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J Appl Physiol 97: 165-172, 2004. First published March 5, 2004; doi:10.1152/japplphysiol.01179.2003
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Effect of age on O2 uptake kinetics and the adaptation of muscle deoxygenation at the onset of moderate-intensity cycling exercise

Darren S. DeLorey,1,2 John M. Kowalchuk,1,2,3 and Donald H. Paterson1,2

1Canadian Centre for Activity and Aging, 2School of Kinesiology, and 3Department of Physiology, The University of Western Ontario, London, Ontario, Canada N6A 3K7

Submitted 4 November 2003 ; accepted in final form 4 March 2004


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Phase 2 pulmonary O2 uptake (O2p) kinetics are slowed with aging. To examine the effect of aging on the adaptation of O2p and deoxygenation of the vastus lateralis muscle at the onset of moderate-intensity constant-load cycling exercise, young (Y) (n = 6; 25 ± 3 yr) and older (O) (n = 6; 68 ± 3 yr) adults performed repeated transitions from 20 W to work rates corresponding to moderate-intensity (80% estimated lactate threshold) exercise. Breath-by-breath O2p was measured by mass spectrometer and volume turbine. Deoxy (HHb)-, oxy-, and total Hb and/or myoglobin were determined by near-infrared spectroscopy (Hamamatsu NIRO-300). O2p data were filtered, interpolated to 1 s, and averaged to 5-s bins. HHb data were filtered and averaged to 5-s bins. O2p data were fit with a monoexponential model for phase 2, and HHb data were analyzed to determine the time delay from exercise onset to the start of an increase in HHb and thereafter were fit with a single-component exponential model. The phase 2 time constant for O2p was slower (P < 0.01) in O (Y: 26 ± 7 s; O: 42 ± 9 s), whereas the delay before an increase in HHb (Y: 12 ± 2 s; O: 11 ± 1 s) and the time constant for HHb after the time delay (Y: 13 ± 10 s; O: 9 ± 3 s) were similar in Y and O. However, the increase in HHb for a given increase in O2p (Y: 7 ± 2 µM·l–1·min–1; O: 13 ± 4 µM·l–1·min–1) was greater (P < 0.01) in O compared with Y. The slower O2p kinetics in O compared with Y adults was accompanied by a slower increase of local muscle blood flow and O2 delivery discerned from a faster and greater muscle deoxygenation relative to O2p in O.

near-infrared spectroscopy; muscle O2 utilization

PHASE 2 PULMONARY O2 uptake (O2p) kinetics are slowed in older compared with younger adults (1, 6, 12, 16). Whether the slower O2p kinetics are due to a slower delivery of O2 to working muscle or a delayed activation or slowing of the metabolic processes of oxidative phosphorylation remains unclear. The observation of slower heart rate (HR) kinetics at the onset of exercise in older adults suggests that central blood flow adaptations may contribute to an O2 delivery limitation in older adults (6, 12, 20, 46). Peripheral blood flow distribution may also contribute to an O2 delivery limitation (44, 45); however, Mizuno et al. (37) recently reported in healthy young adults that perfusion was well matched to metabolism in five areas of the quadriceps muscles during rest and recovery from exhaustive exercise. Evidence in support of a potential O2 delivery limitation in older adults includes: 1) a lower resting cardiac output () (41), and lower exercise relative to O2p (35, 51); 2) a lower resting limb blood flow and limb vascular conductance (21–23); 3) lower leg blood flow during submaximal exercise (40, 42, 53); 4) impaired ability to redistribute blood flow from the splanchnic and renal circulations to muscle during exercise (28); and 5) decrements in endothelium-dependent vasodilation (39, 50) and myogenic responsiveness (38), which have implications for blood flow distribution. Thus impaired blood flow and blood flow distribution (because of diminished local vascular control) may result in a reduced O2 delivery and greater perfusion-metabolism mismatching during the transition to exercise in older compared with younger adults and may play a role in the slowed adaptation of O2p observed in older adults.

Information on the adaptation of leg blood flow and O2p during the exercise transient in older adults is limited. After the onset of heavy-intensity single-leg knee extension exercise, the adaptation of femoral artery mean blood velocity (a reflection of limb blood flow) was faster than that of O2p, suggesting that bulk O2 delivery to the leg adapted at a faster O2p in older adults (7). Also, in the study of Bell et al. (7), exercise training resulted in a speeding of O2p kinetics without a change in mean blood velocity kinetics or muscle capillarization, whereas muscle oxidative capacity was increased (as reflected by an increase in maximal citrate synthase activity), suggesting that adaptations of muscle oxidative metabolism may have been responsible for the improved O2p kinetics.

Conflicting evidence exists regarding the maintenance of muscle oxidative capacity with aging. Conley et al. (15) reported that older compared with younger subjects had a 50% lower oxidative capacity per volume of quadriceps muscle attributable to both a decrease in mitochondrial volume and a lower oxidative capacity of the mitochondria (15). Others (29, 43) have reported no decline in skeletal muscle oxidative capacity with advancing age. Of importance to the study of O2p kinetics is whether a decline in maximal muscle oxidative capacity with aging affects the adaptation and rate of O2 utilization at the onset of submaximal, moderate-intensity exercise in older adults. Chilibeck et al. (11) reported that, at the onset of plantar flexion exercise performed in the semirecumbent position, the kinetics of phosphocreatine breakdown and increase of O2p were similar in older and younger adults, suggesting that the ability to utilize O2 during the exercise transient was not affected by aging, at least with exercise performed with a small muscle mass accustomed to everyday activity. Thus whether the slowed O2p kinetics observed in older adults during whole body large muscle mass exercise such as cycling are due to an inability to increase muscle blood flow and O2 delivery and/or a reduced capacity to utilize O2 has not been clearly established.

