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Research Reports |
F Chung, PT, is Section Head, Surgical and Critical Care Physiotherapy, Physiotherapy Department, Burnaby Hospital, Burnaby, British Columbia, Canada. This study was completed in partial fulfillment of the requirements of Mr Chung's Master of Science degree
E Dean, PhD, PT, is Professor, School of Rehabilitation Sciences, University of British Columbia, T325-2211 Wesbrook Mall, Vancouver, British Columbia, Canada V6T 1Z3 (elizdean{at}rehab.ubc.ca). Address all correspondence to Dr Dean
J Ross, PT, is Section Head, Critical Care, Rehabilitation Services, Vancouver General Hospital, Vancouver, British Columbia, Canada
Submitted December 4, 1997;
Accepted January 11, 1999
 | Abstract |
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=49.7, SD=9.3), to negative work (eccentric muscle contractions) and to positive work (concentric muscle contractions) were compared. Subjects and Methods. Subjects performed the 2 types of work on a motorized cycle ergometer at pedaling frequencies of 35, 55, and 75 rpm with a constant power output of 60 W. Steady-rate values of oxygen consumption (
O2), heart rate (HR), minute ventilation (E), tidal volume (VT), and breathing frequency (fb) were obtained during 6 test conditions (positive and negative work at each of the 3 pedaling frequencies). Results. Values for all measures were greater during positive work than during negative work, except for fb. During positive work, values for all variables were greatest at 75 rpm, except for fb. During negative work, O2 and HR were greater at 75 and 35 rpm than at 55 rpm, and E and VT were greater at 75 rpm than at 55 rpm. Breathing frequency was not different among pedaling frequencies. Conclusion and Discussion. The results confirmed that negative work performed on a cycle ergometer is associated with low metabolic cost in older men without cardiopulmonary disease. Although E was determined primarily by changes in VT during negative work, a comparable disproportionate increase in fb was observed at the start of negative work. Such changes in breathing patterns have implications for the prescription of negative work for patients with lung disease.
Key Words: Cardiopulmonary responses • Concentric contraction • Cycle ergometry • Eccentric contraction • Negative work • Older men • Positive work • Speed
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During negative work, there is a decrease in minute ventilation (E) that parallels the decrease in oxygen consumption (O2) obtained when these variables are compared with positive work across the same work rates.17–19 Little is known, however, about the effects of negative work on the components of E, namely, tidal volume (VT) and breathing frequency (fb). Dean and Ross38 reported rapid shallow breathing in subjects without cardiopulmonary impairments during downhill walking on a treadmill at 3.5 mph with a -7% grade. They further observed that the fb and VT responses were not consistent with the notion that downhill walking is merely a low-intensity form of positive work. Dean and Ross38 proposed that postural adjustments of the chest wall or restriction of abdominal wall motion, or both, during downhill walking may contribute to the observed rapid shallow breathing response.
In addition to the reduced energy cost of negative work compared with positive work, the energy cost of a given work rate may be affected by the pedaling frequency when a bicycle ergometer is used for exercise. Optimal values for walking speed and pedaling frequency have been reported.17,33,39-41 Banister and Jackson40 reported that a low work rate achieved with a high pedaling frequency and low resistance is metabolically equivalent to a much higher work rate achieved with a low pedaling frequency and high resistance. Although optimal pedaling frequencies for different work rates during positive work have been identified, such values for negative work are less clear.
The literature to date on both negative and positive work includes descriptions of energy cost at different work rates, but these descriptions are based primarily on the responses of young subjects without cardiopulmonary impairments.8,9,13,42–45 Despite the well-known physiological consequences of aging46–48 and age-related changes in response to conventional exercise during positive work, the responses of older adults to negative work are not known.
