ISSUES IN FATIGUE IN SPORT AND EXERCISE
------~------~
Sports Medicine 13 (2): 127-133, 1992 0112-1642/92/0002-0127/$03.50/0 © Adis International Limited. All rights reserved. SPOll19
Limitations to Maximal Oxygen Uptake 1 John R. Sultan Faculty of Health Sciences, University of Sydney, Sydney, New South Wales, Australia
Contents 127 128 129 129 J30 13 J 131 132
Summary
Summary 1. The Oxygen Transport System 2. The Lungs 3. Arterial Oxygen Saturation and Haemoglobin 4. Cardiovascular Function 5. Distribution of Cardiac Output 6. Muscle Blood Flow 7. Conclusion
An increase in exercise capacity depends on the magnitude of increase in maximum aerobic capacity. Central and peripheral factors may limit oxygen uptake. Central oxygen delivery depends on cardiac output and maximal arterial oxygen content. Peripheral extraction of the delivered oxygen is expressed as a-v 02. With increasing intensities of exercise, the respiratory system may become limiting in some trained individuals. Most studies have shown a higher stroke volume in maximal as well as submaximal exercise in the trained vs untrained individuals. A variety of peripheral factors determine vascular tone. Maximal oxygen uptake depends on all components of the oxygen transporting system, but stroke volume appears to be the prime determinant in the trained subject. At maximum exercise the capacity of the muscle capillary network is never reached.
The ability of humans to excel in exercise of significant duration depends on aerobic metabolism. Those with the highest aerobic metabolism will in general be able to perform best, although, of course, additional factors will determine who crosses the finish line first. Furthermore, following an aerobic training programme the magnitude of the increase in exercise capacity will depend on the 1 This article was presented at a Symposium on Fatigue in Sport and Exercise in November 1990 and updated by the author for publication in Sports Medicine.
magnitude of increase in maximum aerobic capacity (V02max). This is the criterion which is used as the 'gold standard' for assessing endurance performance potential. Resting oxygen uptake is similar in trained and untrained individuals, however, there is at least a 2- to 3-fold greater maximal oxygen uptake in the trained vs the untrained individual. In this paper I examine the magnitude of increases in maximal oxygen uptake from rest to exercise in the trained vs untrained individuals, the capacity of each COffi-
Sports Medicine 13 (2) 1992
128
ponent of oxygen transport in determining maximal oxygen uptake and the differences in limitation to maximal uptake in the trained compared with the untrained. The study by Robinson et al. (1938) was the first to identify maximal oxygen uptake as an important determinant of exercise performance. In that study they demonstrated that in men maximal oxygen uptake peaked around about 20 years of age and thereafter decreased. Since that time studies have included men and women, but the overall observation remains, that age by itself will result in a decreased maximal oxygen uptake. Furthermore, women have a lower V02max than men but the difference decreases with increasing age after adolescence (fig. 1). Another crucial factor which determines cardiorespiratory fitness (V02max) is heredity; are athletes born or can they be made? The classic bed rest studies of Saltin and colleagues (1968) contain among the most compelling data to suggest that training can produce marked increases in maximal oxygen uptake (V02max), that bed rest will decrease V02max significantly and that subjects are not able to be trained to levels comparable to the highest seen in the top endurance athletes. In the 1968 study Saltin and colleagues found that 3 weeks of bed rest caused V02max to fall to two-thirds of its control level (25 mljkg/min); however, several months of training resulted in a 2-fold increase 5 4
'2
·E
~
3
.,x
/
'/
~ 2
o .>
'/
'/
/
/
/
10
/
--- --- --........
20
30 Age
Fig. 1.
40
Female
50
60
(years)
Effect of age and sex on maximum oxygen uptake.
above the bed rest levels to 50 mljkg/min. This was still far short of figures seen in the top endurance athletes. When we performed a cross-sectional population study in Australia in the 1960s we found that maximal oxygen uptake varied among different groups considerably, but fell short of the maximal oxygen uptake in the 70 to 80 mlj kg/min range recorded in the endurance-trained athletes (Sutton 1968).
1. The Oxygen Transport System In considering factors which limit maximal oxygen uptake, two separate schools of thought have emerged, one favouring a central limitation and the other favouring a peripheral limitation. 'Central' oxygen delivery depends on maximal cardiac output and maximal arterial oxygen content. The 'peripheral' extraction of the delivered oxygen is traditionally expressed as a-v02 difference. Combining these we have the circulatory ability to deliver and extract oxygen and V02max which is expressed as the Fick equation: V02max = Q X a-v 02. If one considers the individual components of oxygen transport from lungs to mitochondria this is diagrammatically represented in figure 2 (Sutton et al. 1988a) with the possible components contributing to V02max identified. This is also referred to as convective oxygen conductance. Saltin has demonstrated that while central cardiac output may be half as much again in the trained vs untrained person there is a considerably increased capacity for muscle blood flow of the same order in trained vs untrained individuals. A third model of V02max limitation is that determined by the diffusion capacity of the tissue and in quantitive terms the ability of oxygen to be transferred from the capillary to the mitochondria will depend on the diffusion gradient using Fick's Law of Diffusion we have V02max = D02 X PV02. The great respiratory physiologist, Hermann Rahn, compared and contrasted the 2 broad concepts of limitation to maximal oxygen uptake at a recent international hypoxia symposium just prior to his death (Rahn 1988). The setting was a debate between Bengt Saltin who argued from his studies
Limitations to Maximal Oxygen Uptake
Ventilation
\lE \lA/D.
