EDITORIAL COMMENT
Payments for Debts Associated With Exercise Can Become Higher as We Age and Limit Exercise Capacity*
Edward G. Lakatta, MD* and
Paul D. Chantler, PhD
National Institute on Aging Intramural Research Program, Gerontology Research Center, Baltimore, Maryland
* Reprint requests and correspondence: Dr. Edward G. Lakatta, National Institute on Aging, 5600 Nathan Shock Drive, Baltimore, Maryland 21224-6825 (Email: LakattaE{at}grc.nia.nih.gov).
When one considers the oxygen cost of exercise, the body’s rate of oxygen consumption (VO2) in excess of that in the basal state while the exercise is being performed initially comes to mind. But Woo et al. (1), in a paper appearing in this issue of the Journal, remind us that for several minutes after an acute bout of exercise, the body continues to consume oxygen at a rate in excess of the basal rate. This continued increased VO2 during recovery from exercise, sometimes referred to as an "oxygen debt," when expressed relative to work performed during the exercise, can range from 14% to 21% of the total VO2 associated with the performance of and recovery from exercise. The "O2 debt", paid during recovery from exercise, often has not been factored into estimates of exercise efficiency (calories expended for work performed) and reduces efficiency, because it contributes to the total O2 cost associated with the exercise but contributes no external work.
In their study, Woo et al. (1), measured the external work performed, the VO2 during treadmill exercise, and recovery (6 min) from exercise. Exercise efficiency was determined in sedentary younger (20 to 33 years) and older (65 to 79 years) men and women, before and after a supervised exercise training program, consisting of walking/jogging, bicycling, and stretching, each for 30 min, three times/week for 6 months. Although work performed and VO2 during the exercise were lower in older subjects, the VO2 during the exercise, per unit work performed, did not change with age. But VO2 during recovery from exercise in older subjects, however, exceeded that in younger persons by 34%, which translated into a lower efficiency in older subjects. Furthermore, the kinetics of VO2 recovery was reduced in older versus younger subjects. Importantly, similar age-associated differences were also observed after recovery from a submaximal workload at an absolute VO2 common to all subjects. There were no significant gender differences in the O2 debt or efficiency. In older subjects, the exercise-conditioning program reduced the O2 debt by nearly 30%, which translated into an 18% increase in exercise efficiency; but efficiency did not change in younger persons.
The age differences in O2 debt are striking, as is the effect of the training program to reduce this debt to a greater extent in older subjects than in their younger counterparts. But what are the underlying mechanisms and what is the physiological significance of an O2 debt? The O2 debt after exercise is highly correlated with the ability to adjust to the energetic requirements at the onset of exercise, (i.e., attributed to a reduction in the acceleration of the kinetics of O2 delivery and utilization). Long-recognized factors for muscle O2 utilization include lean muscle mass, muscle fiber type, blood flow to working muscle, and O2 extraction and utilization by muscle. An inability to shunt blood flow to working muscles during exercise, a reduced muscle capillary density, and muscle mass are causes for the well-documented age-associated reduction in O2 extraction from the blood with aging. In this respect, it would have been instructive to know the arteriovenous O2 difference, an index of O2 extraction from the blood and a component of the O2 pulse, interpreted by Woo et al. (1) to reflect only the stroke volume. Anaerobic muscle metabolism, indexed as lactate build-up during exercise, resulting either from an inability to shunt blood flow to working muscle or from deficient muscle mitochondrial O2 utilization or to a shift in substrate preference, is another factor involved in the O2 debt. Prior studies indicate a higher age-associated increase in plasma lactate during vigorous exercise (2) and an age-associated reduction in mitochondrial respiration efficiency (3,4).
The exercise training benefits on exercise efficiency identified by Woo et al. (1) were more pronounced in older than younger subjects, irrespective of gender. Aerobic exercise training in older persons not only improves exercise-work capacity but also increases muscle mass; improves capillary density, muscle respiration, mitochondrial enzymes, and muscle oxidative capacity; reduces plasma lactate during exercise; and reduces the O2 debt (5–8). Thus, the interpretation of Woo et al. (1) that a greater recovery VO2 and reduced exercise efficiency occurring with advancing age somehow relates to these factors during the exercise appears to be valid. Still, it remains an enigma that an O2 debt is not reflected in an age-associated difference in the VO2/work performed during exercise or in the anaerobic threshold and that it is also observed after sub-maximal exercise.