The purpose of our study was to compare the responses of middle-aged men (39-65 years of age) to negative and positive work performed on a cycle ergometer at different pedaling frequencies. We studied an older age group because a large proportion of individuals with chronic disabilities who are frequently seen in rehabilitation settings are in their middle to later years. We used a cycle ergometer to minimize postural adjustments that may affect breathing patterns when performing negative work, such as those that occur during downhill walking on a treadmill.38 We hypothesized that negative work performed on a cycle ergometer by older men without cardiopulmonary impairments is not physiologically equivalent to low-intensity positive work when performed at the same work rate and that the physiological responses to negative work are physiologically distinct compared with physiological responses to positive work.
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O2, HR, E, VT, and fb.
Subjects
Twelve middle-aged men with no history of cardiopulmonary disease, based on a medical history questionnaire, volunteered to participate in the study. The subjects were aged 39 to 65 years (=49.7). No subject had participated in any formal exercise program or training over the past year. A detailed explanation of the research design and purpose of the study was given to each subject. Each subject signed an informed consent form.
Equipment and Measures
The subjects' height and weight were recorded, and their body mass index (BMI) was calculated (ie, weight [in kilograms]/height [in square meters]).
Cycle ergometer.
The assembly of the bicycle ergometer is shown in Figure 1. All parts were bolted onto 2 connected rigid wooden frames with wheels. The wheels of the wooden frames were securely braked during testing to maintain the stability of the assembly.
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A standard cycle ergometer (Monark model 817E*) was modified to perform positive and negative work according to the description by Bigland-Ritchie and colleagues.49 The pedaling frequency was held constant by a constant current feedback control, the output of which was also displayed by a digital output gauge. This control allowed a pedaling frequency ranging from 0 to 120 rpm. The maximum allowable torque that could be registered at the pedals was 70 N for pedaling frequencies ranging from 40 to 120 rpm. At pedaling frequencies less than 40 rpm, the maximum allowable torque decreased in proportion to the decrease in pedaling frequency. The original friction belt braking system of the ergometer was retained for forward pedaling or positive work and for calibration. In this motor-driven cycle ergometer, the pedaling frequency is controlled by the motor and the load is controlled by the subject. A second set of pedaling frequency and torque output gauges were placed in front of the subject to provide direct visual feedback.
Both pedaling frequency and torque output gauges were calibrated prior to testing and recalibrated whenever there was a change in pedaling frequency or work setting. The pedaling frequency output gauge was calibrated by matching the pedaling frequency measured with a stopwatch to the pedaling frequency that was registered on the pedaling frequency output gauge. Subsequently, the torque reading was zeroed at each test speed. Torque calibration was done in the forward direction using the original friction band on the ergometer as reference. The friction band on the ergometer was tightened to a known resistive force, and the torque digital output gauge was calibrated to match the resistive force. Torque calibration for the reverse direction was tested using the original friction band and a known resistive force and was identical to torque calibration for the forward direction. Therefore, for a given pedaling frequency, the torque calibration performed in the forward direction also served to calibrate the reverse direction. These procedures constituted the calibration for each pedaling speed for both positive and negative work (ie, pedaling in the forward and backward directions).
Metabolic measurement cart.
A Sensormedics Metabolic Measurement Cart (MMC)
was used during exercise testing to perform breath-by-breath gas sampling. Subjects were connected to the MMC by a headpiece assembly and a mouthpiece. A noseclip was used in a attempt to avoid air leakage through the nose. Expired gas was then analyzed at 15-second intervals during testing. Measures included O2, E, VT, and fb. Before each test, the MMC was calibrated according to the operator-guided calibration procedures recommended by the manufacturer, using specific calibration gases. Heart rate and rhythm were continuously monitored using a 3-lead electrocardiographic (ECG) monitor,
which was calibrated before each test.
Other measures.
For safety reasons, arterial oxygen saturation(SaO2), blood pressure, and perceived exertion were monitored throughout the test sessions. Arterial oxygen saturation was measured using an oximeter
with an earlobe sensor. Blood pressure was measured manually using a brachial cuff and stethoscope at 1-minute intervals throughout each test by the same experienced individual. Subject reports of breathing difficulty were recorded every minute. A modified Borg Rating of Perceived Exertion Scale50 was used to measure breathing difficulty. The scale ranged from 0 ("nothing at all") to 10 ("very, very strong"). Tests were carried out in a temperature-controlled exercise laboratory (21°±2°C).