Diffusion
Haemoglobin 02 affinity
129
Cardiac output Stroke volume Heart rate Blood pressure
Peripheral circulation Metabolism Muscle blood flow Substrate delivery Capillary density Muscle mass Diffusion (fibre size, number) 02 extraction Energy stores Myoglobin Mitochondria
Fig. 2. Oxygen transport: individual components of the oxygen transport chain. VE = ventilation; fusion relationship; SV = stroke volume; HR = heart rate; BP = blood pressure.
that the heart limited maximal oxygen uptake (Saltin 1988) and Peter Wagner who re-examined our Operation 11 data (Sutton et al. 1988b) and concluded that maximal peripheral diffusion capacity limited V02max (Wagner et al. 1992). Hermann Rahn states 'While at first these models may seem far apart, one dealing with cardiac output, the other with tissue diffusion, they actually complement each other'. Thus, rather than there being either a cardiac output limitation or a diffusion limitation a reduction in the former will result in a reduction in the latter.
2. The Lungs We now must consider possible limitations in oxygen transport. There is usually considerable reserve in the pulmonary system of the average sedentary person and thus the lungs do not normally limit exercise performance. Nevertheless, with increasing intensities of exercise in some trained individuals, the respiratory system may become limiting. Dempsey et al. (1984) identified a group of athletes who developed arterial oxygen desaturation on exercise. Although these athletes had a normal or low PC02 on exercise, it was higher than a comparable group of athletes who did not desaturate. Thus, they had a slightly reduced alveolar ventilation. Furthermore, they also had a wider alveolar to arterial oxygen tension difference resulting in an arterial oxygen saturation of 87% com-
VAJO. =
ventilation/per-
pared to 92% in the 'normal' athletes. If the arterial oxygen desaturation was prevented by having them exercise with mildly hyperoxic gases - inspired oxygen of 26% - the V02max increased from 70 to 75 ml/kg/min. The explanation for the slightly lower than expected alveolar ventilation has been postulated to be due to a ventilatory mechanical limit (Dempsey et al. 1990). This is certainly the case in elderly athletes, who will suffer the normal age-related loss of elastic lung recoil and a decrease in maximum expiratory flow. Contrary to popular belief there may be flow limitation in these athletes (fig. 3). There is an increase in end expiratory lung volume which in turn will limit inspiratory muscle function by shortening the inspiratory muscles, which will reduce maximum inspiratory pressure. With a greater metabolic requirement these muscles also become less efficient. With expiratory flow limitation the work of expiratory muscles will also increase. An additional problem is the possibility of significant airway narrowing at relatively high lung volumes when the gas exchanging surface of the lung may be reduced and result in an increased alveolar to arterial P02 difference. Could this increased (A-a) gradient represent transient pulmonary oedema?
3. Arterial Oxygen Saturation and Haemoglobin In normal trained and untrained individuals there is a considerable overlap in haemoglobin and
Sports Medicine 13 (2) 1992
130
10 8 6
= = =
PA02 110mm Hg Pa02 84mm Hg PaC02 34mm Hg
=
VDfVT 0.27 84 L/min VA
4
U 2 Q)
VD
-... :::!. 0 Cl)
3:
0
u::
= = 32 L/min
40 32
0-
2
:I:
16
'"
E
~
~ ::l
V
2 TL
2
Cl) Cl)
Q)
0. Oj
:;
4
Q)
c::
6
i\ i: \.... (Pmaxe) :. ...
"
8 0
4:
-8
CC
3:
RV
2
-16 -24 -32
8
-72
10
Volume (L)
Volume (L)
Fig. 3. Mean ventilatory response to progressive exercise in 8 young endurance athletes. Tidal flow (on the left) and pressure (on the right) volume loops (solid lines) are plotted from rest through maximal exercise. The flow: volume loops are plotted within the pre- (solid) and postexercise (dashed) maximal volitional flow: volume loops relative to a measured EELV. The tidal pressure; volume loops are plotted relative to the maximal effective pressures on expiration and the capacity for pressure generation on inspiration (V02max = 74 ± I ml/kgfmin (range 66 to 80). Also shown are relevant maximal exercise blood gas and ventilatory parameters. Because of the much greater YE demand in the young athletes, they approach a level of mechanical limitation similar to that noted in the older relatively fit adult during maximal exercise at a much lower V02max. Reproduced from Dempsey and 10hnson (199\) with permission of the authors and editors. PA02 = alveolar oxygen pressure; Pa02 = arterial oxygen pressure; PaC02 = arterial carbon dioxide pressure; VD = dead space ventilation; VT = tidal volume; YA = alveolar ventilation; TLC = total lung capacity; CC = closing capacity; RV = residual volume; P maxe = maximum effective pressure on expiration; Pcapi = capacity for inspiratory muscle pressure generation.
arterial oxygen saturation and therefore also overlap in the magnitude of the arterial oxygen content (table I). Arterial oxygen content is the product of arterial oxygen saturation and haemoglobin. Changing blood volume by hypervolaemia will increase work, but this is primarily because of an increase maximum cardiac output increasing venous return rather than changes in total oxygen carrying capacity of the blood.
