Tanaka Physiology

Comparison of 1896 Olympic Winning Times and Current Masters Records

Table 1: Comparison of 1896 Olympic Winning Times in Running Events and Current Masters Records that Surpass Those Winning Times

Running events	1896 Olympic winning time	Current age-group records that surpass 1896 Olympic times	Age at which these records were achieved
100 m (s)	12.0	11.7	61 years
200 m (s)	22.2	22.1	46 years
400 m (s)	54.2	53.9	63 years
800 m (min:s)	2:11.0	2:10.4	60 years
1500 m (min:s)	4:33:2	4:27:7	60 years
Marathon (h:min:s)	2:58:50	2:54:5	73 years

Endurance Exercise Performance with Ageing

Peak Athletic Performance

Peak athletic performance has improved dramatically in the past 100 years, although the age at which peak performance is achieved in Olympic track and field (athletics), swimming, baseball, tennis, and golf has remained constant over this period (Schulz & Curnow, 1988). However, as the number of older adults participating in competitive events has increased (at a much greater rate than young adults), and training and nutritional practices have evolved, Masters athletes have achieved impressive improvements in peak exercise performance (Ericsson, 1993).

For example, in 2005 Kozo Haraguchi of Japan set a new age-group record in the 100 m dash of 21.69 s at the age of 95. In 2003, Ed Whitlock of Canada became the oldest person to break 3 h in marathon at the age of 73. In some athletic events (e.g., marathon running), Masters athletes over 70 years of age have surpassed the winning time at the first Olympic games held in Athens (Table 1). These exceptional individual athletic achievements are fascinating not only to the general public, but also to those of us who study the effects of ageing on physiological functional capacity. It also highlights the broad question of how endurance exercise performance changes with age in healthy adults.

Changes in Marathon Running Times with Age

As illustrated in Fig. 1, endurance performance in running events decreases with age in a curvilinear fashion. In general, peak endurance running performance is maintained until ∼35 years of age, followed by modest decreases until 50–60 years of age, with progressively steeper reductions thereafter (Tanaka & Seals, 2003). The pattern appears to be similar for both non-elite and elite endurance athletes (Joyner, 1993).

In general, the magnitude of decline in endurance running performance with age is greater in women than in men (Joyner, 1993; Tanaka & Seals, 1997; Donato et al. 2003). However, interpretation of this apparent widening of sex differences with advancing age is confounded by the relatively smaller number of female versus male runners in the older groups. Indeed, such increasing sex differences with age are absent in the endurance swimming population.

Physiological Determinants of Endurance Exercise Performance

Based largely on studies in young endurance-trained athletes, the three main physiological determinants of endurance performance are believed to be:

• Maximal oxygen consumption (VO₂max)
• Exercise economy
• The exercise intensity at which a high fraction of the maximal oxygen consumption can be sustained, typically defined by the ‘lactate threshold’ (Hagberg & Coyle, 1983; Joyner, 1993).

Changes in Determinants with Age

In the following section, we review the available information on how changes in these determinants may contribute to age-related declines in endurance exercise performance.

Exercise Economy

Exercise economy is measured as the steady-state oxygen consumption while exercising at a specific submaximal exercise intensity below the lactate threshold. Among endurance athletes, exercise economy is an important determinant of endurance performance, particularly in groups that are more homogeneous in VO₂max (Morgan et al. 1989).

Observations and Studies

• Cross-sectional Observations: Numerous independent laboratories indicate that exercise economy does not change with advancing age (Astrand, 1960; Allen et al. 1985; Wells et al. 1992; Evans et al. 1995).

  • In a cross-sectional study of male endurance runners, there was no difference in running economy between young and older athletes (Allen et al. 1985).
  • No significant association was found between running economy and age among highly trained and competitive female runners aged 35–70 years (Wells et al. 1992).

• Longitudinal Studies: Several longitudinal studies have confirmed that running economy does not change with age in endurance-trained Masters athletes (Robinson et al. 1976; Trappe et al. 1996).

Variance in Endurance Performance

In healthy female athletes, running economy explained little of the variance in age-related decreases in endurance running performance after accounting for differences in VO₂max and lactate threshold, which explained 85% of the variability in 10K performance (Evans et al. 1995).

Physiological Factors Determining Exercise Economy

There are several physiological factors that determine exercise economy, among which the percentage of type I muscle fibers is positively associated with exercise economy in cyclists (Horowitz et al. 1994).

Muscle Fiber Distribution

Well-trained Masters athletes have a similar muscle fiber distribution to performance-matched athletes, indicating that reductions in exercise economy do not significantly contribute to the decreases in endurance exercise performance observed with advancing age.