General Procedures
Performance of positive work.
Subjects were seated for forward cycling or positive work in the same manner as for negative work. The clutch of the motor mechanism was engaged in the forward position. An extra 10-N load was added to the predetermined resistance for each subject to prevent damage to the motor by inadvertently driving it above its set speed. A lap seat belt was fastened to stabilize the subject. The standard distance of the chair from the pedals was determined by the length of the fully extended lower extremity with the pedal positioned vertically and the pedal arm positioned horizontally. The distance of the seat from the pedals was then adjusted for subject comfort prior to the start of testing (no more than 10 degrees of knee flexion was allowed). Because the tension generated by a muscle is, in part, based on its resting length,51 care was taken to ensure that each test was performed at a comparable seat position for each subject. The subject's feet were strapped into position on the pedals. The subject was encouraged to relax the upper body and trunk while allowing the lower extremities to cycle. After the test pedaling frequency was set by the tester, the subject pedaled forward to assist the cycle ergometer with sufficient effort so that the torque output fell to 10 N. The motor maintained the pedaling frequency set by the tester while the subject assisted the movement of the pedals until the desired torque reading was registered. The subject then maintained the same effort for the duration of the test.
Performance of negative work.
The friction band was left slack while the motor drove the pedals in the reverse (backward) direction. At the designated pedaling frequency set by the tester, the subject was directed to resist the movement of the pedals until the desired torque reading was registered. A forced stretch, therefore, was imposed on the same muscles that were used to generate power during conventional cycling using concentric muscle contractions. The rate at which the muscles were "worked upon" was the power being transferred to the subject.37 The subject was then told to maintain the required torque throughout the test.
Performance of free pedaling.
For free pedaling prior to exercise with positive work, the seated subject placed his feet in the appropriate position on the pedals, and then the feet were strapped into place. He was instructed to relax while the motor drove the feet around at the desired pedaling frequency. The subject maintained foot contact with the pedals while passively allowing the pedals to carry the legs around forward. During the test session, the subject free pedaled at the test pedaling frequency during the warm-up and cool-down periods. The procedure was the same for free pedaling prior to exercise with negative work, except that the subject allowed the pedals to carry the legs around in the backward direction.
Practice sessions.
All subjects attended at least 2 practice sessions (2 subjects required 3 practices) of positive and negative work. A subject was deemed to have learned the negative work cycling technique when he could maintain a given torque output for 1 minute over a range of torques. Our initial pilot work suggested that negative work cycling was more difficult to learn than positive work cycling. No major difficulty, however, was encountered with the practice and test sessions. Practice sessions were also used to familiarize the subjects with the testing environment, general procedures, and monitoring equipment. Practice sessions lasted an average of 25 minutes and were designed to promote a learning effect while minimizing any training effect.
Test protocol.
After completion of the practice sessions, subjects completed the two test conditions (ie, positive and negative work) using the cycle ergometer. Tests were conducted at least 1 week apart.
Subjects were requested not to have a large meal at least 3 hours prior to testing and not to consume any substances that contained stimulants (eg, coffee, soft drinks with caffeine). They were asked to have a restful 24-hour period prior to testing and to wear comfortable attire and shoes when they visited the exercise laboratory.
When a subject arrived at the exercise laboratory on each test day, his height and weight were measured and pulmonary function testing was done, including 3 trials of forced expiratory maneuvers for calculation of forced vital capacity and forced expiratory volume in 1 second. These routine pulmonary function measurements were taken to rule out pulmonary dysfunction.
For each test, the subject relaxed while seated on the testing chair, which was adjusted for leg length and comfort, for at least 5 minutes. The ECG electrodes were attached. The subject was then connected to the MMC by means of the headpiece assembly and the mouthpiece, and a noseclip was applied. The subject inspired room air via a low-resistance, one-way valve. The subject was then again asked to relax in this comfortable position for another 3 minutes while resting metabolic measurements were taken. Baseline physiological measurements were usually taken in the second to third minute of the test when O2 and HR of the subject had stabilized, that is, deviation was less than 2%.