4. Cardiovascular Function Can the heart limit exercise performance? Maximum cardiac output is determined by the product of stroke volume and heart rate. Maximum heart rate decreases fairly linearly with age at about the rate of two-thirds of a beat per year of age and is not dramatically affected by training and therefore cardiovascular fitness. Thus, stroke
Table I. Mean value and range for oxygen saturation (802), haemoglobin (Hb) and arterial oxygen content (Ca02) during exhaustive work in studies of young men with different degrees of physical training. Data are from Ekblom (1969), Ekblom and Hermansen (1968) and 8altin et al. (1976) ",,02max (ml/kg/min Young, sedentary (n = 18) Young, trained (n = 18) Endurance athletes (n = 8)
38 52 74
802 (%)
94 (92-96) 94.5 (92-96) 93 (89-95)
Hb (g/L)
Ca02 (mill)
158 (149-169) 159 (151-163) 151 (147-162)
200 (188-218) 201 (191-208) 188 (179-204)
131
Limitations to Maximal Oxygen Uptake
/
180
/
/
/e
Endurance / athletes / ~ e
E
-; 140 E ::J
(5
/
> ID .:.:.
/
/
/
e 100
/',/
/
/'
/'
/'
/'
/'/'
/l:Trained /' Sedentary
U5
factor in determining maximal oxygen uptake was the ability to reduce peripheral resistance. The importance of peripheral resistance was again brought into prominence in a study of Secher et al. (1977) who added arm to leg exercise. While cardiac output slightly increased, leg blood flow was reduced in the presence of unaltered blood pressure suggesting an important regulatory link between the central and peripheral circulation.
/'
6. Muscle Blood Flow
Inactive
60
~~'~i--~~i--~~i--'--'i----
600
800
1000
1200
Heart volume (m I) Fig. 4. The relationship between aerobic work capacity and heart volume. The mean values with ± I SO are from a study of healthy men (slightly modified) and the mean values for specific groups. Reproduced from Saltin (1990) with permission of the authors and editors.
volume is the prime determinant of the difference in maximum cardiac output between individuals. Most studies have shown a higher stroke volume in maximal exercise as well as submaximal exercise in the trained vs untrained individuals (fig. 4). In the Guytonian principle of the heart, the pumping blood returned to it is probably a crucial factor and this is further substantiated by the work of Stray-Gundersen et al. (1986) who demonstrated an increase of 20 to 25% in maximum stroke volume following pericardectomy in dogs and consequently a similar magnitude of increase in maximal oxygen uptake.
5. Distribution
0/ Cardiac
Output
Final determination of oxygen delivery is the peripheral extraction of oxygen. Early in the training regimen the maximum arteriovenous oxygen difference (a-v02) is achieved. It is thought that with further training the amount of cardiac output perfusing the nonexercising tissue is reduced and only the brain and to some extent the skin are well perfused and the splanchnic circulation in particular is reduced (Rowell et al. 1968). The importance of vascular conductance was highlighted by Clausen (1976) when he concluded that a critical
The studies alluded to above by Secher were interpreted to indicate that the addition of an extra vascular bed by adding arm to leg exercise exceeded the maximal central flow. In order to maintain blood pressure with the addition of an extra vascular bed some degree of peripheral vascular constriction was necessary and this resulted in a reduced leg blood flow. There are a variety of peripheral factors that determine vascular tone, none more important than the sympathetic nervous system. It is a balance between the sympathetically mediated noradrenaline (norepinephrine) vasoconstrictor activity and local vasodilatation that determine the final tone in the smooth muscle of the arterioles, the site of blood pressure regulation. This scheme was suggested by Rowell (1986) with local factors controlling vasodilatation in the supine position and centrally mediated sympathetic nervous sytem activity in the form of adrenaline (epinephrine) interacting. This model is consistent with all forms of exercise and with both the small muscle group and large muscle group exercise. The model requires strict control of vasomotor tone for all blood vessels, whether they be those in contracting muscle tissue or the noncontracting tissue, e.g. vessels supplying the skin. In the latter, the role of vasodilatation and thermoregulation are particularly important (fig. 5). In this setting Rowell has indicated that under pressure a compromise may be necessary and a hierarchy has been established with the maintenance of blood pressure dominating that of thermoregulation. The capacity of the peripheral circulation is sig-
Sports Medicine 13 (2) 1992
132
Maximal 1-legged exercise 90
MAP(mm~ Blood flow 150 ml/100g/min
Maximal whole body exercise MAP (mm Hg): 100
60 Blood flow 80-90 ml/100g/min
Fig. 5. A schematic illustration of the hypothesis of the larger vessels feeding the exercising muscles to be the target for vasconstriction during whole body exercise. When exercising with a small muscle group, no constriction is needed (upper), but when a large fraction of the muscle mass is engaged in exercise, muscle blood flow has to be reduced. This could be accomplished by sympathetically mediated vasoconstrictor activity to arterial vessels outside the muscle and 'out of reach' of vasodilator substances within the muscle. Reproduced from Saltin (1988).