Lactate Threshold and Endurance Performance

The lactate threshold is a critical physiological marker used in endurance training. It is generally defined as the exercise intensity at which blood lactate concentration increases significantly above baseline (Allenet al. 1985; Coyle, 1995). In young endurance-trained adults, the lactate threshold predicts exercise performance in distance events ranging from 2 miles to the marathon (Hagberg & Coyle, 1983; Allen et al. 1985; Joyner, 1993), whereas power output at the lactate threshold is the best laboratory predictor of time-trial performance among competitive female Masters cyclists (Nicholset al. 1997).

Absolute work rate or running speed at lactate threshold declines with advancing age in endurance athletes (Iwaoka et al. 1988; Maffulli et al. 1994; Evans et al. 1995; Wiswell et al. 2000). However, lactate threshold does not appear to change with increasing age when expressed relative to the percentage of ˙V O2max (Iwaoka et al. 1988; Maffulli et al. 1994; Evans et al. 1995). This finding suggests that the contribution of decreases in lactate threshold to reductions in endurance exercise performance with ageing may be secondary to decreases in ˙V O2max. Indeed, a recent longitudinal study of 51 male and 23 female Masters runners reported that the change in lactate threshold over a mean follow-up period of 6 years was not predictive of a corresponding change in running performance when it was expressed as a percent of ˙V O2max (Marcell et al. 2003).

Maximal Aerobic Capacity (˙V O2max)

Maximal oxygen consumption establishes the upper limit of maximal energy production through oxidative phosphorylation and is generally considered to be a primary determinant of endurance exercise performance among young endurance-trained athletes (Joyner, 1993; Coyle, 1995). ˙V O2max declines approximately 10% per decade after age 25–30 years in healthy sedentary adults of both sexes (Heath et al. 1981; Buskirk & Hodgson, 1987; FitzGerald et al. 1997; Tanaka et al. 1997; Eskurza et al. 2002; Pimentel et al. 2003).

Early investigations suggested that the rate of decline in ˙V O2max with advancing age was as much as 50% smaller in endurance exercise-trained athletes than in sedentary adults (Heath et al. 1981; Kasch et al. 1990). However, subsequent studies established that when expressed as a percentage decrease from early adulthood, the rate of decline in ˙V O2max with age is not reduced in healthy adults who habitually perform aerobic exercise (Hodgson & Buskirk, 1977; FitzGerald et al. 1997; Tanaka et al. 1997; Wilson & Tanaka, 2000; Eskurza et al. 2002; Pimentel et al. 2003; Fleg et al. 2005). In fact, endurance exercise-trained men and women demonstrate greater ‘absolute’ decline in ˙V O2max with age compared to sedentary individuals.

Endurance Performance and Masters Athletes

Decline in VO2max Over Age

Recent evidence suggests that the decline in VO2max over the entire adult age range is not linear but rather curvilinear, with the rate of decline accelerating with advancing age (Fleg et al. 2005). This concept, originally described by Buskirk & Hodgson in 1987 (Buskirk & Hodgson, 1987), aligns with the idea that a decrease in maximal oxygen consumption is the primary mechanism causing age-related reductions in endurance exercise performance.

Factors Contributing to Reductions in VO2max

The factors contributing to reductions in VO2max with age in Masters endurance athletes are not fully understood. Available evidence points to an overall reduction in the exercise training ‘stimulus’ (i.e., exercise-training intensity, session duration, and weekly frequency) with advancing age (Pollock et al. 1997; Tanaka et al. 1997; McGuire et al. 2001; Eskurza et al. 2002).

Reduction in Training Stimulus

• Early Observations: As early as 1967, Dill et al. suggested that highly trained distance runners who become sedentary exhibit a greater than normal decrease in maximal aerobic capacity with advancing age (Dill et al. 1967).
• Longitudinal Studies: Longitudinal studies indicate that VO2max can be fairly well maintained over phases of middle-age lasting up to 10 years in men and women who continue to train vigorously (Kasch & Wallace, 1976; Pollock et al. 1987).
• Long-term Maintenance: However, there is no evidence that exercise training intensity and volume (and VO2max) can be maintained for longer periods, especially at older ages (Dill et al. 1967; Pollock et al. 1997).

