Aging is characterized by a decline in several physiological functions that result in a reduction in physical performance. On the other hand, regular exercise training can limit this negative effect of aging. As a matter of fact, master athletes are capable of remarkable exercise performances (22,23) and therefore represent an optimal model to study the potential for maintaining physiological functional capacity.
Among other factors, the capacity to sustain exercise intensity at high fractions of maximal oxygen uptake (o2max) is thought to be an important determinant of endurance performance (2,10). This capacity, which is associated with the concept of metabolic thresholds (13), can be evaluated noninvasively by analyzing pulmonary gas exchange during an incremental exercise test. During such a test, the first rise in blood-lactate concentration is associated with an overproduction of carbon dioxide relative to o2 as a consequence of bicarbonate buffering of the protons arising from lactic acid dissociation. This CO2 excess is thought to be responsible for the compensatory increase in pulmonary ventilation (E), which also increases out of proportion with o2. The metabolic rate (o2) at which this occurs is referred to as anaerobic threshold (7,24,27) or as ventilatory threshold (VT). As exercise intensity is further increased, a second ventilatory response, characterized by an exponential increase in VE relative to CO2, can be observed. This point is referred to as respiratory compensation point (RCP). The region between VT and RCP, where the increase in VE is associated with stable PETCO2, has been termed as the isocapnic buffering (IB) phase and should represent a phase of compensation for the metabolic acidosis generated by the exercise (25,26). Finally, the phase between RCP and maximal exercise capacity is defined as hypocapnic hyperventilation (HHV).
Although a large body of evidence exists on the effect of training on VT (15), much less attention has been dedicated to investigating the training effects on IB. The few studies available have consistently reported that the phase of IB may enlarge in response to high-intensity training (16,17,20), that it may be more closely correlated to o2max than VT in young athletes, and that it shifts toward higher values in the o2 spectrum (thereby reducing the HHV phase) in professional cyclists throughout the competitive season (5). The concept of IB, therefore, might represent a useful tool for both the trainer willing to track changes in performance potential of their athletes and for the physiologist to characterize the metabolic adaptations induced by a given training regime.
With aging, VT has been shown to decline at a slower rate than o2max (18,21) and therefore to occur at higher relative intensities (6). This effect, together with a larger IB phase, might be important to understand the relatively well-maintained endurance capacity of master athletes (22) despite the reduction in maximal aerobic power.
Recently, the physiological characteristics of masters-level cyclists of different ages have been described (19). However, in that study, the subjects were not compared to an untrained age-matched counterpart, which is relevant to the understanding of the physiological, functional, and performance advantage of maintaining a high level of physical activity throughout life and especially in older age.
With this in mind, the present study was aimed at investigating the possible interaction between aging and training on the ventilatory response during incremental maximal cycling exercise, with a particular focus on the IB phase. It was also intended to verify whether IB could represent a tool for performance evaluation and control. We hypothesized that the training status would be reflected in a wider IB phase and that this would occur in both young and older individuals.
Experimental Approach to the Problem
The intensity of occurrence of the metabolic thresholds was obtained by using an incremental maximal cycling test. To study the effect of endurance training and aging, young and older highly trained competitive cyclists were compared to age-matched untrained subjects. To characterize the endurance exercise potential, ventilatory markers indicative of the capacity to sustain a given metabolic load, together with the maximal workload reached during an incremental test, were compared. Finally, IB was calculated and related to the training status and age to obtain indications on its trainability in young and order adults.
Thirty-two male subjects volunteered to participate in this study. Sixteen of them, 8 young and 8 older, were road cyclists engaged in regular training and amateur racing, whereas the remaining 16 were young untrained university students and untrained pensioners. The characteristics of the 4 study groups are reported in Table 1.
The amateur cyclists had competition experience of at least 8 years. Some in the older group had >20 years of experience. All of them trained at least 3 times a week covering a distance ranging between 300 and 500 km, in addition to competition or Sunday training. The untrained subjects were healthy and physically active but not engaged in regular training. Before entering the study, the older subjects underwent a medical screening to exclude cardiovascular, orthopedic, and metabolic diseases.
The study was approved by the local ethical committee. After being informed about the purpose of the study and the possible risks connected with the experimental procedures, each participant provided signed, informed consent.
Subjects were instructed to refrain from exercise during the last 2 days preceding the experimental trial, which consisted of a maximal incremental exercise test on a friction-loaded cycle ergometer (Monark type 894E, Stockholm, Sweden). After a standard warm-up, the workload was increased every minute by 21 W in trained and young untrained subjects, and by 10 W in untrained older subjects. Subjects were instructed to maintain a pedaling cadence of 70 rpm throughout the test, during which ventilatory and gas exchange variables were measured using a breath-by-breath gas analyzer (Quark b2, Cosmed, Rome, Italy). Before each test, the analyzers were calibrated with gases of known concentration, and the turbine was calibrated by means of a 3-L syringe. The 12-lead electrocardiogram and heart rate (HR) were continuously monitored throughout the test, which was terminated when the subjects could no longer maintain the requested pedaling cadence or when the criteria for documentation of o2max were met (plateau in o2 despite increasing work rate; respiratory exchange ratio (RER) ≥ 1.1; reaching 95% of the age-predicted maximal HR).