After warming up with free pedaling for 2 minutes, the subject pedaled at the assigned pedaling frequency (the first of the 3 randomized pedaling frequencies) and power output. After a steady-state was reached (usually within 3 minutes) data, were collected for 5 to 7 minutes before the test at the assigned pedaling frequency was terminated. The subject free pedaled during the cool-down period for several minutes. Vital signs were continuously monitored until they were within 15% of the baseline values. The subject then rested for 30 minutes prior to being tested at the next pedaling frequency. This procedure was continued until tests at all 3 pedaling frequencies were completed. This protocol was repeated on the second test day for the other type of work.
Data Analysis
Descriptive statistics for the 5 dependent variables for each of the 6 steady-state tests were calculated. Arterial saturation and blood pressure were recorded as a safety precaution, and the data were not included in the analysis of the present study.
A 2 x 3 (2 types of work and 3 pedaling frequencies) factorial design for repeated measures on both factors was used to analyze the data. An analysis of variance (ANOVA) for repeated measures was used for each of the 5 dependent variables. Multivariate ANOVAs for repeated measures were used to analyze the main effects for pedaling frequency and the interaction when the assumptions for ANOVA for repeated measures were violated, resulting in inflated probability values.52 Newman-Keuls post hoc tests were used to test the effect of pedaling frequency when a significant omnibus F value was found.
Linear regression was used to determine the relationship between VT and E, fb and E, HR and O2, and E and O2 during both positive and negative work. The regression lines for each of the 4 relationships were tested for homogeneity of the regression coefficients between positive and negative work. An alpha of less than .05 was used as the critical value for the statistical tests.
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All exercise tests were performed without any untoward episodes. The average SaO2 was 97%, and this variable remained stable throughout exercise testing. The ECG and blood pressure measurements were within normal limits during rest, during exercise, and after exercise recovery for all subjects. The Borg subjective rating of breathing difficulty averaged one unit for both positive and negative work during the steady-state portions of the exercise tests. The baseline values preceding positive and negative work represent a composite mean of the 3 baseline periods for each test day.
Oxygen Consumption
Descriptive statistics (means±standard deviations) for O2 are shown in Figure 2. During positive work, the O2 values were 1.04±0.13, 1.12±0.13, and 1.25±0.13 L/min for pedaling frequencies of 35, 55, and 75 rpm, respectively. During negative work, the O2 values were 0.64±0.17, 0.55±0.14, and 0.67±0.24 L/min for pedaling frequencies of 35, 55, and 75 rpm, respectively.
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O2 was lower during negative work than during positive work (P<.001), and there was an effect of pedaling frequency on O2 (P=.002). Post hoc tests revealed that O2 during positive work was higher at 75 rpm (1.25±0.13 L/min) than at 35 rpm (1.04±0.13 L/min) and 55 rpm (1.12±0.13 L/min) (P<.05). During negative work, O2 was higher at 75 rpm (0.67±0.24 L/min) than at 55 rpm (0.55±0.14 L/min). There was also an interaction (P<.01) showing that O2 increased linearly during positive work and that O2 was lowest at 55 rpm (0.55±0.14 L/min) during negative work.
Heart Rate
Descriptive statistics (means±standard deviations) for HR are shown in Figure 3. During positive work, the HR values were 93.0±9.4, 95.4±10.5, and 99.2±12.1 bpm for pedaling frequencies of 35, 55, and 75 rpm, respectively. For negative work, the HR values were 82.5±11.5, 77.8±14.0, and 85.1±15.4 bpm for pedaling frequencies of 35, 55, and 75 rpm, respectively.