The technique of near-infrared spectroscopy (NIRS) allows the noninvasive and continuous monitoring of relative concentration changes in deoxy (HHb)-, oxy (HbO2)-, and total (Hbtot) Hb and/or myoglobin in the microvasculature (small arterioles, capillaries, and venules) of the muscle (8). O2 extraction and Hb deoxygenation at the onset of exercise are influenced by the time course and magnitude of increase in local metabolic rate and local muscle blood flow. Therefore, the NIRS-derived HHb signal reflects the regional balance between O2 delivery and O2 utilization at the site of O2 exchange (i.e., the microvasculature of the volume of muscle being interrogated by NIRS) (19). An additional advantage of NIRS technology is that there is no need to estimate and correct for tissue-to-sampling site transit delays, as there is with the calculation of O2 across an exercising limb utilizing arterial-to-venous blood samples. Therefore, the simultaneous measurement of O2p and NIRS data may yield important information on how muscle O2 delivery and muscle O2 utilization are modulated during the exercise transient in the exercising human.

The purpose of the present study was to examine the effect of age on the adaptation of O2p and muscle deoxygenation at the onset of moderate-intensity cycling exercise. We hypothesized that, at the onset of moderate-intensity exercise, 1) O2p kinetics would be slower in older compared with younger adults in accordance with previous findings, and 2) there would be a greater increase [i.e., change ({Delta}) from pretransition baseline] and faster adaptation of muscle deoxygenation in older compared with younger adults which, combined with the anticipated slower adaptation of O2p in the older adult, would reflect a lower and/or more slowly adapting regional muscle blood flow in the older adult during the on-transient of exercise.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 REFERENCES
 
Subjects.   Six young (Y) (25 ± 3 yr; mean ± SD) and six older (O) (68 ± 3 yr) adults volunteered and gave written, informed consent to participate in the study. All procedures were approved by The University of Western Ontario Ethics Committee for Research on Human Subjects. All subjects were physically active. Older subjects were medically screened and had no history of cardiovascular, respiratory, or musculoskeletal diseases and were not taking any medications that would affect the cardiorespiratory response to exercise.

Protocol.   Subjects reported to the laboratory on five occasions. A maximal cycle ergometer ramp test (25 W/min) was performed on the first day of testing for the determination of the estimated lactate threshold ({theta}L) and peak O2 (O2 peak). {theta}L was defined as the O2 at which CO2 production (CO2) began to increase out of proportion in relation to O2 with a systematic rise in minute ventilation-to-O2 ratio and end-tidal PO2 whereas minute ventilation-to-CO2 ratio and end-tidal PCO2 were stable. The incremental ramp test also served as a medical screening of older subjects. This test was supervised by a physician and included monitoring of a 12-lead ECG. After this test, subjects returned to the laboratory on four occasions to perform step transitions in work rate from 20 W to a moderate-intensity work rate selected to elicit a O2 corresponding to 80% {theta}L. Each work rate transition was 6 min in duration and was preceded and followed by 6 min of cycling at 20 W.

Measurements.   Gas-exchange measurements were similar to those described previously (1). Briefly, inspired and expired flow rates were measured using a low-dead-space (90 ml) bidirectional turbine (Alpha Technologies VMM 110), which was calibrated before each test by using a syringe of known volume. Inspired and expired gases were sampled continuously at the mouth and analyzed for concentrations of O2, CO2, and N2 by mass spectrometry (Morgan Medical) after calibration with precision-analyzed gas mixtures. Changes in gas concentration were aligned with gas volumes by measuring the time delay for a square-wave bolus of gas passing the turbine to the resulting changes in fractional gas concentrations as measured by the mass spectrometer. Data collected every 20 ms were transferred to a computer, which aligned concentrations with volume data to build a profile of each breath. Breath-by-breath alveolar gas exchange was calculated by using algorithms of Beaver et al. (3). HR was continuously monitored by ECG.

Local muscle oxygenation profiles of the quadriceps vastus lateralis muscle were made with NIRS (Hamamatsu NIRO 300, Hamamatsu Photonics). Optodes were placed on the belly of the muscle midway between the lateral epicondyle and greater trochanter of the femur. The optodes were housed in an optically dense plastic holder, thus ensuring that the relative positions of the optodes was fixed and invariant. The optode assembly was secured on the skin surface with tape and then covered with an optically dense, black vinyl sheet, thus minimizing the intrusion of extraneous light and loss of near infrared (NIR)-transmitted light from the field of interrogation. The thigh, with attached optodes and covering, was wrapped with an elastic bandage to minimize movement of the optodes while still permitting freedom of movement for cycling. This preparation essentially prevented any optode movement relative to the skin surface.