All tests were performed in the morning and 3 hours after a standardized breakfast. The cyclists were tested in the middle of the competitive season, when a constant exercise performance was assumed.
Determination of Ventilatory Threshold and Respiratory Compensation Point
To increase the accuracy of the identification of VT and RCP, a combination of graphical methods was used. Ventilatory threshold was determined using the V-slope and the ventilatory equivalent methods (3,24). Respiratory compensation point was instead determined by using the loss of linearity of the CO2 vs. E plot (similarly to the V-slope method) and adopting the first systematic increase of E/CO2 and the first decrease in PETCO2 (15,24). To reduce the variability connected with the identification of VT and RCP, analyses were performed by 2 independent investigators. In cases of a discrepancy >3%, the same procedure was performed by a third researcher and the values averaged with the closer values from the previous evaluation.
Determination of Isocapnic Buffering and Hypocapnic Hyperventilation
Isocapnic buffering was calculated as the difference in o2 between RCP and VT and expressed in either absolute or relative (% o2max) values. Hypocapnic hyperventilation was computed as the difference in o2 between o2max and RCP.
Differences in the ventilatory variables (VT, RCP, o2max), the calculated parameters (IB, HHV), and the mechanical parameters (PO) between groups were assessed by using analysis of variance (ANOVA). If the ANOVA indicated a significant main effect, a post hoc Student t test with Bonferroni correction was used to locate the differences. Pearson product-moment correlations were determined for all correlation analyses. Data are presented as mean ± SD. The level of significance was set at p ≤ 0.05.
o2, power output, and HR at VT, RCP, and maximal exercise intensity are reported in Table 2. o2max was significantly higher in young trained (YT) and in older trained (OT) subjects compared to in the young untrained (YU) and older untrained (OU) counterparts. It was also higher in YT than in OT, who showed, however, a o2max comparable with that of YU individuals. Training was associated with a higher peak power output both in old and young subjects (26 and 32% in YT vs. YU and OT vs. OU, respectively). Peak power output was also affected by aging, being substantially higher (36%) in YU than in OU (p < 0.01).
Ventilatory threshold, expressed as either absolute o2 or power output, was higher (p < 0.01) in trained than in untrained subjects (33 and ∼25% in YT vs. YU and OT vs. OU, respectively). In relative terms, VT occurred at similar intensities in all groups, although a tendency (p = 0.06) was observed for a higher relative value in OU than in YU. At RCP, absolute o2 and PO were higher in trained than in untrained subjects and occurring at a higher fraction of o2max.
Isocapnic buffering phase, relative buffering capacity, and absolute and relative HHV are shown in Figures 1 and 2. Isocapnic buffering phase and relative buffering capacity were significantly higher in YT and OT subjects compared to the untrained subjects, whereas no effect of age could be detected.
Hypocapnic hyperventilation phase in absolute values was higher in YT than in YU subjects, whereas it was similar in OT and in OU subjects. However, in relative terms, HHV was significantly lower in YT than in YU and in OT than in OU.
When pooling the data of all subjects, a significant correlation was found between o2max and VT (R2 = 0.88), RCP (R2 = 0.96), and IB (R2 = 0.61), whereas no significant correlation was observed between o2max and HVV (Figure 3).
Heart rate at VT, RCP, and peak exercise intensity was similar in trained and untrained subjects but was higher in young than in older participants (Table 2). This also implies that HR at VT and RCP occurred at the same percentage of HRmax.
In the present study, the effect of aging and training status on ventilatory response during incremental exercise was investigated by comparing young and older well-trained cyclists with active, but untrained, individuals of the same age. The results indicate that aging reduces the IB phase, and that on the contrary, it is higher in trained individuals independent of age.
The identification of parameters that can describe the highest metabolic rate that can be maintained for long periods of time has applications both in the clinical context, for instance to evaluate exercise tolerance, and in analyzing endurance sport performance (7). In this regard, physiological variables such as o2max, VT, and RCP are thought, among others, to be suggestive of endurance performance. They therefore provide indications of the adaptations induced by training (15,22) and precious information for the trainer who wants to monitor the training outcome.
In the present study, as expected, o2max was higher in trained than in untrained subjects and was reduced by aging to a similar extent in both groups, in line with the ∼10% decline per decade normally reported (22). Of note, trained old cyclists showed a o2max comparable to that of young untrained individuals, which allowed us to evaluate the changes in IB without the confounding effect of different maximal aerobic capacity values.