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Minute Ventilation
Descriptive statistics (means±standard deviations) for E are shown in Figure 4. During positive work, the E values were 24.6±4.9, 26.2±5.7, and 29.4±6.0 L/min for pedaling frequencies of 35, 55, and 75 rpm, respectively. For negative work, the E values were 16.0±4.1, 14.8±4.2, and 18.6±7.2 L/min for pedaling frequencies of 35, 55, and 75 rpm, respectively.
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E was lower during negative than during positive work (P<.001), and there was an effect of pedaling frequency on E (P<.01). Post hoc tests revealed that E during both positive and negative work was higher at 75 rpm (29.4±6.0 L/min and 18.6±7.2 L/min, respectively) than at 55 rpm (26.2±5.7 L/min and 14.8±4.2 L/min, respectively) and 35 rpm (24.6±4.9 L/min and 16.0±4.1 L/min, respectively) (P<.05). There was no interaction.
Tidal Volume
Descriptive statistics (means±standard deviations) for VT are shown in Figure 5. During positive work, the VT values were 1.40±0.31, 1.41±0.30, and 1.57±0.35 L/breath for pedaling frequencies of 35, 55, and 75 rpm, respectively. For negative work, the VT values were 0.93±0.24, 0.93±0.29, and 1.12±0.41 L/breath for pedaling frequencies of 35, 55, and 75 rpm, respectively.
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Breathing Frequency
Descriptive statistics (means±standard deviations) for fb are shown in Figure 6. During positive work, the fb values were 18±4.1, 19±3.6, and 19±4.2 breaths/min for pedaling frequencies of 35, 55, and 75 rpm, respectively. For negative work, the fb values were 18±6.3, 17±4.7, and 18±5.8 breaths/min for pedaling frequencies of 35, 55, and 75 rpm, respectively. The results of the ANOVA showed that there were no differences in fb between positive and negative work or among pedaling frequencies.
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O2 during positive work is described by the equation HR=62.1+(29.8)O2, and the Pearson product-moment correlation coefficient (r) was .42 (P<.05). The HR and O2 relationship during negative work is described by the equation HR=52.0+(47.8)O2, and the Pearson r was .66 (P<.05). The slopes and intercepts of the regression lines between positive and negative work for the relationship of HR and O2 did not differ (P>.05).
The relationship between E and O2 during positive work is described by the equation E=–8.86+(31.4)O2, and the Pearson r was .81 (P<.05). The E and O2 relationship during negative work is described by the equation E=1.24 +(24.4)O2, and the Pearson r was .85 (P<.05). The slopes of the regression lines between positive and negative work for the E and O2 relationship did not differ, and the intercept was smaller during positive work (P<.05).
The relationship between VT and E during positive work is described by the equation VT=0.89 + (0.022)E, and the Pearson r was .39 (P<.05). The VT and E relationship during negative work is described by the equation VT=0.51+(0.030)E, and the Pearson r was .49 (P<.05). The slopes and intercepts of the regression lines between positive and negative work for the VT and E relationship did not differ.
The relationship between fb and E during positive work is described by the equation fb=9.62+(0.34)E, and the Pearson r was .51 (P<.05). The relationship between fb and E during negative work is described by the equation fb=11.08 + (0.393)E, and the Pearson r was .39 (P<.05). The slopes and intercepts of the regression lines between positive and negative work for the fb and E relationship did not differ.
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Effects of Steady-Rate Cycling on Oxygen Consumption
Oxygen consumption during negative work was about 55% that for positive work at the constant work output of 60 W. There was more variation in O2 among subjects during negative work than during positive work. The lower O2 associated with negative work is well-established in the literature.1,3,4,8–10,13,17,18 At the correspondingly low work rate of 60 W, these studies showed that the energy cost measured by O2 during negative work ranged from 45% to 65% of the energy cost measured by O2 during positive work.1,10,13,17,18 The coefficients of variation (CVs) (standard variation divided by the mean) reported in the literature for O2 during negative work range from 1.4 to 4.4 times those reported for O2 during positive work.10,13,37,43 In our study, the average CV for O2 during negative work was about 2.5 times that for O2 during positive work. The lower O2 is explained by the increased elastic energy generated during negative work compared with positive work.1,3,4,8–10,13,17,18 The higher CV during negative work, however, has not been explained previously. It could reflect the novelty involved in this activity compared with more conventional forward pedaling during positive work.