nificantly greater than occurs under physiological circumstances with 2-legged exercise; furthermore, there is incomplete oxygen extraction even at maximum exercise, an argument which has been used to suggest that the periphery never limits V02max (conversely it has been argued that the periphery may be limiting because oxygen can't be extracted maximally). The reasons for incomplete extraction are not well understood but the likelihood of some degree of AV shunting in human muscle must be considered where there is a mismatch between the blood flow and the muscle fibres. More likely, however, is the fact that there is an admixture of blood from noncontracting tissue. Finally, of course, from a logical point of view it is vital to have some head of pressure for oxygen flux to occur along the length of muscle capillary and therefore venous P02 could never be zero. The time for blood flow and therefore oxygen transit through a capillary network (mean transit time) is also important and will decrease as arteriovenous oxygen tension difference increases. It is greatest in small muscle group
exercise, for instance I-leg knee extension. With increasing intensity of exercise there is an increased capillary network recruited until finally there is a sharp drop in mean transit time which can be demonstrated with I-leg knee extension exercise, but not when 2-leg maximal exercise occurs.
7. Conclusion Maximal oxygen uptake depends on the optimal linkage between all components of the oxygen transporting system from the lungs to the capillary network. Of all the determinants of maximal oxygen uptake which change with physical training the cardiovascular system is most adaptable and within that system it is the maximum increases in stroke volume which are most important.
References Clausen JP. Circulatory adjustments to dynamic exercise and effect of physical training in normal subjects and in patients with coronary artery disease. Progress in Cardiovascular Disease 18 '(6): 459-495, 1976 Dempsey JA, Hanson P, Henderson K. Exercise-induced arterial hypoxemia in healthy humans at sea-level. Journal of Physiology (London) 355: 161-175, 1984 Dempsey JA, Johnson BD. Demand vs capacity in the healthy pulmonary system. In Sutton JR & Balnave R. (Eds) Cardiovascular and respiratory responses to exercise in health and disease, Cumberland College of Health Sciences, Sydney, 1991 Dempsey JA, Powers SK, Gledhill N. Discussion: cardiovascular and pulmonary adaptation to physical activity. In Bouchard C et al. (Eds) Exercise, fitness and health pp. 205-213, Human Kinetics Books, Champaign, 1990 Ekblom B. Effect of physical training on oxygen transport system in man. Acta Physiologica Scandinavica (Suppl. 328): 5-45, 1969 Ekblom B, Hermansen L. Cardiac output in athletes. Journal of Applied Physiology 25: 619-625, 1968 Rahn H. Maximal oxygen uptake: central or peripheral limitation? In Sutton JR et al. (Eds) Hypoxia: the tolerable limits, pp. 35-37, SUITon JR, et al. Benchmark Press, Indianapolis 1988 Robinson, S, Edwards HT, Dill DB. New records in human power. Science 85: 409-410, 1937 Rowell LB, Brengelmann GL, Blackmon JR, Twiss RD, Kusumi F. Splanchnic blood flow and metabolism in heat-stressed humans. Journal of Applied Physiology 24: 475-484, 1968 Rowell LB. Human circulation regulation during physical stress, Oxford University Press, New York, 1986 Saltin B, Blomqvist G, Mitchell JH, Johnson Jr RL, Wildenthal K, et al. Response to exercise after bed rest and after training. Circulation 38 (7): 1-78, 1968 Saltin B. Limitations to performance at altitude. In Sutton JR, et al. (Eds) Hypoxia: the tolerable limits pp. 9-31, Benchmark Press, Indianapolis, 1988 Saltin B, Nazar K, Costill PL, Stein E, Jansson E, et al. The nature of the training response; peripheral and central adaptations to
Limitations to Maximal Oxygen Uptake
one-legged exercise. Acta Physiologica Scandinavica 96: 289305, 1976 Secher NH, Clausen JP, Klausen K, Nore I, Trap-Jensen J. Central and regional circulatory effects of adding arm exercise to leg exercise. Acta Physiologica Scandinavica 100: 288-297, 1977 Stray-Gundersen J, Musch TI, Haidet GC, Swain DP, Ordway GA, et al. The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circulation Research 58: 523-530, 1986 Sulton JR. Exercise-fitness. In Nash & Lazarus L (Eds) Contribution to medicine and surgery, pp. 84-86, EJ Dwyer, Sydney, 1968 Sulton JR, Houston CS, Cymerman C. Hypoxia: the tolerable limits. In Sulton JR, et al. (Eds) Operation Everest 11. pp. 36, Benchmark Press, Indianapolis, 1988a
133
Sulton JR, Reeves JT, Wagner PO, Groves BM, Cymerman A, et al. Operation 11: Oxygen transport during exercise at extreme simulated altitude. Journal of Applied Physiology 64: 1309-1321, 1988b Wagner PO, Reeves JT, Sulton JR, Groves BM, Cymerman, et al. Operation Everest 11: Evidence for peripheral tissue diffusion limitation of maximal oxygen uptake. Journal of Applied Physiology, in press, 1992
Correspondence and reprints: Prof. Jahn Sultan, Cumberland College of Health Sciences, East St,' Lidcombe, NSW 2141, Australia.