The theory of NIRS is described in detail by Elwell (25). Briefly, one fiber optic bundle carried the NIR-light produced by the laser diodes to the tissue of interest while a second fiber optic bundle returned the transmitted light from the tissue to a photon detector (photomultiplier tube) in the spectrometer. Four different wavelength laser diodes (775, 810, 850, and 910 nm) provided the light source. The diodes were pulsed in rapid succession, and the light was detected by the photomultiplier tube. The use of four laser diodes enables more chromophores to be detected and also increases the sensitivity of the instrument, thus providing an advantage of the NIRO 300 over other simpler NIR-detection systems that have been used (5, 10, 32). The intensity of incident and transmitted light was recorded continuously at 2 Hz and, along with the relevant specific extinction coefficients and optical pathlength, used for online estimation and display of the concentration changes from the resting baseline of HbO2, HHb, and Hbtot. The raw attenuation signals (in optical density units) were transferred to computer and stored for further analysis.

The interoptode spacing was 5 cm. Although values exist for differential pathlength factors in muscle for calf and forearm (24, 52), there are presently no published values for the quadriceps muscle. In the present study, we used a value for differential pathlength factor of 3.83; thus values for HbO2, HHb, and Hbtot are reported as a change from baseline in micromolar units.

The HHb signal can be regarded as being essentially blood volume insensitive during exercise (17, 26); thus it was assumed to be a reliable estimator of changes in intramuscular oxygenation status and O2 extraction in the field of interrogation (18, 26).

Analysis.   Breath-by-breath gas-exchange data were filtered for aberrant data points, interpolated to 1-s intervals, ensemble averaged, and then averaged into 5-s time bins to yield a single response for each subject. Phase 2 O2p kinetics were determined by the use of a monoexponential model of the form

(1)
where Y represents O2p at any time (t); b is the average baseline value of Y during the 30 s before the exercise on-transient; A is the amplitude of the increase in Y above the baseline value; {tau} is the time constant defined as the duration of time through which Y increases to a value equivalent to 63% of A, and TD is the time delay. Data were fit from the phase 1-phase 2 interface to minute 4 of exercise.

The NIRS-derived HbO2, HHb, and Hbtot data were time aligned and ensemble averaged to 5-s time bins to yield a single response for each subject. The time delay before an increase in HHb (TDHHb) was determined as the duration between the onset of exercise and the first point greater than one standard deviation above the mean of the preexercise baseline HHb signal and was performed on the second-by-second data for each of the individual trials; the TDHHb was calculated as the average of four trials for each subject. After the time delay, HHb data were then fit from the time of initial increase in HHb to 180 s with a monoexponential model of the form in Eq. 1 to determine the time course of muscle deoxygenation. Although we are not certain that the underlying processes determining muscle deoxygenation are exponential in nature, visual inspection of the NIRS-derived HHb signal and analysis of least squares residuals suggested that fitting with a monoexponential model would provide a reasonable estimate of the time course of muscle deoxygenation (i.e., effective {tau}). The HbO2 and Hbtot signals did not approximate an exponential response, and these data were not modeled; however, the response of these signals was compared qualitatively to the HHb data at corresponding time intervals.

Beat-by-beat HR data were filtered for aberrant beats, time aligned and averaged to 5 s time bins. These data were then fit from exercise onset with a monoexponential model of the form in Eq. 1.

Statistical analysis.   Comparisons between groups were made by independent t-tests, whereas comparisons between O2p, HHb, and HR kinetics within each group were by ANOVA. Relationships among key variables were determined by Pearson product correlation. All data are presented as means ± SD. A P value <0.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 REFERENCES
 
Subject characteristics and peak exercise values are presented in Table 1. Older subjects had a lower peak work rate (P < 0.01) and absolute (l/min) and relative (ml·kg–1·min–1) O2 peak (P < 0.01). To confirm that a moderate-intensity steady-state O2p had been achieved, and that a slow component of O2p characteristic of heavy-intensity exercise performed above {theta}L did not exist, the slope of the O2p responses between 3 and 6 min were calculated in O and Y. The O2p slope was not different from zero for O or Y. End-exercise O2p (calculated as the average O2p during the last 30 s of the exercise transient) was also similar to the sum of the O2p baseline and amplitude from modeling in O and Y. Additionally, steady-state O2p equaled 82 ± 4% (range: 78–87%) and 85 ± 4% (range: 81–91%) of estimated {theta}L in the O and Y, respectively, demonstrating that the prescribed exercise intensity was achieved and exercise was performed below the estimated {theta}L in all subjects.


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  		Table 1. Subject characteristics

 
O2 kinetics.   Baseline O2p during the 20 W pretransition baseline was similar in the O (0.80 ± 0.04 l/min) and Y (0.91 ± 0.12 l/min). The amplitude of the increase in O2p was lower in O (0.35 ± 0.10 l/min) compared with Y (0.79 ± 0.21 l/min; P < 0.001), reflecting the lower work rate in the O (O: 56 ± 9 W; Y: 100 ± 20 W; P < 0.001). The gain ({Delta}O2p/{Delta}WR, where WR is work rate) of the O2p response was similar in O (9.7 ± 0.6 ml·min–1·W–1) and Y (9.9 ± 0.5 ml·min–1·W–1). Phase 2 {tau} O2p was greater (P < 0.01) in O (42 ± 9 s) compared with Y (26 ± 7 s) during the moderate-intensity exercise on-transient (Fig. 1, Table 2).