Contributing Factors

• Increased Responsibilities: Increases in job- and family-related responsibilities may impinge on the availability of time and energy for the intensive training required to remain competitive.
• Injuries: Increased prevalence of exercise training-associated injuries among Masters athletes also probably contributes to their reduced training intensity and volume (Kallinen & Markku, 1995).
• Motivation: The motivation to train may be reduced with advancing age among Masters athletes, similar to the declines in compliance observed in older patients participating in cardiac rehabilitation programs (Cooper et al. 2002).
• Shift in Goals: The goals underlying the motivation to train may shift from achieving personal records in younger athletes to health benefits in older athletes (Ogles & Masters, 2000), accommodating reductions in exercise intensity with age.
• Intrinsic Drive: The ‘intrinsic drive’ to exercise or be physically active may decline with ageing, as demonstrated by rodents given lifelong access to running wheels showing marked reductions in nocturnal running behavior with advancing age (Valentinuzzi et al. 1997).

Summary

It appears that in healthy adults, the ability to maintain the overall exercise-training stimulus contributes to the rate of decline in VO2max and therefore endurance performance.

Oxygen Consumption and Its Determinants at Maximal Exercise in Endurance-Trained Men

Table 2: Oxygen Consumption and Its Determinants at Maximal Exercise

Parameter	Young Men (28 years)	Older Men (60 years)	Age-Related Change (%)
Oxygen consumption (ml kg−1 min−1)	68.2	49.4	28
Cardiac output (l min−1)	27.0	21.7	20
Stroke volume (ml beat−1)	147	132	10
Heart rate (beats min−1)	184	165	10
a–v O2 difference (ml (100 ml)−1)	16.7	15.2	8

The data were compiled from four studies in which values for all of the variables were reported in groups of young and older groups (Grimby et al. 1966; Hagberg et al. 1985; Rivera et al. 1989; Ogawa et al. 1992).

Central Factors

Maximal Cardiac Output

Although it has been reported that maximal cardiac output is maintained with advancing age (Rodeheffer et al. 1984), the majority of the evidence supports the idea that maximal cardiac output decreases with advancing age in healthy sedentary adults (Julius et al. 1967; Saltin, 1986; Rivera et al. 1989; Ogawa et al. 1992; Hunt et al. 1998) in proportion to the decline in maximal oxygen consumption (Grimby et al. 1966; Proctor et al. 1998). Maximal cardiac output also is reduced in older Masters (60–70 years) compared with young (20–30 years) endurance-trained athletes as a result of reductions in both maximal stroke volume and maximal heart rate (Rivera et al. 1989; Ogawa et al. 1992) (Table 2).

Maximal Heart Rate

Historically, maximal heart rate has been viewed as the primary mechanism mediating age-related reductions in maximal cardiac output and ( \dot{V}O_{2max} ), particularly in endurance exercise-trained athletes (Heath et al. 1981; Hagberg et al. 1985). Starting from early adulthood, maximal heart rate declines with age at a rate of ∼0.7 beats min(^{-1}) year(^{-1}) in healthy sedentary, recreationally active and endurance exercise-trained adults (Tanaka et al. 2001). A slower conduction velocity, a reduced responsiveness of the sinoatrial node to β-adrenergic stimulation (Fleget al. 1994) and a decreased intrinsic heart rate (Jose & Collison, 1970) are among the mechanisms believed to contribute to the reduction in maximal heart rate with ageing.

Maximal Stroke Volume

In older endurance exercise-trained adults, maximal stroke volume is reduced modestly to 80–90% of that observed in young endurance-trained adults (Ogawa et al. 1992) (Table 2). There is very limited information as to how changes in the major determinants of stroke volume (e.g., preload, afterload and intrinsic contractility of the heart) contribute to the age-related reduction in maximal stroke volume in endurance-trained adults. It is unclear if a reduction in left ventricular filling is involved. Results of studies indicating that left ventricular preload, as expressed as left ventricular end-diastolic dimension, area or volume, is not related to age in healthy relatively active adults (Fleg, 1986) do not support such a role.

Endurance Performance and Masters Athletes

Central Factors

Endurance performance is influenced by central factors such as ventricular preload and afterload. Studies have shown that contractility declines significantly with advancing age in endurance-trained rats, similar to sedentary rats (Starnes & Rumsey, 1988). Observations in human studies also indicate that older sedentary and endurance-trained athletes exhibit lower ejection fractions at maximal exercise compared to young men (Schulman et al. 1992).

Peripheral Factors

Peripheral factors, particularly the capacity of active skeletal muscles and respiratory muscles to extract and consume oxygen from the blood for ATP production during maximal exercise, are crucial. In sedentary adults, maximal arterio-venous O₂ difference declines with age, consistent with reductions in capillary density and mitochondrial enzyme activities (Coggan et al. 1992).