Banister and Jackson40 observed large variations in O2 when pedaling frequency varied during positive work on a cycle ergometer at a constant power output. A subsequent study by Gaesser and Brooks54 further illustrated this point. As observed in our study, O2 increased with pedaling frequency during positive work, with O2 being greatest at the highest pedaling frequency of 75 rpm. Less is known about the effect of pedaling frequency on O2 during negative work performed at a constant work rate. Researchers8,17 have reported a gentle rise in O2 with increasing work rate during negative work. Furthermore, Knuttgen et al17,18 reported that lower O2, HR, and E occurred at 60 rpm during negative work when compared with 20 and 100 rpm at a low work rate similar to that used in our study. This finding, however, was not explained. Our work needs to be extended to study in detail the O2 during negative work at intermediate pedaling frequencies such as 55 rpm. Even though O2 at 55 rpm was not different from O2 at 35 rpm, we believe further study is needed to determine whether a pedaling frequency of 55 rpm is more efficient than lower and higher pedaling frequencies using our model.
When E and HR were plotted against O2 during both positive and negative work, linear relationships were found (P<.05). These results also showed that, at a work rate of 60 W, E and HR during both positive and negative work increased correspondingly with O2. The intercepts of the E and O2 regression lines differed between positive and negative work (P<.05). Thomson19 reported comparable E when comparing positive and negative work using a cycle ergometer at the same O2. Other researchers,17,18,38 however, have reported that both E and HR were higher during negative work than during positive work when compared at the same O2. The E and O2 relationship that we reported is similar to previously reported relationships.17,18,38 Studying a wider range of exercise intensities would have enabled us to examine these relationships more thoroughly.
Effects of Steady-Rate Cycling on Heart Rate
In this study, the HR response followed the same trends as O2 during positive and negative work. Because O2 and HR are highly correlated,55,56 this similarity could be expected. Although not statistically significantly lower, such a trend in HR measured at 55 rpm during negative work may reflect the lower O2. From our observation, a cadence of 55 rpm, which approximates an intermediate speed that an individual would self-select, may be associated with less co-contraction, which may reduce peripheral vascular resistance, thus lowering the HR. Whether there is a true difference needs to be established in a study with a larger sample size.
Effects of Steady-Rate Cycling on Minute Ventilation and Its Components
Minute ventilation during both positive and negative work was not different at 35 and 55 rpm, but an increase in E was observed at 75 rpm. Moreover, there was no interaction in this study reflecting a negligible difference in trend between positive and negative work. A lower E at 55 rpm was also reported by Knuttgen et al.17,18 This phenomenon was likely related to a lower metabolic demand at 55 rpm.
Changes in E reflect changes in its components, VT and fb. In the steady-state component of this study, this fb was statistically the same for all 3 pedaling frequencies in both positive and negative work. Variation in VT, therefore, largely explained the change in E. When VT and fb were plotted against E during positive and negative work, however, positive linear relationships between VT and E and between fb and E were found (P<.05). The potential importance of these findings needs further clarification, given that the ranges for all 3 variables (ie, E, VT, and fb) were relatively small. To illustrate, the mean difference for E between positive and negative work was 15 L/min and the mean difference for fb was only 2 breaths/min. In addition, the mean increase in VT during exercise ranged from 18% to 32% of mean force vital capacity. Thus, the change in VT could explain the increase in E in this ventilatory range. Furthermore, the lowest mean E, observed at 55 rpm during negative work, could be explained by the low fb (Fig. 4).