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  		Fig. 1. Adaptation of pulmonary O2 uptake (O2) during a step change in work rate for a representative young (Y; A) and older (O; B) subject. Monoexponential fit of phase 2 data is also illustrated. Solid vertical line represents exercise onset.

 

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  		Table 2. Kinetics parameters for O2, HR, and HHb

 
HR kinetics.   Baseline HR during the 20 W pretransition baseline was similar in the O [83 ± 7 beats/min (bpm)] and Y (86 ± 7 bpm). The amplitude of the increase in HR was lower (P < 0.01) in O (14 ± 3 bpm) compared with Y (26 ± 7 bpm); however, the increase in HR for a given increase in O2p ({Delta}HR/{Delta}O2p) was similar in O (39 ± 4 beats/l) and Y (36 ± 19 beats/l). The {tau} HR was greater (P < 0.05) in O (47 ± 21 s) compared with Y (23 ± 12 s; Fig. 2, Table 2).



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  		Fig. 2. Adaptation of heart rate (HR) during a step change in work rate for a representative Y (A) and O (B) subject. Monoexponential fit of data is also illustrated. Solid vertical line represents exercise onset.

 
NIRS.   The adaptation of muscle deoxgenation at the onset of exercise is shown for a representative O and Y adult in Fig. 3. After the step increase in work rate, a similar TDHHb before an increase in NIRS-derived HHb was observed in O (11 ± 1 s) and Y (12 ± 2 s; Table 2). The amplitude of the increase in HHb was similar between O (5 ± 2 µM) and Y (6 ± 2 µM) groups; however, the increase in HHb ({Delta}HHb) for a given increase in O2p ({Delta}O2p) was greater (P < 0.01) in O (13 ± 4 µM·l–1·min) than Y (7 ± 2 µM·l–1·min) (Fig. 4). After the time delay, HHb increased rapidly in both groups and the effective {tau} HHb of the response was similar between O (9 ± 3 s) and Y (13 ± 10 s) subjects (Fig. 3, Table 2).



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  		Fig. 3. Adaptation of muscle deoxygenation (HHb) during a step change in work rate for a representative Y (A) and O (B) subject. Monoexponential fit of data is also illustrated. Solid vertical line represents exercise onset.

 


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  		Fig. 4. Ratio of change in HHb to change in pulmonary O2 uptake ({Delta}HHb/{Delta}O2p) in Y and O adults. **P < 0.01.

 
The adaptation of HHb during the on-transient of exercise was faster than the adaptation of phase 2 O2p in both O and Y subjects (Table 2). Also, in O the time course for the overall change in HHb [mean response time (MRT)-HHb = TDHHb + effective {tau} HHb] was less than (P < 0.01) the {tau} O2p, whereas in Y, the MRT-HHb and {tau} O2p were similar.

The {tau} O2p was not correlated with the effective {tau} HHb response, nor was it correlated with the MRT-HHb or {tau} HR in O or Y subjects. When the O and Y data were collapsed into a single data set, {tau} O2p was positively correlated (r = 0.756; P = 0.004; Fig. 5) with {tau} HR, whereas {tau} O2p was not correlated with the effective {tau} HHb or the MRT-HHb.



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  		Fig. 5. Relationship between pulmonary O2 and HR kinetics in Y and O adults. {bullet} and {circ}, O and Y adults, respectively.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 REFERENCES
 
This study examined the effect of age on the adaptation of O2p and muscle deoxygenation at the onset of moderate-intensity leg cycling exercise. The main findings were as follows: 1) O2p kinetics were slower (P < 0.01) in O compared with Y, in agreement with previous reports (1, 6, 12, 16); 2) HR kinetics were also slower (P < 0.05) in O compared with Y; 3) the TDHHb was similar in O and Y; 4) after the time delay, the adaptation of HHb (effective {tau} HHb) was similar in O and Y; and 5) the ratio of change in HHb to change in pulmonary uptake ({Delta}HHb/{Delta}O2p) during the steady state of moderate-intensity exercise was greater (P < 0.05) in O compared with Y. Given the slower adaptation of O2p and HR in O compared with Y and the fact that the NIRS-derived HHb signal reflects the balance between O2 delivery and O2 utilization, these results suggest that, during the on-transient of moderate-intensity exercise, muscle blood flow may be lower and adapt at a slower rate in O compared with Y, placing a greater reliance on O2 extraction. Therefore, the slower O2p kinetics observed in O may be the result of a slower adaptation of regional O2 delivery during the exercise on-transient in O relative to Y adults. However, these results do not preclude the possibility that the fundamental limitation to O2p kinetics in the O and Y resides within the muscle cell.

To date, technical limitations have precluded study at the level of the microvasculature in the exercising human; thus the ability to monitor noninvasively the balance between O2 delivery and utilization in the microvasculature of the exercising human with NIRS is a major advance in the study of muscle O2 consumption. Previous studies examining the factors responsible for the regulation of O2 consumption at the onset of exercise have utilized measurements of bulk blood flow in large conduit arteries to exercising limbs along with sampling of mixed venous (and occasionally, arterial) blood at discrete time points for calculation of arteriovenous O2 difference [(a-v)O2] to examine the relationship between muscle blood flow and muscle O2 consumption. However, this methodology is invasive and provides a global assessment of muscle O2 consumption across an exercising limb. Thus analysis of local tissue oxygenation changes is not possible, and the influence of blood perfusing inactive muscle groups may contribute to an elevated mixed venous O2 content and lead to an underestimation of local muscle O2 consumption. Conversely, NIRS data have been shown to reflect closely the muscle metabolic rate as determined by magnetic resonance spectroscopy-derived phosphocreatine changes (a proxy for muscle O2 consumption) but correlated poorly with the metabolic rate determined from blood flow and (a-v)O2 measurements (9).

