    Hildebrandt W, Schwarzbach H, Pardun A, Hannemann L, Bogs B, König AM, et al. Age-related differences in skeletal muscle microvascular response to exercise as detected by contrast-enhanced ultrasound (CEUS). PLoS ONE. 2017;12:1–25.

    Google Scholar 

  112. 112.

    Ingjer F. Maximal aerobic power related to the capillary supply of the quadriceps femoris muscle in man. Acta Physiol Scand. 1978;104:238–40.

    CAS  PubMed  Google Scholar 

  113. 113.

    Hoppeler H, Howald H, Conley K, Lindstedt SL, Claassen H, Vock P, et al. Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol. 1985;59:320–7.

    CAS  PubMed  Google Scholar 

  114. 114.

    Andersen P, Henriksson J. Capillary supply of the quadriceps femoris muscle of man: adaptive response to exercise. J Physiol. 1977;270:677–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. 115.

    Lundby C, Montero D. CrossTalk opposing view: diffusion limitation of O2 from microvessels into muscle does not contribute to the limitation of VO2max. J Physiol. 2015;593:3759–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  116. 116.

    Wagner PD. CrossTalk proposal: diffusion limitation of O2 from microvessels into muscle does contribute to the limitation of VO2max. J Physiol. 2015;593:3757–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Gifford JR, Garten RS, Nelson AD, Trinity JD, Layec G, Witman MAH, et al. Symmorphosis and skeletal muscle VO2max: in vivo and in vitro measures reveal differing constraints in the exercise-trained and untrained human. J Physiol. 2016;594:1741–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 118.

    van der Zwaard S, de Ruiter CJ, Noordhof DA, Sterrenburg R, Bloemers FW, de Koning JJ, et al. Maximal oxygen uptake is proportional to muscle fiber oxidative capacity, from chronic heart failure patients to professional cyclists. J Appl Physiol. 2016;121:636–45.

    PubMed  Google Scholar 

  119. 119.

    Esposito F, Reese V, Shabetai R, Wagner P, Richardson R. Isolated quadriceps training increases maximal exercise capacity in chronic heart failure: the role of skeletal muscle convective and diffusive oxygen transport. J Am Coll Cardiol. 2011;58:1353–62.

    PubMed  PubMed Central  Google Scholar 

  120. 120.

    Lundby C, Jacobs RA. Adaptations of skeletal muscle mitochondria to exercise training. Exp Physiol. 2016;101:17–22.

    CAS  PubMed  Google Scholar 

  121. 121.

    Vigelsø A, Andersen NB, Dela F. The relationship between skeletal muscle mitochondrial citrate synthase activity and whole body oxygen uptake adaptations in response to exercise training. Int J Physiol Pathophysiol Pharmacol. 2014;6:84–101.

    PubMed  PubMed Central  Google Scholar 

  122. 122.

    Wagner PD. Modeling O2 transport as an integrated system limiting VO2max. Comput Methods Programs Biomed. 2011;101:109–14.

    PubMed  Google Scholar 

  123. 123.

    Adelnia F, Cameron D, Bergeron C, Fishbein K, Spencer R, Reiter D, et al. The role of perfusion in the age-associated decline of mitochondrial function with aging in healthy individuals. Front Physiol. 2019;10:427.

    PubMed  PubMed Central  Google Scholar 

  124. 124.

    Layec G, Trinity JD, Hart CR, Le Fur Y, Sorensen JR, Jeong EK, et al. Evidence of a metabolic reserve in the skeletal muscle of elderly people. Aging. 2017;9:52–67.

    CAS  Google Scholar 

  125. 125.

    Wray DW, Nishiyama SK, Monnet A, Wary C, Duteil SS, Carlier PG, et al. Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics. Am J Physiol Heart Circ Physiol. 2009;297:1870–5.

    Google Scholar 

  126. 126.

    Carrick-Ranson G, Hastings JL, Bhella PS, Shibata S, Fujimoto N, Palmer D, et al. The effect of age-related differences in body size and composition on cardiovascular determinants of VO2max. J Gerontol Ser A Biol Sci Med Sci. 2013;68:608–16.

    Google Scholar 

  127. 127.

    Ogawa T, Spina RJ, Martin WH, Kohrt WM, Schechtman KB, Holloszy JO, et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation. 1992;86:494–503.

    CAS  PubMed  Google Scholar 

  128. 128.

    Irrcher I, Adhihetty PJ, Joseph AM, Ljubicic V, Hood DA. Regulation of mitochondrial biogenesis in muscle by endurance exercise. Sports Med. 2003;33:783–93.

    PubMed  Google Scholar 

  129. 129.

    Kang C, Ji LL. Role of PGC-1α in muscle function and aging. J Sports Health Sci. 2013;2:81–6.

    Google Scholar 

  130. 130.

    Gavin TP, Ruster RS, Carrithers JA, Zwetsloot KA, Kraus RM, Evans CA, et al. No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol. 2007;585:231–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 131.

    Iversen N, Krustrup P, Rasmussen HN, Rasmussen UF, Saltin B, Pilegaard H. Mitochondrial biogenesis and angiogenesis in skeletal muscle of the elderly. Exp Gerontol. 2011;46:670–8.

    CAS  PubMed  Google Scholar 

  132. 132.

    Pollock RD, O’Brien KA, Daniels LJ, Nielsen KB, Rowlerson A, Duggal NA, 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:e12735.

    PubMed Central  Google Scholar 

  133. 133.

    Poole DC, Jones AM. Measurement of the maximum oxygen uptake VO2max: VO2peak is no longer acceptable. J Appl Physiol. 2017;122:997–1002.

    CAS  PubMed  Google Scholar 

  134. 134.

    Joyner MJ. Physiological limits to endurance exercise performance: influence of sex. J Physiol. 2017;595:2949–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Howden EJ, Perhonen M, Peshock RM, Zhang R, Arbab-Zadeh A, Adams-Huet B, et al. Females have a blunted cardiovascular response to one year of intensive supervised endurance training. J Appl Physiol. 2015;119:37–46.

    PubMed  PubMed Central  Google Scholar 

  136. 136.

    Ingjer F. Maximal oxygen uptake as a predictor of performance ability in women and men elite cross-country skiers. Scand J Med Sci Sports. 1991;1:25–30.

    Google Scholar 

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Acknowledgements

We sincerely thank Adrián Castillo García (http://www.fissac.com) for designing the figures included in this work.

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Correspondence to Pedro L. Valenzuela.

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The work of Pedro Valenzuela is supported by University of Acalá (FPI2016) and the research by Alejandro Lucia on aging is funded by the Fondo de Investigaciones Sanitarias, Instituto de Salud Carlos III (FIS, Grant PI15/00558) and cofunded by ‘Fondos FEDER’. No other specific sources of funding were used to assist in the preparation of this article.

Conflict of interest

Pedro L. Valenzuela, Nicola A. Maffiuletti, Michael J. Joyner, Alejandro Lucia and Romuald Lepers declare that they have no conflicts of interest relevant to the content of this review.

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Valenzuela, P.L., Maffiuletti, N.A., Joyner, M.J. et al. Lifelong Endurance Exercise as a Countermeasure Against Age-Related \(\dot{V}{\text{O}}_{{ 2 {\text{max}}}}\) Decline: Physiological Overview and Insights from Masters Athletes. Sports Med 50, 703–716 (2020). https://doi.org/10.1007/s40279-019-01252-0

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