With aging, an association between decline in maximal aerobic power and endurance performance has been shown (9). However, the rate of decline of the latter can be smaller than the former (12), suggesting that other factors might be associated with the age-related impairment of endurance performance. Moreover, VT has been shown to decline at a lower rate than o2max with aging (18,21) and to occur at higher relative exercise intensities (8). In the present study, VT was occurring at a similar fraction of o2max in all groups, although a tendency was observed for a higher value in the YT and OU groups. This similar and relatively high value, however, might be indicative of different physiological adaptations causing different functional consequences. In fact, although in young and older cyclists, a relatively high VT is important for sustaining an intense exercise training regime, in the untrained older individuals, the same adaptation could be important to cope with the functional tasks of everyday life. In this respect, for example, Cunningham et al. (6) explained the observation of a maintained high level of VT relative to o2max in older individuals based on the fact that the intensity of exercise corresponding to VT was equivalent to the o2 necessary for normal walking.
The region between VT and RCP during an incremental maximal test is referred as IB phase and was a major focus of this study. The studies that specifically address IB in relation to aging and training are scarce and, to the best of our knowledge, the present investigation is the first to describe the effect of both factors on IB.
The longer IB phase observed in trained subjects was associated with RCP occurring at higher intensities. This is in accordance with previous investigations showing a higher relative buffering capacity in young individuals accustomed to training at high intensities (20) and with an enlargement of the IB phase after 6 months of endurance training at intensities higher than the VT (17). Moreover, the larger IB phase in older athletes compared with the untrained older participants is also in agreement with previous research on subjects of a comparable age (8). In addition, the effect of aging was made evident by significantly lower values of absolute and relative IB values in the older untrained compared to young untrained volunteers. Furthermore, IB was similar between young and older cyclists and was associated with a smaller HHV phase in trained individuals. Taken together, these observations highlight an age-independent adaptability of IB and HVV to endurance training.
To investigate the relevance of IB on endurance performance, Bentley et al. (4) studied the relationship between IB phase and time trial performance in male endurance athletes and found a weak correlation between 20-minute cycling time trial and IB. In our study, we did not directly measure endurance performance, but, if peak power output is considered as indicative for cycling performance (1,11), it would appear that individuals who show a larger IB are those who reach higher peak power output values (R2 = 0.52, data not shown). Moreover, Chicharro et al. (5) reported an unchanged magnitude of the IB phase in professional cyclists throughout the competitive season, but observed a shift toward higher power output values, with a consequent reduction of the HHV phase. On the basis of the above-reported previous findings, the data of the present study suggest that a better maintained endurance exercise performance with aging is realized by maintaining a relatively high buffering capacity and a small HHV phase. Both adaptations can be interpreted as an improvement in the capacity to sustain exercise at high intensities.
Previous data (16) indicated a positive and significant correlation between IB and o2max in young athletes. When pooling the data from all groups, we also observed a significant correlation between o2max and VT, RCP, and IB. In addition, our young untrained subjects had a lower IB phase than older cyclists did, despite similar o2max values. Moreover, the length of the IB phase was similar in older and young cyclists despite o2max being higher in the latter. This would suggest that the magnitude of the IB phase is related more to the training status rather than o2max or aging. On the other hand, it should be considered that the effect of training on o2max could be related to the magnitude of the IB phase and to its collocation in the o2 spectrum. It is possible, in fact, that individuals with a high buffering capacity could exercise for longer periods of time at higher intensities, and this may influence the gain in o2max, which is promoted by high-intensity training. In this way, it could be suggested that IB might be functionally related to o2max. In support of this notion, a correlation between the increase in o2max and the increase in the range of IB after 6 months of training has been reported (17). The cyclists who volunteered in the present study were accustomed to training at intensities within the IB phase, and therefore, their larger IB could be viewed as a specific adaptation to the training regime. Longitudinal studies are, however, needed to verify the responsiveness of IB to training, also in relation to the different training strategies, and especially in older individuals.
In conclusion, the present data indicate that aging reduces the IB phase recorded during incremental maximal cycling exercise and that this is larger in competitive endurance cyclists, independent of age.
From a practical standpoint, the analysis of the IB phase can be used as a noninvasive tool to obtain indications about the capacity to compensate, or resist, the metabolic acidosis generated during exercise. It could also be used to control and monitor training intensity and adaptations. As a matter of fact, a model of exercise prescription using intensities below, at, or above IB has been presented (15) and used to characterize the physical effort during extreme endurance exercise, such as the Tour de France (14). The present data confirm that IB is sensitive to the training status and that it could be used to monitor exercise performance and training adaptation of both young and older individuals.
We thank our subjects for their time and effort. This study was supported by a grant (250-07) from Università degli studi di Roma Foro Italico. The results of the present study do not constitute endorsement of the product by the authors or the National Strength and Conditioning Association.
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Keywords:© 2011 National Strength and Conditioning Association
ventilatory threshold; respiratory compensation point; master athletes; isocapnic buffering