In agreement with our hypothesis and consistent with several previous reports (1, 6, 12, 16), O2p kinetics were slower in O compared with Y adults at the onset of moderate-intensity exercise. Because of technical difficulties associated with studying the adaptation of local muscle blood flow and O2 utilization in the exercising human, the mechanism(s) responsible for the slowing of O2p kinetics with advancing age have yet to be elucidated. Evidence for both a muscle O2 delivery and a muscle O2 utilization limitation has been reported; however, no clear consensus has been reached.

Age-associated structural and functional changes within the heart (31) and peripheral vasculature (30, 38, 39, 50) suggest that the older adult has a reduced ability to increase and muscle blood flow during exercise and that O2p kinetics may be limited by O2 delivery in older adults. Previous studies comparing older to younger adults have demonstrated that the increase in for a given increase in O2p was attenuated in older adults (35, 51). Furthermore, reductions in limb blood flow and vascular conductance in older adults at rest (21–23) and during steady-state exercise (40, 42, 53), as well as a reduced ability to redistribute blood flow from the splanchnic and renal circulations to muscle during exercise (28), also suggest that muscle O2 delivery may be reduced in older adults. The adaptation of HR after the onset of exercise has been used as an indicator of the rate of adaptation of and presumably muscle O2 delivery. In agreement with previous studies (6, 12, 20, 46), HR kinetics were slower (P < 0.01) in O compared with Y in the present study. The slower adaptation of HR at exercise onset in O has been attributed to a slower withdrawal of vagal activity and decreased {beta}-adrenergic responsiveness (47). There was also a significant relationship (r = 0.756; P = 0.004) between HR and O2p kinetics across all subjects in the present study, suggesting an association between the adaptation of HR and the kinetics of O2p (Fig. 5). However, if a greater percentage of is distributed to the leg muscles as reported by Proctor et al. (41), then muscle blood flow may not be reduced despite a slower adaptation of in healthy older adults. Bell et al. (7), using Doppler ultrasonography, observed that the kinetics of femoral arterial blood flow during the on-transient of heavy-intensity single-leg knee extension exercise were faster than O2p kinetics in older adults, suggesting that limb O2 delivery was adequate to meet O2 demand. Furthermore, after exercise training that resulted in a speeding of O2p kinetics in O adults, the kinetics of limb blood flow were unchanged. Thus a slow increase of blood flow to the exercising limb appears not to be cause of slow O2p kinetics in the study of Bell et al. In studies that have reported a lower limb blood flow during steady-state exercise in older compared with younger adults, the reduced O2 delivery was compensated for by an increased (a-v)O2 in O compared with Y at similar exercise intensities (40, 42, 53). Therefore, if muscle blood flow and O2 delivery were lower and slower to adapt in older compared with younger adults in the present study, a faster and greater increase of muscle deoxygenation relative to the adaptation of O2p would be expected in older adults.

After a time delay, HHb increased rapidly toward a "steady-state" level in Y (effective {tau} HHb = 13 ± 10 s) and O (effective {tau} HHb = 9 ± 3 s) in the present study. Comparison of the {tau} O2p with both the effective {tau} HHb (Table 2) and the MRT-HHb (Table 2) revealed that muscle deoxygenation increased at a faster rate (P < 0.001) than phase 2 O2p in O adults, whereas the adaptation of MRT-HHb and O2p was similar in Y subjects. Additionally, the increase in local muscle HHb concentration ({Delta}HHb) from pretransition levels to the steady state of exercise was similar in O and Y, but, expressed relative to the increase in O2p ({Delta}HHb/{Delta}O2p) from pretransition levels to the steady state of exercise, the {Delta}HHb/{Delta}O2p was greater (P < 0.01) in O, suggesting a greater reliance on O2 extraction for a given metabolic demand in O. These data suggest that, at the microvascular level, the degree of mismatch between local muscle perfusion and metabolism requires that O2 extraction increase rapidly in O to support tissue metabolic demand, evidenced by the rapid increase of MRT-HHb relative to the adaptation of O2p and greater {Delta}HHb/{Delta}O2p in O. Thus the slower O2p kinetics in O adults appear to be associated with a slower increase in local muscle O2 delivery. However, whether a slower adaptation of muscle blood flow in the older adult is the fundamental limitation to O2p kinetics in the older adult or whether the limitation lies with intracellular mechanisms cannot be discerned from the present study.

The greater {Delta}HHb/{Delta}O2p in O also suggests that the ability to extract O2 during submaximal moderate intensity is not diminished in older adults. This finding is consistent with other reports of a greater (a-v)O2 (40, 53) and/or fractional O2 extraction (42) in older compared with younger adults. Thus, whereas previous studies (13, 14, 33, 34, 36) have reported a decline in maximal skeletal muscle oxidative capacity with aging, the results from this and other studies suggest that the ability of the older adult to utilize available O2 during the on-transient and steady-state of submaximal exercise is well preserved. Furthermore, these results suggest that changes in maximal muscle oxidative capacity with aging do not impact on the ability of the older adult to extract O2 during the exercise on-transient of moderate-intensity cycling exercise evidenced by the greater {Delta}HHb/{Delta}O2p in O compared with Y adults. However, it is also apparent that O adults were unable to increase O2 extraction to the level required for O2p in O to increase at a rate comparable to that of Y adults at the onset of exercise.

