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European Journal of Heart Failure 2005 7(6):991-996; doi:10.1016/j.ejheart.2005.05.005
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© 2005 European Society of Cardiology

Metabolic gas kinetics depend upon the level of exercise performed

Klaus K.A. Wittea,*, Simon D.R. Thackray, Kenneth A. Lindsayb, John G.F. Cleland and Andrew L. Clark

a Department of Academic Cardiology, Castle Hill Hospital Castle Road, Cottingham, Hull HU16 5JQ, United Kingdom
b Department of Mathematics, Glasgow University, United Kingdom

* Corresponding author. Tel.: +44 1482 624073; fax: +44 1482 624071. E-mail address: klauswitte{at}hotmail.com


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Background: The kinetics of oxygen and carbon dioxide at the onset of and recovery from exercise are slowed in patients with chronic heart failure (CHF). The aim of the present study was to establish whether the kinetics of O2 are influenced by the work rate.

Methods: Thirteen CHF patients and 12 control subjects underwent bicycle-based peak exercise testing with metabolic gas exchange analysis. Each subject then exercised at 15%, 25% and 50% of the maximal workload achieved until reaching steady state. Time constants for onset (Tonset) and offset (Toffset) for O2 uptake and CO2 output were correlated to the workload and the percentage of peak VO2 performed during the steady state tests.

Results: Patients had lower peak oxygen uptake (pVO2) and the relation between ventilation and carbon dioxide output was steeper in patients than controls. Toffset for both oxygen (O2) and carbon dioxide (CO2) from peak exercise was significantly greater in the patients than the controls and correlated with peak VO2 (r=0.56, p<0.005 and r=0.58, p<0.005). Tonset and Toffset for O2 were increased in patients for each of the steady state tests and peak VO2 correlated with T for recovery of O2 (r=0.44; p<0.05 from 15%, r=0.35; p=<0.05 from 25%, and r=0.54; p<0.01 from 50%). There was a correlation between the Tonset (r=0.42; p<0.0005 for O2 and r=0.23; p<0.05 for CO2) and Toffset (r=0.49; p<0.0001 for O2 and r=0.42; p<0.0005 for CO2) and oxygen uptake as a percentage of peak exercise.

Conclusions: This study demonstrates that the time constants of onset and offset for oxygen are dependent upon the degree of exertion performed relative to the individual's peak capacity.

Key Words: Gas kinetics • Chronic heart failure

Received October 13, 2004; Revised February 2, 2005; Accepted May 10, 2005


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Chronic heart failure is a syndrome characterised by exercise intolerance due to breathlessness and fatigue [1]. Patients have reduced peak oxygen uptake (pVO2) [2] and an increased ventilatory response to exercise as shown by an increase in the slope relating ventilation to carbon dioxide output (VE/VCO2 slope) [3-5]. This correlates inversely with pVO2 so that the greater the ventilatory response, the lower the exercise capacity [3,4] and both pVO2 and VE/VCO2 are related to symptom scores and prognosis [6,7].

In response to the imposition of a fixed workload below the anaerobic threshold, VO2 does not increase in a stepwise manner but, rather, gradually to a plateau. An exponential curve can be fitted to this, describing the process in terms of the jump in VO2 requirement from rest to steady state and a time constant, T. A similar profile of response can describe the recovery of oxygen uptake (see Appendix) [8]. Previous investigators have shown that the time constants for onset (Tonset) and recovery (Toffset) of the metabolic gases are prolonged in patients with chronic heart failure compared with control subjects [9–11]. The degree of impairment of the kinetics of particularly oxygen correlates with peak exercise capacity, [10] neurohormonal status, [12] and prognosis [13,14]. The cause of this abnormality is unknown but does not seem to be related to muscle blood flow and oxygen transport into the working tissues [15,16]. It has been reported as a consequence of normal ageing [17]. However, the data examining onset and offset kinetics originate from either peak exercise [18,19] or fixed workload tests [8,20] and it is possible that the workload and duration of exercise influence the time constant of onset and recovery. If this were the case, the workload would need to be taken into account when assessing recovery rates in patients. This study was designed to explore the relation between metabolic gas exchange kinetics and workload in patients with heart failure and in control subjects.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
Thirteen patients with chronic heart failure and 12 control subjects participated in the study. Each subject gave informed, written consent prior to involvement in the study, which was approved by the local ethics committee. Chronic heart failure was defined as the presence of symptoms of fatigue or breathlessness on exertion and a left ventricular ejection fraction on echocardiography of less than 40% at rest with no other cause of breathlessness apparent. The condition had to be of at least three months duration with no recent exacerbation or change in medication in the preceding three months. All patients were taking optimal medical therapy including beta-blockers. We excluded patients with neurological conditions or inducible ischaemia upon exercise. Individuals in both groups were also excluded if there was any history of pulmonary disease or if their FEV1 was less than 80% of predicted. The controls were individuals of similar age chosen at random from the patient lists of local general practitioners. None was on regular medication and all underwent echocardiography to exclude left ventricular dysfunction.