Factors relating to a continued demand for VO2 during recovery from exercise that differ with age and conditioning (9,10) might include increased plasma catecholamines, lactate, core temperature, and cardiac function, each of which can remain elevated for at least 1 h after vigorous exercise (5). Thus, estimation of O2 debt for 6 min by Woo et al. (1) did not likely capture the full magnitude of the debt. Age differences in the intensity and duration of some of these factors that increase VO2 demand during recovery from exercise can be linked to age differences that occur during vigorous exercise. For example, owing to an age-associated "loss of regulation of mitochondrial and peripheral circulatory function," older persons reach their anaerobic threshold at a lower absolute level of work performed, and this limits their exercise duration. Notwithstanding that, the greater lactate build-up by working muscles and the general increase in core temperature during exercise in older versus young persons need to be dissipated during recovery from exercise. Thus, reduced blood flow to working muscles or reduced O2 utilization by muscle and a reduced ability to increase skin blood flow to dissipate heat during exercise are among the real culprits that both limit the exercise performed and require a greater O2 unitization during recovery from exercise. Often, less-well-characterized factors that might contribute to the age-associated limitations in exercise capacity and contribute to the debt paid during recovery from exercise include an increased production of reactive O2 species or inflammatory cytokines in older persons.
During exercise, sympathetic stimulation increases markedly, whereas vagal "tone" is withdrawn, thus increasing heart rate, myocardial contractility, cardiac output distribution, and muscle O2 utilization. During recovery from exercise, vagal influence waxes and adrenergic tone wanes. In older persons during exercise, an excessive accumulation of catecholamines can maintain the excessive O2 utilization by muscles during recovery even in the absence of demand for muscle work. Plasma norepinephrine during exercise is positively correlated with O2 debt (5). Thus, one could envision a scenario for which continued O2 consumption during recovery occurs, in part at least, on the basis of delayed restitution or reduction of a stimulus (beta adrenergic receptor signaling [beta AR] signaling) that continues to drive O2 consumption during recovery. Subjects in the Woo et al. study assumed the seated position during recovery from exercise. Catecholamines increase mitochondrial [Ca2+], leading to enhanced respiration via stimulation of dyhydrogenases that drive oxidative phosphorylation. Prolonged exposure of the older heart to catecholamines leads to excessive mitochondrial Ca2+ gain (11) and continued activation of oxidative phosphorylation that might transiently persist in the absence of a continued energy demand. This markedly increases the catecholamine drive and might add to the O2 debt particularly in older subjects, because in assuming the seated position after exercise, smaller cardiac volumes and a higher heart rate are reported and these effects are blunted by beta AR blockade (10). Cellular effects of beta AR stimulation, which include phosphorylation of numerous proteins, are reversed after exercise, in large part by activation of cholinergic receptor stimulation, which unfortunately also declines with aging (9). Exercise conditioning markedly improves the efficiency of vagal stimulation and also lowers catecholamine build-up during exercise (12), thus the lower O2 debt identified in trained individuals might be related to the lower peak exercise catecholamine concentrations (or inflammatory cytokines).
In summary, the bad news conveyed to us by Woo et al. (1) is that metabolic debts associated with the performance of dynamic exercise increase with aging. These debts, paid during recovery from exercise are likely attributable to an inability of the older body to adapt to the energy requirements of exercise. Specific factors include reductions in muscle mass and strength, inadequate blood flow to muscles, and a reduced efficiency of muscle respiration. Excessive elevation of catecholamines and core temperature occurs during exercise in older persons, as do other less-well-characterized factors (e.g., excessive reactive O2 species and an exaggerated elevation of inflammatory cytokines). These factors cause muscle fatigue and a shift to anaerobic metabolism. During recovery, excessive catecholamine concentrations and incomplete waning of cell responses to catecholamine drive during exercise might continue to stimulate both muscle respiration in the absence of continued demand for muscle work and the cardiovascular system to dissipate lactate and heat generated during exercise. The physiological significance of this metabolic debt incurred during exercise is that its underlying factors collectively reduce exercise capacity, with all the attendant health and performance drawbacks of such a reduction. The good news is that all of these age-associated deficits can be substantially reduced by regular exercise (i.e., physical conditioning)!
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Footnotes
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* Editorials published in the Journal of American College of Cardiology reflect the views of the authors and do not necessarily represent the views of JACC or the American College of Cardiology. 
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References
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- Brodde OE, Leineweber K. Autonomic receptor systems in the failing and aging human heartsimilarities and differences. Eur J Pharmacol 2004;500:167-176.[CrossRef][ISI][Medline]
- Renlund DG, Lakatta EG, Fleg JL, et al. Prolonged decrease in cardiac volumes after maximal upright bicycle exercise J Appl Physiol 1987;63:1947-1955.[Abstract/Free Full Text]
- Pepe S, Tsuchiya N, Lakatta EG, et al. PUFA and aging modulate cardiac mitochondrial membrane lipid composition and Ca2+ activation of PDH Am J Physiol 1999;276:149-158.
- Peronnet F, Cleroux J, Perrault H, et al. Plasma norepinephrine response to exercise before and after training in humans J Appl Physiol 1981;51:812-815.[Abstract/Free Full Text]
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