Also, after the onset of constant-load moderate-intensity cycling exercise, a time delay of ~12 s was observed before an increase in the NIRS-derived HHb signal above preexercise baseline levels in both Y and O adults. We have previously documented a delay before an increase in HHb in Y adults at the onset of moderate-intensity cycling exercise (19). To our knowledge, this is the first study to document a similar delay in O adults. The potential explanations for this delay have been discussed previously in detail (19). We believe that the HHb delay reflects a complex balance between Hb-myoglobin deoxygenation, O2 delivery, and the effect of muscle contraction on microvascular volume, such that muscle O2 consumption is actually increasing during the delay and an increase in HHb is "masked" by other factors that impact on the volume of Hb in the field of NIRS interrogation (19). The presence of a similar HHb time delay in the O and Y in the present study suggests that, immediately after the onset of exercise when muscle O2 consumption is presumably increasing, local muscle oxygenation status is maintained during the early (first 10–12 s) phase of the increase in muscle O2 consumption in both O and Y subjects. In contrast to our previous study (19), in this study we observed an early decrease in HHb below the pretransition baseline level in 2 Y and 3 O subjects, suggesting that muscle blood flow may actually be in excess of muscle O2 consumption immediately after the onset of exercise in these subjects. Grassi et al. (27) and Bangsbo et al. (2) have reported previously that muscle O2 delivery may be in excess of muscle O2 consumption in young adults during the first ~15 s of a work rate transition, evidenced by a decrease in the (a-v)O2 immediately after the onset of exercise. Behnke et al. (4), utilizing phosphorescence quenching to study the adaptation of microvascular PO2 after the onset of electrical stimulation in the isolated rat spinotrapezius muscle, reported that muscle O2 delivery was closely matched to (71% of animals studied) or in excess of (29% of animals studied) muscle O2 consumption during the first ~20 s of electrical stimulation. This rapid increase in muscle O2 delivery after the onset of exercise has been attributed to a mechanical muscle pump-mediated increase in muscle blood flow (48, 49) because a metabolic vasodilatory substance capable of inducing the dilation necessary to increase muscle blood flow to this extent in the first several seconds after onset of exercise has yet to be identified (54). Therefore, in the present study, the constant or decreased HHb in O and Y adults suggest that the effectiveness of the muscle pump is not diminished with advancing age and that the greater reliance on O2 extraction in older adults throughout the remainder of the exercise transient may be the result of a slowed local muscle vasodilation. An increase in HHb immediately after the onset of exercise, which would suggest that muscle O2 consumption was increasing at a faster rate than muscle O2 delivery, was not observed in any of the Y or O subjects.

In conclusion, this study demonstrated slower O2p and HR kinetics, a similar adaptation of muscle deoxygenation (HHb) and a greater {Delta}HHb/{Delta}O2p in O compared with Y adults during a moderate-intensity work rate transition. These results suggest that local muscle perfusion may adapt at a slower rate and be lower in O compared with Y subjects during the exercise on-transient, placing a greater reliance on O2 extraction. These results also suggest that the ability to extract O2 after the onset of moderate-intensity exercise is preserved in the older adult and that the slowed O2p kinetics in O may be a consequence of a diminished local vascular control and poorer matching of O2 delivery to muscle metabolism during the exercise on-transient. Finally, it must be recognized that whereas a slower adaptation of local muscle blood flow may impose an additional limitation on the adaptation of O2p in older adults, the fundamental limitation to activation of muscle O2 consumption may be related to factors other than muscle O2 delivery (i.e., intramuscular factors).


   GRANTS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 GRANTS
REFERENCES
 
This study was supported by Natural Science and Engineering Research Council of Canada (NSERC) research and equipment grants. Additional support was provided by a University of Western Ontario Academic Development Fund Grant and infrastructure support from the Canadian Foundation for Innovation and Ontario Innovation Trust. D. S. DeLorey was supported by doctoral research scholarships from NSERC and the Canadian Institutes of Health Research.