After an initial familiarisation test, each subject underwent a symptom-limited peak electromagnetically braked bicycle-based exercise test (Rehcor, Cardiokinetics, Salford, UK). After an initial unloaded stage the load was increased by 25 W every 3 min until the subject was exhausted. During the tests patients wore a tightly fitting facemask to which was connected a flow meter and sample tube enabling on-line breath-by-breath ventilation and metabolic gas exchange measurements (Oxycon Record, Jaeger, Germany). The system was recalibrated prior to each test. A respiratory exchange ratio (RER), (VCO2/VO2), greater than 1 was taken as evidence of maximal effort. Standard spirometry (FEV1 and FVC) was also performed before the exercise test. Peak VO2 and the anaerobic threshold (AT), using the VCO2/VO2 slope method [21], were determined. The VE/VCO2 slope was calculated by linear regression.

The tests were then repeated on a separate occasion at fixed workloads of 15%, 25% and 50% of the resistance achieved at peak exercise. Each test was initiated from rest and continued until steady state was achieved [22]. This was taken to be the point at which no further changes in ventilatory or oxygen intake had occurred for at least 1 min. The order in which the tests were performed was randomised and each patient had 30 min recovery between each steady state test. The readings taken for the final minute of exercise were averaged to give steady state results.

We used unpaired Student's t-test for between-group comparisons of the baseline data. The time constants for onset (Tonset) and offset (Toffset) of exercise were calculated for CO2 and O2 (see Appendix) and correlated to the workload and the percentage of peak VO2 achieved during the steady state tests using linear regression. We also compared T for each level of work and peak using ANOVA with Fishers PLSD correction. A p value of <0.05 was taken to be significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
The baseline variables for the patients and control subjects are shown in Table 1. During the peak tests, patients had a shorter exercise time, a significantly lower peak oxygen uptake (pVO2), and the relation between VE and carbon dioxide (CO2) (VE/VCO2 slope) was steeper in patients than controls. Patients also exercised to a lower peak workload than controls.


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  		Table 1 Subject characteristics

 
3.1. Recovery constants from peak test
The values for Toffset for both oxygen and carbon dioxide from peak exercise were significantly greater in the patients than the controls (Table 1). Both correlated with peak VO2 (r=0.56, p<0.005 (Fig. 1) and r=0.58, p<0.005). There was a significant relationship between Toffset and peak VO2 for patients alone (r=0.12, p<0.05).


Figure 1
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  		Fig. 1 The relation between the time constant of offset of oxygen from maximal exercise and peak exercise capacity (pVO2) for patients (unfilled points) and controls (filled points).

 
3.2. Variables from steady state tests
Steady state was achieved for all subjects after 3 min of exercise. Oxygen uptake, ventilation and carbon dioxide were not different at rest between patients and controls and also between the repeated tests (Table 2). Although absolute VO2 and VCO2 were greater in controls than patients at each of the steady states when corrected for the differences in workload, by relating these values to those achieved at peak exercise, the patients had a greater VO2 and VCO2 at each stage than the controls. There was no difference in VE at the lower workloads but, at 50%, controls had greater absolute ventilation than patients. As with the metabolic gases, ventilation during the steady state tests as a percentage of that achieved at peak was significantly greater in patients for all of the submaximal tests. Each of the patients and control subjects exercised below their anaerobic thresholds at all levels of the repeated tests.