The ventilatory responses observed in our study during low-intensity exercise resemble those reported in the literature.57–59 In theory, for a given E, there is an optimal combination of VT and fb that minimizes the work of the respiratory muscles.57–61 Ventilatory responses have been described as having 2 stages (range 1 and range 2), which enable the respiratory system to adapt efficiently to increasing demands imposed by exertion. Range 1 is characterized by a small change in fb with a linear increase in VT to account for the increase in E observed during low levels of exercise (ie, associated with a VT of less than 50% of vital capacity).57–59 In addition, range 1 is characterized by shortening of the expiratory duration (Te), with no change in inspiratory duration (Ti).61 Range 2 is characterized by a relatively constant VT of about 50% of vital capacity, whereas fb accounts for most of the increase in E associated with moderate to high intensities of exercise.57,59 Both Ti and Te are shortened in range 2.61
In our study, the mean VT was below 50% of the mean forced vital capacity during both steady-state positive and negative work. In addition, the changes in fb and VT followed closely those described above for range 1. The strong positive linear relationship between VT and E in this study, regardless of the type of work, is consistent with the characteristics of range 1 described by Hey et al.58 The results of our study, therefore, showed that at a low work rate of 60 W, the VT and E relationship during positive work is qualitatively similar to that during negative work for the 3 pedaling frequencies.
The negligible change in fb observed in our study over the 3 pedaling frequencies for each type of work probably reflects the relatively low intensity of the exercise; therefore, we believe that it represents the flat plateau stage of range 1. The negligible change in fb may reflect entrainment or coordination of fb to exercise rhythm.58,62–64 Entrainment of fb to exercise rhythm is characterized by adopting an fb that is a multiple (subharmonic frequency) of the exercise rhythm.64 The fb values in our study were similar for the 3 pedaling frequencies for each type of work, resulting in an overall mean fb of 18 breaths/min. The mean fb of 18 breaths/min was approximately the second, third, and fourth subharmonics of the pedaling frequencies 35, 55, and 75 rpm chosen in our study. The subjects' fb may have been entrained onto the subharmonic of the exercise rhythm. Examination of the individual data indicates that only 2 subjects entrained their fb to 18 breaths/min, which is a multiple of their exercise rhythm. Furthermore, the VT and E relationship had a positive intercept, which does not support any contribution of entrainment of fb to exercise rhythm.59 In summary, the relationship of both fb and VT to E during both positive and negative work can be described by the range 1 ventilatory response described in the literature. To verify this conclusion, Ti and Te will need to be measured in future studies.
Changes in Minute Ventilation and Its Components From Baseline to Steady-Rate Exercise
With negative work, the increase in E from baseline to steady-rate exercise was low compared with positive work (Fig. 4). This finding reflects the characteristics of negative work (eg, metabolically less demanding compared with positive work). This change in E during negative work was associated with relatively small changes in VT (ie, 0.85 L/breath at baseline to 0.93 L/breath at 35 and 55 rpm to 1.12 L/breath at 75 rpm) (Fig. 5). In contrast, for positive work, the increase in VT were more marked (ie, 0.81 L/breath at baseline to 1.4 L/breath at 35 and 55 rpm to 1.57 L/breath at 75 rpm). Figure 6 shows that for negative and positive work, fb increased statistically to the same extent from baseline to steady-rate exercise. Thus, despite the difference in E between positive and negative work during steady-rate exercise, the ventilatory response from baseline to steady-rate exercise at a power output of 60 W showed a comparable quantitative increase in fb for positive and negative work. The difference in E for positive and negative work from baseline to steady-rate exercise, therefore, can be explained by a differential increase in VT. For negative work, the increase in E from baseline to steady-rate exercise was largely effected by an increase in fb with a relatively small increase in VT. In contrast, for positive work, the increase in E from baseline to steady-rate exercise was effected by increases in both VT and fb.
Although a comparable quantitative increase in fb was observed for positive and negative work, this increase appears to be disproportionately high in negative work, given its relatively low intensity, compared with positive work. In addition, this observation is not consistent with the typical range 1 ventilatory response that was evident in positive work. The predominant increase in fb during negative work at the start of exercise has been reported by Dean and Ross.38 The mechanism for this ventilatory response to negative work is unclear. Dean and Ross,38 who observed rapid shallow breathing during downhill walking, acknowledged that this response may be related to factors other than negative work (eg, postural stabilization). In our study, we believe that we eliminated the role of postural stabilization because subjects were in a sitting position and were performing negative work on a cycle ergometer.