   FOOTNOTES
 

Address for reprint requests and other correspondence: D. H. Paterson, Canadian Centre for Activity and Aging, School of Kinesiology, The University of Western Ontario, London, ON, Canada N6A 3K7 (E-mail: dpaterso{at}uwo.ca).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
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  1. Babcock MA, Paterson DH, Cunningham DA, and Dickinson JR. Exercise on-transient gas exchange kinetics are slowed as a function of age. Med Sci Sports Exerc 26: 440–446, 1994.
  2. Bangsbo J, Krustrup P, Gonzalez-Alonso J, Boushel R, and Saltin B. Muscle oxygen kinetics at onset of intense dynamic exercise in humans. Am J Physiol Regul Integr Comp Physiol 279: R899–R906, 2000.
  3. Beaver WL, Lamarra N, and Wasserman K. Breath-by-breath measurement of true alveolar gas exchange. J Appl Physiol 51: 1662–1675, 1981.
  4. Behnke BJ, Kindig CA, Musch TI, Koga S, and Poole DC. Dynamics of microvascular oxygen pressure across the rest-exercise transition in rat skeletal muscle. Respir Physiol 126: 53–63, 2001.
  5. Belardinelli R, Barstow TJ, Porszasz J, and Wasserman K. Skeletal muscle oxygenation during constant work rate exercise. Med Sci Sports Exerc 27: 512–519, 1995.
  6. Bell C, Paterson DH, Kowalchuk JM, and Cunningham DA. Oxygen uptake kinetics of older humans are slowed with age but are unaffected by hyperoxia. Exp Physiol 84: 747–759, 1999.
  7. Bell C, Paterson DH, Kowalchuk JM, Moy AP, Thorp DB, Noble EG, Taylor AW, and Cunningham DA. Determinants of oxygen uptake kinetics in older humans following single-limb endurance exercise training. Exp Physiol 86: 659–665, 2001.
  8. Boushel R, Langberg H, Olesen J, Gonzales-Alonzo J, Bulow J, and Kjaer M. Monitoring tissue oxygen availability with near infrared spectroscopy (NIRS) in health and disease. Scand J Med Sci Sports 11: 213–222, 2001.
  9. Boushel R, Pott F, Madsen P, Radegran G, Nowak M, Quistorff B, and Secher N. Muscle metabolism from near infrared spectroscopy during rhythmic handgrip in humans. Eur J Appl Physiol 79: 41–48, 1998.
  10. Chance B, Dait MT, Zhang C, Hamaoka T, and Hagerman F. Recovery from exercise-induced desaturation in the quadriceps muscles of elite competitive rowers. Am J Physiol Cell Physiol 262: C766–C775, 1992.
  11. Chilibeck PD, Paterson DH, McCreary CR, Marsh GD, Cunningham DA, and Thompson RT. The effects of age on kinetics of oxygen uptake and phosphocreatine in humans during exercise. Exp Physiol 83: 107–117, 1998.
  12. Chilibeck PD, Paterson DH, Petrella RJ, and Cunningham DA. The influence of age and cardiorespiratory fitness on kinetics of oxygen uptake. Can J Appl Physiol 21: 185–196, 1996.
  13. Coggan AR, Abduljalil AM, Swanson SC, Earle MS, Farris JW, Mendenhall LA, and Robitaille PM. Muscle metabolism during exercise in young and older untrained and endurance-trained men. J Appl Physiol 75: 2125–2133, 1993.
  14. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, and Holloszy JO. Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J Gerontol B Psychol Sci Soc Sci 47: B71–B76, 1992.
  15. Conley KE, Jubrias SA, and Esselman PC. Oxidative capacity and ageing in human muscle. J Physiol 526: 203–210, 2000.
  16. Cunningham DA, Himann JE, Paterson DH, and Dickinson JR. Gas exchange dynamics with sinusoidal work in young and elderly women. Respir Physiol 91: 43–56, 1993.
  17. De Blasi RA, Cope M, Elwell C, Safoue F, and Ferrari M. Noninvasive measurement of human forearm oxygen consumption by near infrared spectroscopy. Eur J Appl Physiol 67: 20–25, 1993.
  18. De Blasi RA, Ferrari M, Natali A, Conti G, Mega A, and Gasparetto A. Noninvasive measurement of forearm blood flow and oxygen consumption by near-infrared spectroscopy. J Appl Physiol 76: 1388–1393, 1994.
  19. DeLorey DS, Kowalchuk JM, and Paterson DH. Relationship between pulmonary O2 uptake kinetics and muscle deoxygenation during moderate-intensity exercise. J Appl Physiol 95: 113–120, 2003.
  20. DeVries HA, Wiswell RA, Romero G, Moritani T, and Bulbulian R. Comparison of oxygen kinetics in young and old subjects. Eur J Appl Physiol 49: 277–286, 1982.
  21. Dinenno FA, Jones PP, Seals DR, and Tanaka H. Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation 100: 164–170, 1999.
  22. Dinenno FA, Seals DR, Desouza CA, and Tanaka H. Age-related decreases in basal limb blood flow in humans: time course, determinants and habitual exercise effects. J Physiol 531: 573–579, 2001.
  23. Dinenno FA, Tanaka H, Stauffer BL, and Seals DR. Reductions in basal limb blood flow and vascular conductance with human ageing: role for augmented alpha-adrenergic vasoconstriction. J Physiol 536: 977–983, 2001.
  24. Duncan A, Meek JH, Clemence M, Elwell CE, Tyszczuk L, Cope M, and Delpy DT. Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. Phys Med Biol 40: 295–304, 1995.
  25. Elwell C. A Practical Users Guide to Near Infrared Spectroscopy. London: Hamatsu Photonics, 1995, p. 1–155.
  26. Ferrari M, Binzoni T, and Quaresima V. Oxidative metabolism in muscle. Philos Trans R Soc Lond B Biol Sci 352: 677–683, 1997.