In endurance-trained adults, the maximal arterio-venous O₂ difference declines modestly (5–10%) over a span of approximately 30 years (Hagberg et al. 1985; Saltin, 1986; Rivera et al. 1989). Older endurance-trained athletes can oxygenate blood in the lungs to a similar extent as young athletes, and their contracting muscles are capable of extracting oxygen as effectively as their younger counterparts (Saltin, 1986). Muscle oxidative enzyme activities and capillarization are similar between young and older endurance-trained adults (Coggan et al. 1992; Proctor et al. 1995). Therefore, maximal oxygen delivery, rather than oxygen extraction, is likely a major contributor to the age-related reduction in maximal arterio-venous O₂ difference in endurance-trained adults.

Skeletal Muscle Mass and VO₂max

Skeletal muscle mass is closely related to maximal aerobic capacity among healthy humans across the adult age range (Fleg & Lakatta, 1988). However, ˙VO₂max remains lower in older compared with young endurance-trained athletes after correcting for muscle mass (Proctor & Joyner, 1997). Fat-free mass exerts its permissive influence on ˙VO₂max via an effect on central circulatory function involving blood volume, stroke volume, and cardiac output (Hunt et al. 1998).

Summary and Conclusions

In summary, Masters endurance athletes maintain significant capacities despite age-related physiological changes. Central circulatory function and oxygen delivery play critical roles in sustaining endurance performance in older athletes.

References

• Cooper AF, Jackson G, Weinman J & Horne R (2002). Factors associated with cardiac rehabilitation attendance: a systematic review of the literature. Clin Rehabil 16, 541–552.
• Coyle EF (1995). Integration of the physiological factors determining endurance performance ability. In Exercise and Sports Sciences Reviews, Vol. 23, ed. Holloszy JO, pp. 25–63. Williams & Wilkins, Baltimore, MD.
• Dill DB, Robinson S & Ross JC (1967). A longitudinal study of 16 champion runners. J Sports Med 7, 4–27.
• Donato AJ, Trench K, Glueck DH, Seals DR, Eskurza I & Tanaka H (2003). Declines in physiological functional capacity with age: a longitudinal study in peak swimming performance. J Appl Physiol 94, 764–769.
• Ericsson KA (1993). Peak performance and age: an examination of peak performance in sports. In Successful Aging: Perspectives from the Behavioral Sciences, ed. Baltes PB & Baltes MM, pp. 164–196. Cambridge University Press, Cambridge, UK.
• Eskurza I, Donato AJ, Moreau KL, Seals DR & Tanaka H (2002). Changes in maximal aerobic capacity with age in endurance-trained women: 7-year follow-up. J Appl Physiol 92, 2303–2308.
• Evans SL, Davy KP, Stevenson ET & Seals DR (1995). Physiological determinants of 10-km performance in highly trained female runners of different ages. J Appl Physiol 78, 1931–1941.
• FitzGerald MD, Tanaka H, Tran ZV & Seals DR (1997). Age-related decline in maximal aerobic capacity in regularly exercising vs sedentary females: a meta-analysis. J Appl Physiol 83, 160–165.
• Fleg JL (1986). Alterations in cardiovascular structure and function with advancing age. Am J Cardiol 57, 33C–44C.
• Fleg JL & Lakatta EG (1988). Role of muscle loss in the age-associated reduction in VO2max. J Appl Physiol 65, 1147–1151.
• Fleg JL, Morrell CH, Bos AG, Brant LJ, Talbot LA, Wright JG & Lakatta EG (2005). Accelerated longitudinal decline of aerobic capacity in healthy older adults. Circulation 112, 674–682.
• Fleg JL, Schulman S, O’Connor F, Becker LC, Gerstenblith G, Clulow JF, Renlund DG & Lakatta EG (1994). Effects of acute β-adrenergic receptor blockade on age-associated changes in cardiovascular performance during dynamic exercise. Circulation 90, 2333–2341.
• Fuchi T, Iwaoka K, Higuchi M & Kobayashi S (1989). Cardiovascular changes associated with decreased aerobic capacity and aging in long-distance runners. Eur J Appl Physiol 58, 884–889.
• Giada F, Bertaglia E, De Piccoli B, Franceschi M, Sartori F, Ravielle A & Pasotto G (1998). Cardiovascular adaptations to endurance training and detraining in young and older athletes. Int J Cardiol 65, 149–155.
• Grimby G, Nilsson NJ & Saltin B (1966). Cardiac output during submaximal and maximal exercise in active middle-aged athletes. J Appl Physiol 21, 1150–1156.
• Grimby G & Saltin B (1983). The ageing muscle. Clin Physiol 3, 209–218.
• Hagberg JM, Allen WK, Seals DR, Hurley BF, Ehsani AA & Holloszy JO (1985). A hemodynamic comparison of young and older endurance-trained men. J Appl Physiol 58, 1884–1890.