------~------~
Sports Medicine 13 (2): 127-133, 1992 0112-1642/92/0002-0127/$03.50/0 © Adis International Limited. All rights reserved. SPOll19
Limitations to Maximal Oxygen Uptake 1 John R. Sultan Faculty of Health Sciences, University of Sydney, Sydney, New South Wales, Australia
Contents 127 128 129 129 J30 13 J 131 132
Summary
Summary 1. The Oxygen Transport System 2. The Lungs 3. Arterial Oxygen Saturation and Haemoglobin 4. Cardiovascular Function 5. Distribution of Cardiac Output 6. Muscle Blood Flow 7. Conclusion
An increase in exercise capacity depends on the magnitude of increase in maximum aerobic capacity. Central and peripheral factors may limit oxygen uptake. Central oxygen delivery depends on cardiac output and maximal arterial oxygen content. Peripheral extraction of the delivered oxygen is expressed as a-v 02. With increasing intensities of exercise, the respiratory system may become limiting in some trained individuals. Most studies have shown a higher stroke volume in maximal as well as submaximal exercise in the trained vs untrained individuals. A variety of peripheral factors determine vascular tone. Maximal oxygen uptake depends on all components of the oxygen transporting system, but stroke volume appears to be the prime determinant in the trained subject. At maximum exercise the capacity of the muscle capillary network is never reached.
The ability of humans to excel in exercise of significant duration depends on aerobic metabolism. Those with the highest aerobic metabolism will in general be able to perform best, although, of course, additional factors will determine who crosses the finish line first. Furthermore, following an aerobic training programme the magnitude of the increase in exercise capacity will depend on the 1 This article was presented at a Symposium on Fatigue in Sport and Exercise in November 1990 and updated by the author for publication in Sports Medicine.
magnitude of increase in maximum aerobic capacity (V02max). This is the criterion which is used as the 'gold standard' for assessing endurance performance potential. Resting oxygen uptake is similar in trained and untrained individuals, however, there is at least a 2- to 3-fold greater maximal oxygen uptake in the trained vs the untrained individual. In this paper I examine the magnitude of increases in maximal oxygen uptake from rest to exercise in the trained vs untrained individuals, the capacity of each COffi-
Sports Medicine 13 (2) 1992
128
ponent of oxygen transport in determining maximal oxygen uptake and the differences in limitation to maximal uptake in the trained compared with the untrained. The study by Robinson et al. (1938) was the first to identify maximal oxygen uptake as an important determinant of exercise performance. In that study they demonstrated that in men maximal oxygen uptake peaked around about 20 years of age and thereafter decreased. Since that time studies have included men and women, but the overall observation remains, that age by itself will result in a decreased maximal oxygen uptake. Furthermore, women have a lower V02max than men but the difference decreases with increasing age after adolescence (fig. 1). Another crucial factor which determines cardiorespiratory fitness (V02max) is heredity; are athletes born or can they be made? The classic bed rest studies of Saltin and colleagues (1968) contain among the most compelling data to suggest that training can produce marked increases in maximal oxygen uptake (V02max), that bed rest will decrease V02max significantly and that subjects are not able to be trained to levels comparable to the highest seen in the top endurance athletes. In the 1968 study Saltin and colleagues found that 3 weeks of bed rest caused V02max to fall to two-thirds of its control level (25 mljkg/min); however, several months of training resulted in a 2-fold increase 5 4
'2
·E
~
3
.,x
/
'/
~ 2
o .>
'/
'/
/
/
/
10
/
--- --- --........
20
30 Age
Fig. 1.
40
Female
50
60
(years)
Effect of age and sex on maximum oxygen uptake.
above the bed rest levels to 50 mljkg/min. This was still far short of figures seen in the top endurance athletes. When we performed a cross-sectional population study in Australia in the 1960s we found that maximal oxygen uptake varied among different groups considerably, but fell short of the maximal oxygen uptake in the 70 to 80 mlj kg/min range recorded in the endurance-trained athletes (Sutton 1968).
1. The Oxygen Transport System In considering factors which limit maximal oxygen uptake, two separate schools of thought have emerged, one favouring a central limitation and the other favouring a peripheral limitation. 'Central' oxygen delivery depends on maximal cardiac output and maximal arterial oxygen content. The 'peripheral' extraction of the delivered oxygen is traditionally expressed as a-v02 difference. Combining these we have the circulatory ability to deliver and extract oxygen and V02max which is expressed as the Fick equation: V02max = Q X a-v 02. If one considers the individual components of oxygen transport from lungs to mitochondria this is diagrammatically represented in figure 2 (Sutton et al. 1988a) with the possible components contributing to V02max identified. This is also referred to as convective oxygen conductance. Saltin has demonstrated that while central cardiac output may be half as much again in the trained vs untrained person there is a considerably increased capacity for muscle blood flow of the same order in trained vs untrained individuals. A third model of V02max limitation is that determined by the diffusion capacity of the tissue and in quantitive terms the ability of oxygen to be transferred from the capillary to the mitochondria will depend on the diffusion gradient using Fick's Law of Diffusion we have V02max = D02 X PV02. The great respiratory physiologist, Hermann Rahn, compared and contrasted the 2 broad concepts of limitation to maximal oxygen uptake at a recent international hypoxia symposium just prior to his death (Rahn 1988). The setting was a debate between Bengt Saltin who argued from his studies
Limitations to Maximal Oxygen Uptake
Ventilation
\lE \lA/D.