  27. Grassi B, Poole DC, Richardson RS, Knight DR, Erickson BK, and Wagner PD. Muscle O2 uptake kinetics in humans: implications for metabolic control. J Appl Physiol 80: 988–998, 1996.
  28. Horvath SM and Borgia JF. Cardiopulmonary gas transport and aging. Am Rev Respir Dis 129: S68–S71, 1984.
  29. Kent-Braun JA and Ng AV. Skeletal muscle oxidative capacity in young and older women and men. J Appl Physiol 89: 1072–1078, 2000.
  30. Lakatta EG and Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part I: aging arteries: a "set up" for vascular disease. Circulation 107: 139–146, 2003.
  31. Lakatta EG and Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part II: the aging heart in health: links to heart disease. Circulation 107: 346–354, 2003.
  32. Mancini DM, Bolinger L, Li H, Kendrick K, Chance B, and Wilson JR. Validation of near-infrared spectroscopy in humans. J Appl Physiol 77: 2740–2747, 1994.
  33. McCully KK, Fielding RA, Evans WJ, Leigh JS Jr, and Posner JD. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 75: 813–819, 1993.
  34. McCully KK, Forciea MA, Hack LM, Donlon E, Wheatley RW, Oatis CA, Goldberg T, and Chance B. Muscle metabolism in older subjects using 31P magnetic resonance spectroscopy. Can J Physiol Pharmacol 69: 576–580, 1991.
  35. McElvaney GN, Blackie SP, Morrison NJ, Fairbarn MS, Wilcox PG, and Pardy RL. Cardiac output at rest and in exercise in elderly subjects. Med Sci Sports Exerc 21: 293–298, 1989.
  36. Meredith CN, Frontera WR, Fisher EC, Hughes VA, Herland JC, Edwards J, and Evans WJ. Peripheral effects of endurance training in young and old subjects. J Appl Physiol 66: 2844–2849, 1989.
  37. Mizuno M, Kimura Y, Iwakawa T, Oda K, Ishii K, Ishiwata K, Nakamura Y, and Muraoka I. Regional differences in blood flow and oxygen consumption in resting muscle and their relationship during recovery from exhaustive exercise. J Appl Physiol 95: 2204–2210, 2003.
  38. Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD, and Delp MD. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282: H1843–H1854, 2002.
  39. Muller-Delp JM, Spier SA, Ramsey MW, and Delp MD. Aging impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283: H1662–H1672, 2002.
  40. Poole JG, Lawrenson L, Kim J, Brown C, and Richardson RS. Vascular and metabolic response to cycle exercise in sedentary humans: effect of age. Am J Physiol Heart Circ Physiol 284: H1251–H1259, 2003.
  41. Proctor DN, Newcomer SC, Koch DW, Le KU, MacLean DA, and Leuenberger UA. Leg blood flow during submaximal cycle ergometry is not reduced in healthy older normally active men. J Appl Physiol 94: 1859–1869, 2003.
  42. Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, Loeffler DL, and Joyner MJ. Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol 85: 68–75, 1998.
  43. Proctor DN, Sinning WE, Walro JM, Sieck GC, and Lemon PW. Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 78: 2033–2038, 1995.
  44. Richardson RS, Haseler LJ, Nygren AT, Bluml S, and Frank LR. Local perfusion and metabolic demand during exercise: a noninvasive MRI method of assessment. J Appl Physiol 91: 1845–1853, 2001.
  45. Russell JA, Kindig CA, Behnke BJ, Poole DC, and Musch TI. Effects of aging on capillary geometry and hemodynamics in rat spinotrapezius muscle. Am J Physiol Heart Circ Physiol 285: H251–H258, 2003.
  46. Scheuermann BW, Bell C, Paterson DH, Barstow TJ, and Kowalchuk JM. Oxygen uptake kinetics for moderate exercise are speeded in older humans by prior heavy exercise. J Appl Physiol 92: 609–616, 2002.
  47. Seals DR, Taylor JA, Ng AV, and Esler MD. Exercise and aging: autonomic control of the circulation. Med Sci Sports Exerc 26: 568–576, 1994.
  48. Sheriff DD, Rowell LB, and Scher AM. Is rapid rise in vascular conductance at onset of dynamic exercise due to muscle pump? Am J Physiol Heart Circ Physiol 265: H1227–H1234, 1993.
  49. Shoemaker JK and Hughson RL. Adaptation of blood flow during the rest to work transition in humans. Med Sci Sports Exerc 31: 1019–1026, 1999.
  50. Taddei S, Virdis A, Mattei P, Ghiadoni L, Gennari A, Fasolo CB, Sudano I, and Salvetti A. Aging and endothelial function in normotensive subjects and patients with essential hypertension. Circulation 91: 1981–1987, 1995.
  51. Thomas SG, Paterson DH, Cunningham DA, McLellan DG, and Kostuk WJ. Cardiac output and left ventricular function in response to exercise in older men. Can J Physiol Pharmacol 71: 136–144, 1993.
  52. Van der Zee P, Cope M, Arridge SR, Essenpreis M, Potter LA, Edwards AD, Wyatt JS, McCormick DC, Roth SC, and Reynolds EO. Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. Adv Exp Med Biol 316: 143–153, 1992.
  53. Wahren J, Saltin B, Jorfeldt L, and Pernow B. Influence of age on the local circulatory adaptation to leg exercise. Scand J Clin Lab Invest 33: 79–86, 1974.
  54. Wunsch SA, Muller-Delp J, and Delp MD. Time course of vasodilatory responses in skeletal muscle arterioles: role in hyperemia at onset of exercise. Am J Physiol Heart Circ Physiol 279: H1715–H1723, 2000.



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