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  		Table 2 Time constants and steady state results

 
Constants for onset and recovery were significantly increased in patients when compared with controls for all levels of exercise and peak VO2 correlated with T for recovery of O2 from the steady state tests (r=0.44; p<0.05 from 15%, r=0.35; p=<0.05 from 25%, and r=0.54; p<0.01 from 50%). There was no difference between patients and controls in Tonset and Toffset of carbon dioxide during any of the submaximal tests. There was no correlation with age for either onset or offset of both oxygen and carbon dioxide in control subjects and patients.

There was no correlation between either Tonset or Toffset for oxygen or carbon dioxide and absolute oxygen uptake at steady state. Despite attempts to standardise the workload in order to achieve similar levels of exertion for patients and controls, subjects with chronic heart failure exercised at a greater proportion of peak than normal subjects (Table 2). We corrected for this by correlating these time constants with percentage of peak oxygen uptake rather than absolute oxygen uptake at steady state. There was a correlation between the Tonset of O2 and CO2 and the oxygen uptake as a percentage of peak exercise (r=0.31; p<0.05 for patients and r=0.39; p<0.02 for controls for O2 (combined in Fig. 2A) and r=0.21; p<0.05 for patients and r=0.35; p<0.05 for controls for CO2). There was also a correlation for the Toffset of both O2 and CO2 and oxygen uptake as a percentage of peak exercise (r=0.43; p<0.05 for patients and r=0.48; p<0.005 for controls for O2 (combined in Fig. 2B) and r=0.42; p<0.02 for controls and r=0.35; p<0.05 for patients for CO2). Fig. 3 shows that Toffset for O2 and CO2 from the steady state tests and from peak exercise increases as work increases as a percentage of peak.


Figure 2
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  		Fig. 2 A. The relation between the time constant of onset of oxygen during the steady state tests and degree of exercise performed for patients (unfilled points) and controls (filled points). B. The relation between the time constant of offset of oxygen during the steady state tests and the degree of exertion performed for patients (unfilled points) and controls (filled points).

 


Figure 3
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  		Fig. 3 The time constants of offset from each of the steady state tests and peak for oxygen (unfilled) and carbon dioxide (filled) (*p<0.001, **p<0.0001 for difference between steady state and peak test (100%)).

 
The respiratory exchange ratio was significantly greater at all of the steady state tests in patients (Table 2). This is despite the significantly lower workload and absolute VO2 and VCO2 of the patients than the controls.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
This study shows that time constants of recovery depend upon the preceding workload and the proportion of the maximal capacity of the exercising individual that it represents. Previous reports have examined this phenomenon during recovery from peak exercise [18,19] or fixed-load exercise [8,20]. This makes assessment of the degree of impairment of metabolic gas kinetics difficult, as recovery from peak exercise is potentially physiologically significantly different from recovery from submaximal or subanaerobic exercise. Similarly, a fixed workload test represents a different proportion of maximal capacity to each subject, possibly confounding the assessment of kinetics in a group of patients with a wide variability in exercise capacity.

In this study, the percentage of maximal exercise capacity performed during steady state tests correlated with the time constants of recovery and onset for oxygen. This was seen in patients with heart failure and in control subjects. The apparent impairment of metabolic gas kinetics demonstrated by previous investigators following peak exercise and fixed workload tests might therefore be a consequence significant impairment of exercise capacity with patients exercising at a greater proportion of their maximal capacity even at low workloads. We were unable to demonstrate a slowing of carbon dioxide kinetics between workloads. This suggests that at low workloads carbon dioxide kinetics are less affected than oxygen kinetics.