Diffusion
Haemoglobin 02 affinity
129
Cardiac output Stroke volume Heart rate Blood pressure
Peripheral circulation Metabolism Muscle blood flow Substrate delivery Capillary density Muscle mass Diffusion (fibre size, number) 02 extraction Energy stores Myoglobin Mitochondria
Fig. 2. Oxygen transport: individual components of the oxygen transport chain. VE = ventilation; fusion relationship; SV = stroke volume; HR = heart rate; BP = blood pressure.
that the heart limited maximal oxygen uptake (Saltin 1988) and Peter Wagner who re-examined our Operation 11 data (Sutton et al. 1988b) and concluded that maximal peripheral diffusion capacity limited V02max (Wagner et al. 1992). Hermann Rahn states 'While at first these models may seem far apart, one dealing with cardiac output, the other with tissue diffusion, they actually complement each other'. Thus, rather than there being either a cardiac output limitation or a diffusion limitation a reduction in the former will result in a reduction in the latter.
2. The Lungs We now must consider possible limitations in oxygen transport. There is usually considerable reserve in the pulmonary system of the average sedentary person and thus the lungs do not normally limit exercise performance. Nevertheless, with increasing intensities of exercise in some trained individuals, the respiratory system may become limiting. Dempsey et al. (1984) identified a group of athletes who developed arterial oxygen desaturation on exercise. Although these athletes had a normal or low PC02 on exercise, it was higher than a comparable group of athletes who did not desaturate. Thus, they had a slightly reduced alveolar ventilation. Furthermore, they also had a wider alveolar to arterial oxygen tension difference resulting in an arterial oxygen saturation of 87% com-
VAJO. =
ventilation/per-
pared to 92% in the 'normal' athletes. If the arterial oxygen desaturation was prevented by having them exercise with mildly hyperoxic gases - inspired oxygen of 26% - the V02max increased from 70 to 75 ml/kg/min. The explanation for the slightly lower than expected alveolar ventilation has been postulated to be due to a ventilatory mechanical limit (Dempsey et al. 1990). This is certainly the case in elderly athletes, who will suffer the normal age-related loss of elastic lung recoil and a decrease in maximum expiratory flow. Contrary to popular belief there may be flow limitation in these athletes (fig. 3). There is an increase in end expiratory lung volume which in turn will limit inspiratory muscle function by shortening the inspiratory muscles, which will reduce maximum inspiratory pressure. With a greater metabolic requirement these muscles also become less efficient. With expiratory flow limitation the work of expiratory muscles will also increase. An additional problem is the possibility of significant airway narrowing at relatively high lung volumes when the gas exchanging surface of the lung may be reduced and result in an increased alveolar to arterial P02 difference. Could this increased (A-a) gradient represent transient pulmonary oedema?
3. Arterial Oxygen Saturation and Haemoglobin In normal trained and untrained individuals there is a considerable overlap in haemoglobin and
Sports Medicine 13 (2) 1992
130
10 8 6
= = =
PA02 110mm Hg Pa02 84mm Hg PaC02 34mm Hg
=
VDfVT 0.27 84 L/min VA
4
U 2 Q)
VD
-... :::!. 0 Cl)
3:
0
u::
= = 32 L/min
40 32
0-
2
:I:
16
'"
E
~
~ ::l
V
2 TL
2
Cl) Cl)
Q)
0. Oj
:;
4
Q)
c::
6
i\ i: \.... (Pmaxe) :. ...
"
8 0
4:
-8
CC
3:
RV
2
-16 -24 -32
8
-72
10
Volume (L)
Volume (L)
Fig. 3. Mean ventilatory response to progressive exercise in 8 young endurance athletes. Tidal flow (on the left) and pressure (on the right) volume loops (solid lines) are plotted from rest through maximal exercise. The flow: volume loops are plotted within the pre- (solid) and postexercise (dashed) maximal volitional flow: volume loops relative to a measured EELV. The tidal pressure; volume loops are plotted relative to the maximal effective pressures on expiration and the capacity for pressure generation on inspiration (V02max = 74 ± I ml/kgfmin (range 66 to 80). Also shown are relevant maximal exercise blood gas and ventilatory parameters. Because of the much greater YE demand in the young athletes, they approach a level of mechanical limitation similar to that noted in the older relatively fit adult during maximal exercise at a much lower V02max. Reproduced from Dempsey and 10hnson (199\) with permission of the authors and editors. PA02 = alveolar oxygen pressure; Pa02 = arterial oxygen pressure; PaC02 = arterial carbon dioxide pressure; VD = dead space ventilation; VT = tidal volume; YA = alveolar ventilation; TLC = total lung capacity; CC = closing capacity; RV = residual volume; P maxe = maximum effective pressure on expiration; Pcapi = capacity for inspiratory muscle pressure generation.
arterial oxygen saturation and therefore also overlap in the magnitude of the arterial oxygen content (table I). Arterial oxygen content is the product of arterial oxygen saturation and haemoglobin. Changing blood volume by hypervolaemia will increase work, but this is primarily because of an increase maximum cardiac output increasing venous return rather than changes in total oxygen carrying capacity of the blood.