Endurance Performance and Masters Athletes

Factors Affecting Running Economy

Morgan DW, Martin PE & Krahenbuhl GS (1989). Factors affecting running economy. Sports Med 7, 310–330.

Relationship Between Blood Lactate Response to Exercise and Endurance Performance

Nichols JF, Phares SL & Buono MJ (1997). Relationship between blood lactate response to exercise and endurance performance in competitive female master cyclists. Int J Sports Med 18, 458–463.

Effects of Aging, Sex, and Physical Training on Cardiovascular Responses to Exercise

Ogawa T, Spina RJ, Martin WH III, Kohrt WM, Schechtman KB, Holloszy JO & Ehsani AA (1992). Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 86, 494–503.

Older vs. Younger Adult Male Marathon Runners: Participative Motives and Training Habits

Ogles BM & Masters KS (2000). Older vs. younger adult male marathon runners: participative motives and training habits. J Sport Behavior 23, 130–143.

Greater Rate of Decline in Maximal Aerobic Capacity with Age in Endurance-Trained vs. Sedentary Men

Pimentel AE, Gentile CL, Tanaka H, Seals DR & Gates PE (2003). Greater rate of decline in maximal aerobic capacity with age in endurance-trained vs. sedentary men. J Appl Physiol 94, 2406–2413.

Effect of Age and Training on Aerobic Capacity and Body Composition of Master Athletes

Pollock ML, Foster C, Knapp D, Rod JL & Schmidt DH (1987). Effect of age and training on aerobic capacity and body composition of master athletes. J Appl Physiol 62, 725–731.

Twenty-Year Follow-Up of Aerobic Power and Body Composition of Older Track Athletes

Pollock ML, Mengelkoch LJ, Graves JE, Lowenthal DT, Limacher MC, Foster C & Wilmore JH (1997). Twenty-year follow-up of aerobic power and body composition of older track athletes. J Appl Physiol 82, 1508–1516.

Influence of Age and Gender on Cardiac Output–VO2 Relationships During Submaximal Cycle Ergometry

Proctor DN, Beck KC, Shen PH, Eickhoff TJ, Halliwill JR & Joyner MJ (1998). Influence of age and gender on cardiac output–VO2 relationships during submaximal cycle ergometry. J Appl Physiol 84, 599–605.

Skeletal Muscle Mass and the Reduction of VO2,max in Trained Older Subjects

Proctor DN & Joyner MJ (1997). Skeletal muscle mass and the reduction of VO2,max in trained older subjects. J Appl Physiol 82, 1411–1415.

Oxidative Capacity of Human Muscle Fiber Types: Effects of Age and Training Status

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

Physiological Factors Associated with the Lower Maximal Oxygen Consumption of Master Runners

Rivera AM, Pels AE, Sady SP, Sady MA, Cullinane EM & Thompson PD (1989). Physiological factors associated with the lower maximal oxygen consumption of master runners. J Appl Physiol 66, 949–954.

Experimental Studies of Physical Fitness in Relation to Age

Robinson S (1938). Experimental studies of physical fitness in relation to age. Arbeitsphysiol 10, 251–323.

Physiological Aging of Champion Runners

Robinson S, Dill DB, Robinson RD, Tzankoff SP & Wagner JA (1976). Physiological aging of champion runners. J Appl Physiol 41, 46–51.

Exercise Cardiac Output is Maintained with Advancing Age in Healthy Human Subjects

Rodeheffer RJ, Gerstenblith G, Becker LC, Fleg JL, Weisfeldt ML & Lakatta EG (1984). Exercise cardiac output is maintained with advancing age in healthy human subjects: cardiac dilatation and increased stroke volume compensate for a diminished heart rate. Circulation 69, 203–213.

The Aging Endurance Athlete

Saltin B (1986). The aging endurance athlete. In Sports Medicine for the Mature Athlete, ed. Sutton JR & Brock RM, pp. 59–80. Benchmark Press, Indianapolis, IN.

Age-Related Decline in Left Ventricular Filling at Rest and Exercise

Schulman SP, Lakatta EG, Fleg JL, Lakatta L, Becker LC & Gerstenblith G (1992). Age-related decline in left ventricular filling at rest and exercise. Am J Physiol Heart Circ Physiol 263, H1932–H1938.