We also demonstrated increased RER values in patients at each level of steady state exercise. Since oxygen uptake by the active skeletal muscles is not impaired [23], this suggests that there is an increase in carbon dioxide output consistent with increased anaerobic exercise even at low workloads. This implies that patients with chronic heart failure are, even at low workloads, already more ‘anaerobic— than control subjects. Moderate exercise below the anaerobic threshold in healthy individuals leads to a lactic acidosis, which can impose a slowing of the onset kinetics of oxygen [24]. This might be the cause of the apparent discrepancy between the oxygen kinetics and those of carbon dioxide at low levels of work.

Patients with chronic heart failure have generalized muscle atrophy and a relative decrease in the concentration of the oxidative (type I) muscle fibres [25,26]. They are therefore more dependent on the fast twitch glycolytic (type IIb) fibres during exercise which fatigue rapidly [27]. The anaerobic environment that occurs as a consequence of this altered metabolism might contribute to the increased time constants of onset and offset seen in heart failure. We have demonstrated in Fig. 2 that the time constants increase with workload. This might be due to the worsening local acidosis when a greater workload is imposed.

Exercise restriction in heart failure has been linked to metabolic abnormalities in the peripheral muscles [28] and training in chronic heart failure leads to improvements in exercise capacity which are linked to changes in the proportions of the major types of skeletal muscle fibre in the periphery [29]. It is possible that training, which can reverse the structural changes associated with wasting [30] and improve the oxidative capacity in the peripheral muscles [31,32], might reduce the level of anaerobic metabolism. This would lead to a reduction in RER during the early stages of exercise, shortened time constants of onset and offset and thereby improved recovery rates.


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
References
 
We have shown that the time constants of onset and offset for oxygen are dependent upon the degree of exertion performed relative to the individual's peak capacity. This should be taken into account when such analyses are performed both in patients with heart failure and in control subjects.

These results are important to patients with chronic heart failure, for whom the activities of daily living represent a significant percentage of their maximum exercise tolerance. They therefore spend a greater proportion of their lives recovering from previous exertion, which has bearing on their ability to perform subsequent tasks. The use of rapidly fatiguing fast twitch skeletal muscle fibres for low workload activities by patients with heart failure might contribute to the slow recovery and the symptoms of fatigue.

The method of calculation of the time constants has been presented elsewhere [8]. Briefly, the experimental procedure collects data in three distinct phases, each of typical duration 10 min. During the first phase of the experiment, the subject is at rest and the corresponding state variable X (VO2, VCO2 or VE) takes the constant value A. The second stage of the experiment involves a period of uniform exercise during which the state variable X migrates to a new steady state A+B where the value of B is dependent on the level of exercise. During the final phase of the experiment, the subject rests and X once more relaxes towards its resting value A. Fig. 4 illustrates the general shape of the response of X to the experimental procedure.


Figure 4
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  		Fig. 4 The profile of state variable X is illustrated. A is the baseline level of X and B is the jump in level required to sustain the exercise program over a prolonged period of time. Shaded areas A1 and A2 represent, respectively, the deficit and surfeit of X as a consequence of the transitions in X induced by exercise.

 
The biological model and formulae in Fig. 4 assume, first, that a given level of exercise is sustained by a constant value of X (e.g. oxygenation level of the blood) and, second, that X adjusts to changes in exercise at a rate which is proportional to the imbalance between its current value and the value to be attained. It is demonstrated easily that A1, the deficit in X at the onset of exercise, and A2, the surfeit in X at the cessation of exercise are respectively A1=BTe and A2=BTr where Te and Tr are the time constants for exercise and relaxation.

The parameters A, B, Te and Tr for any subject are found by fitting the entire solution for X(t) to observations which in this experiment are heavily contaminated by noise. The parameter estimation procedure assumes that the noise is purely a result of imperfections in measurement and has mean value X(t) and constant standard deviation {sigma} (to be determined by the fitting procedure). Under these assumptions, the parameters A, B, Te, Tr and {sigma} are chosen to minimise the sum of squares


Formula

where the observations are (t1,X1), (t2,X2), ...(tn,Xn).


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 

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