4. Cardiovascular Function Can the heart limit exercise performance? Maximum cardiac output is determined by the product of stroke volume and heart rate. Maximum heart rate decreases fairly linearly with age at about the rate of two-thirds of a beat per year of age and is not dramatically affected by training and therefore cardiovascular fitness. Thus, stroke
Table I. Mean value and range for oxygen saturation (802), haemoglobin (Hb) and arterial oxygen content (Ca02) during exhaustive work in studies of young men with different degrees of physical training. Data are from Ekblom (1969), Ekblom and Hermansen (1968) and 8altin et al. (1976) ",,02max (ml/kg/min Young, sedentary (n = 18) Young, trained (n = 18) Endurance athletes (n = 8)
38 52 74
802 (%)
94 (92-96) 94.5 (92-96) 93 (89-95)
Hb (g/L)
Ca02 (mill)
158 (149-169) 159 (151-163) 151 (147-162)
200 (188-218) 201 (191-208) 188 (179-204)
131
Limitations to Maximal Oxygen Uptake
/
180
/
/
/e
Endurance / athletes / ~ e
E
-; 140 E ::J
(5
/
> ID .:.:.
/
/
/
e 100
/',/
/
/'
/'
/'
/'
/'/'
/l:Trained /' Sedentary
U5
factor in determining maximal oxygen uptake was the ability to reduce peripheral resistance. The importance of peripheral resistance was again brought into prominence in a study of Secher et al. (1977) who added arm to leg exercise. While cardiac output slightly increased, leg blood flow was reduced in the presence of unaltered blood pressure suggesting an important regulatory link between the central and peripheral circulation.
/'
6. Muscle Blood Flow
Inactive
60
~~'~i--~~i--~~i--'--'i----
600
800
1000
1200
Heart volume (m I) Fig. 4. The relationship between aerobic work capacity and heart volume. The mean values with ± I SO are from a study of healthy men (slightly modified) and the mean values for specific groups. Reproduced from Saltin (1990) with permission of the authors and editors.
volume is the prime determinant of the difference in maximum cardiac output between individuals. Most studies have shown a higher stroke volume in maximal exercise as well as submaximal exercise in the trained vs untrained individuals (fig. 4). In the Guytonian principle of the heart, the pumping blood returned to it is probably a crucial factor and this is further substantiated by the work of Stray-Gundersen et al. (1986) who demonstrated an increase of 20 to 25% in maximum stroke volume following pericardectomy in dogs and consequently a similar magnitude of increase in maximal oxygen uptake.
5. Distribution
0/ Cardiac
Output
Final determination of oxygen delivery is the peripheral extraction of oxygen. Early in the training regimen the maximum arteriovenous oxygen difference (a-v02) is achieved. It is thought that with further training the amount of cardiac output perfusing the nonexercising tissue is reduced and only the brain and to some extent the skin are well perfused and the splanchnic circulation in particular is reduced (Rowell et al. 1968). The importance of vascular conductance was highlighted by Clausen (1976) when he concluded that a critical
The studies alluded to above by Secher were interpreted to indicate that the addition of an extra vascular bed by adding arm to leg exercise exceeded the maximal central flow. In order to maintain blood pressure with the addition of an extra vascular bed some degree of peripheral vascular constriction was necessary and this resulted in a reduced leg blood flow. There are a variety of peripheral factors that determine vascular tone, none more important than the sympathetic nervous system. It is a balance between the sympathetically mediated noradrenaline (norepinephrine) vasoconstrictor activity and local vasodilatation that determine the final tone in the smooth muscle of the arterioles, the site of blood pressure regulation. This scheme was suggested by Rowell (1986) with local factors controlling vasodilatation in the supine position and centrally mediated sympathetic nervous sytem activity in the form of adrenaline (epinephrine) interacting. This model is consistent with all forms of exercise and with both the small muscle group and large muscle group exercise. The model requires strict control of vasomotor tone for all blood vessels, whether they be those in contracting muscle tissue or the noncontracting tissue, e.g. vessels supplying the skin. In the latter, the role of vasodilatation and thermoregulation are particularly important (fig. 5). In this setting Rowell has indicated that under pressure a compromise may be necessary and a hierarchy has been established with the maintenance of blood pressure dominating that of thermoregulation. The capacity of the peripheral circulation is sig-
Sports Medicine 13 (2) 1992
132
Maximal 1-legged exercise 90
MAP(mm~ Blood flow 150 ml/100g/min
Maximal whole body exercise MAP (mm Hg): 100
60 Blood flow 80-90 ml/100g/min
Fig. 5. A schematic illustration of the hypothesis of the larger vessels feeding the exercising muscles to be the target for vasconstriction during whole body exercise. When exercising with a small muscle group, no constriction is needed (upper), but when a large fraction of the muscle mass is engaged in exercise, muscle blood flow has to be reduced. This could be accomplished by sympathetically mediated vasoconstrictor activity to arterial vessels outside the muscle and 'out of reach' of vasodilator substances within the muscle. Reproduced from Saltin (1988).