Exercise Responses of Older Subjects to Steady-Rate Cycling
We found individual variation in response to negative work, especially at the highest pedaling frequency of 75 rpm. Two of the oldest subjects, for example, showed a relatively high O2 (ie, 1.0 and 1.2 L/min) during negative work at 75 rpm. When a box plot, as described by Wilkinson,52 was used to map the distribution of O2 at 75 rpm during negative work, the subject with a O2 of 1.2 L/min was an outlier. Tests were repeated for these 2 subjects, and the results were comparable to the results of each of these subjects' initial tests. Two factors could explain this finding. First, one subject appeared to be tense throughout the test sessions, particularly during negative work at 75 rpm. The subject needed to frequently be reminded to relax his upper body. Tension could increase the O2 due to isometric work. The greater O2 observed for the other subject, however, was apparently not associated with an increase in upper-body stabilization. An alternate explanation is that negative work for this subject involved relatively more concentration and coordination to perform than for the other subjects. Shock and Norris65 reported that neuromuscular coordination generally decreases with age. Other authors also have reported a corresponding decrease in muscle torque at high velocities of muscle contraction66,67 and in the number of motor units.66
Vandervoort et al48 reported that older subjects do not perform activities requiring rapid muscle contraction because of biomechanical factors. In our study, it is possible that other muscle groups not normally involved in performing negative work were active. This additional work could explain the increase in O2. Another hypothesis is that age-related changes of the series elastic component reduce the muscle's ability to use elastic energy generated during negative work. Aging has been reported to induce degenerative changes in the fibroelastic tissue,46 which may also affect the series elastic component of muscle. Thus, older people may lose the normal integrity of the fibroelastic connective tissue, making it less able to perform negative work. This hypothesis was not examined in our study.
Clinical Implications
Patients with severe exercise limitations who are unable to benefit from conventional positive work may be able to derive additional benefit from negative work because it can be performed with less active muscle contraction and thus less energy cost and ventilatory demand than the same workload in positive work.68 The results of our study have confirmed that negative work is not physiologically comparable to low-intensity positive work and that negative work can be tolerated by older individuals. Whether negative work is better tolerated by patients who are prone to rapid, shallow breathing (eg, patients with restrictive lung disease) compared with patients who require prolonged inspiratory and expiratory respiratory phases (eg, patients with chronic air flow limitation) remains to be elucidated.
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The data confirm and extend previous findings that the ventilatory responses to negative work compared with positive work, especially ventilatory demands, are decreased commensurate with oxygen demand at a given work rate. The effect of pedaling frequency on ventilation during negative work led us to conclude that E was determined primarily by a change in VT because fb was not different among the 3 pedaling frequencies between the 2 types of work. Considering the effect of negative work versus positive work, changes inE from baseline in our study appear to be influenced primarily by a disproportionate increase in fb in relation to VT. This finding sheds new light on the ventilatory responses described by range 1 for low-intensity exercise. This finding has implications for patients who require long time constants (ie, prolonged inspiratory and expiratory phases). Thus, further investigation into the unique effects of the work type versus pedaling frequency on ventilation is warranted. In addition, further study is needed to elucidate the mechanism underlying these responses.
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This study was supported, in part, by funding from the Canadian Lung Association.
* Sammons-Preston Canada, 3219 Yonge St, Ste 326, Toronto, Ontario, Canada M4N 2L3. 
Summit Technologies Inc, 840-71 H Ave SW, Ste 900, Calgary, Alberta, Canada T2P 3G2.
Hewlett-Packard Co, 3495 Deer Creek Rd, Palo Alto, CA 94304.
Datex-Ohmeda (Canada) Inc, 1093 Meyerside Dr, Unit 2, Missisauga, Ontario, Canada, L5T 1J6.
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