nificantly greater than occurs under physiological circumstances with 2-legged exercise; furthermore, there is incomplete oxygen extraction even at maximum exercise, an argument which has been used to suggest that the periphery never limits V02max (conversely it has been argued that the periphery may be limiting because oxygen can't be extracted maximally). The reasons for incomplete extraction are not well understood but the likelihood of some degree of AV shunting in human muscle must be considered where there is a mismatch between the blood flow and the muscle fibres. More likely, however, is the fact that there is an admixture of blood from noncontracting tissue. Finally, of course, from a logical point of view it is vital to have some head of pressure for oxygen flux to occur along the length of muscle capillary and therefore venous P02 could never be zero. The time for blood flow and therefore oxygen transit through a capillary network (mean transit time) is also important and will decrease as arteriovenous oxygen tension difference increases. It is greatest in small muscle group
exercise, for instance I-leg knee extension. With increasing intensity of exercise there is an increased capillary network recruited until finally there is a sharp drop in mean transit time which can be demonstrated with I-leg knee extension exercise, but not when 2-leg maximal exercise occurs.
7. Conclusion Maximal oxygen uptake depends on the optimal linkage between all components of the oxygen transporting system from the lungs to the capillary network. Of all the determinants of maximal oxygen uptake which change with physical training the cardiovascular system is most adaptable and within that system it is the maximum increases in stroke volume which are most important.
References Clausen JP. Circulatory adjustments to dynamic exercise and effect of physical training in normal subjects and in patients with coronary artery disease. Progress in Cardiovascular Disease 18 '(6): 459-495, 1976 Dempsey JA, Hanson P, Henderson K. Exercise-induced arterial hypoxemia in healthy humans at sea-level. Journal of Physiology (London) 355: 161-175, 1984 Dempsey JA, Johnson BD. Demand vs capacity in the healthy pulmonary system. In Sutton JR & Balnave R. (Eds) Cardiovascular and respiratory responses to exercise in health and disease, Cumberland College of Health Sciences, Sydney, 1991 Dempsey JA, Powers SK, Gledhill N. Discussion: cardiovascular and pulmonary adaptation to physical activity. In Bouchard C et al. (Eds) Exercise, fitness and health pp. 205-213, Human Kinetics Books, Champaign, 1990 Ekblom B. Effect of physical training on oxygen transport system in man. Acta Physiologica Scandinavica (Suppl. 328): 5-45, 1969 Ekblom B, Hermansen L. Cardiac output in athletes. Journal of Applied Physiology 25: 619-625, 1968 Rahn H. Maximal oxygen uptake: central or peripheral limitation? In Sutton JR et al. (Eds) Hypoxia: the tolerable limits, pp. 35-37, SUITon JR, et al. Benchmark Press, Indianapolis 1988 Robinson, S, Edwards HT, Dill DB. New records in human power. Science 85: 409-410, 1937 Rowell LB, Brengelmann GL, Blackmon JR, Twiss RD, Kusumi F. Splanchnic blood flow and metabolism in heat-stressed humans. Journal of Applied Physiology 24: 475-484, 1968 Rowell LB. Human circulation regulation during physical stress, Oxford University Press, New York, 1986 Saltin B, Blomqvist G, Mitchell JH, Johnson Jr RL, Wildenthal K, et al. Response to exercise after bed rest and after training. Circulation 38 (7): 1-78, 1968 Saltin B. Limitations to performance at altitude. In Sutton JR, et al. (Eds) Hypoxia: the tolerable limits pp. 9-31, Benchmark Press, Indianapolis, 1988 Saltin B, Nazar K, Costill PL, Stein E, Jansson E, et al. The nature of the training response; peripheral and central adaptations to
Limitations to Maximal Oxygen Uptake
one-legged exercise. Acta Physiologica Scandinavica 96: 289305, 1976 Secher NH, Clausen JP, Klausen K, Nore I, Trap-Jensen J. Central and regional circulatory effects of adding arm exercise to leg exercise. Acta Physiologica Scandinavica 100: 288-297, 1977 Stray-Gundersen J, Musch TI, Haidet GC, Swain DP, Ordway GA, et al. The effect of pericardiectomy on maximal oxygen consumption and maximal cardiac output in untrained dogs. Circulation Research 58: 523-530, 1986 Sulton JR. Exercise-fitness. In Nash & Lazarus L (Eds) Contribution to medicine and surgery, pp. 84-86, EJ Dwyer, Sydney, 1968 Sulton JR, Houston CS, Cymerman C. Hypoxia: the tolerable limits. In Sulton JR, et al. (Eds) Operation Everest 11. pp. 36, Benchmark Press, Indianapolis, 1988a
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Sulton JR, Reeves JT, Wagner PO, Groves BM, Cymerman A, et al. Operation 11: Oxygen transport during exercise at extreme simulated altitude. Journal of Applied Physiology 64: 1309-1321, 1988b Wagner PO, Reeves JT, Sulton JR, Groves BM, Cymerman, et al. Operation Everest 11: Evidence for peripheral tissue diffusion limitation of maximal oxygen uptake. Journal of Applied Physiology, in press, 1992
Correspondence and reprints: Prof. Jahn Sultan, Cumberland College of Health Sciences, East St,' Lidcombe, NSW 2141, Australia.
