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European Journal of Heart Failure 2001 3(6):685-692; doi:10.1016/S1388-9842(01)00187-8
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© 2001 European Society of Cardiology

Early recovery of oxygen kinetics after submaximal exercise test predicts functional capacity in patients with chronic heart failure

Serafim Nanasa,*, John Nanasb, Christos Kassiotisa, Chara Nikolaoua, Eleytheria Tsagaloub, Demetrios Sakellarioua, Ioannis Terovitisb, Ourania Papazachoua, Stavros Drakosb, Antonios Papamichalopoulosa and Charis Roussosa

a Pulmonary & Critical Care Medicine Department, National and Kapodestrian University Papadiamantopoulou 20, Athens 115 28, Greece
b Clinical Therapeutics Department, National and Kapodestrian University Papadiamantopoulou 20, Athens 115 28, Greece

* Corresponding author. Tel.: +30-1-7236743; fax: +30-1-7242785. E-mail address: snanas{at}cc.uoa.gr (S. Nanas).


   Abstract
Top
 Abstract
1. Introduction
 2. Study populations and...
 3. Results
 4. Discussion
 References
 
Background: Oxygen (O2) uptake at peak exercise (VO2 peak) is an objective measurement of functional capacity in patients with chronic heart failure (CHF). The significance of recovery O2 kinetics parameters in predicting exercise capacity, and the parameters of submaximal exercise testing have not been thoroughly examined.

Methods and results: Thirty-six patients (mean age=48±14 years) with CHF and New York Heart Association functional class I [12], II [17], or III [7], and eight healthy volunteers (mean age=39±13 years) were studied with maximal and submaximal cardiopulmonary exercise testing (CPET). The first degree slope of O2 uptake decay during early recovery from maximal (VO2/t-slope), and submaximal exercise (VO2/t-slope)sub, were calculated, along with VO2 half-time (T1/2VO2). Patients with CHF had a longer recovery of O2 uptake after exercise than healthy volunteers, expressed by a lower VO2/t-slope (0.616±0.317 vs. 0.956±0.347 l min–1 min–1, P=0.029) and greater T1/2VO2 (1.28±0.30 vs. 1.05±0.15 min, P=0.005). VO2/t-slope correlated with the VO2 peak (r=0.84, P<0.001), anaerobic threshold (r=0.79, P<0.001), and T1/2VO2, a previously established estimate of recovery O2 kinetics (r=–0.59, P<0.001). (VO2/t-slope)sub was highly correlated with VO2/t-slope after maximal exercise (r=0.87, P<0.001), with the VO2 peak (r=0.87, P<0.001) and with T1/2VO2 after maximal exercise (r=–0.62, P<0.001). VO2/t-slope after maximal and submaximal exercise was reduced in patients with severe exercise intolerance (F=9.3, P<0.001 and F=12.8, P<0.001, respectively).

Conclusions: Early recovery O2 kinetics parameters after maximal and submaximal exercise correlate closely with established indices of exercise capacity in patients with CHF and in healthy volunteers. These findings support the use of early recovery O2 kinetics after submaximal exercise testing as an index of functional capacity in patients with CHF.

Key Words: Exercise recovery • Cardiopulmonary exercise testing • Heart failure • Functional capacity • Risk stratification

Received February 23, 2001; Revised April 17, 2001; Accepted July 18, 2001


   1. Introduction
Top
 Abstract
 1. Introduction
2. Study populations and...
 3. Results
 4. Discussion
 References
 
Oxygen (O2) uptake at peak exercise (VO2 peak) is considered an objective measurement of functional capacity with prognostic significance in patients with chronic heart failure (CHF) [1,2]. A low VO2 peak is the most reliable single criterion for heart transplantation candidacy [3–5], and percent predicted the VO2 peak has been used to risk stratify heart failure patients [6]. However, the VO2 peak is influenced by motivation and deconditioning [7], and some authors have questioned its reliability as a risk stratifier, or in the guidance of treatment for CHF patients [8]. Other indices, such as recovery O2 kinetics [9] and ventilatory response to exercise estimated by the VE/VCO2-slope [10], may improve the risk stratification of CHF patients.

Recent data support a high correlation between rate of decay in O2 uptake (VO2) during early recovery from exercise and exercise tolerance in patients with CHF. Half-time (T1/2VO2) and time constant of VO2 decay in early recovery from exercise are longer in CHF patients than in normal volunteers [11–14]. We hypothesized that the first-degree slope of VO2 would be more accurate in describing the first minute of recovery. Using this method, it was shown that, in patients with CHF, respiratory muscle performance is related to O2 kinetics during early recovery [15]. We further hypothesized that data from recovery after a submaximal exercise would predict maximal exercise performance in CHF patients. If confirmed, evaluation of their functional status could be performed by submaximal exercise, which is better tolerated than maximal exercise testing.

The objective of this study was to test the correlation between early recovery O2 kinetics after maximal and submaximal exercise tests and maximum exercise capacity in patients with CHF and healthy volunteers.


   2. Study populations and methods
Top
 Abstract
 1. Introduction
 2. Study populations and...
3. Results
 4. Discussion
 References
 
Thirty-six patients (32 males/4 females, mean age=48±14 years) with CHF and New York Heart Association (NYHA) functional class I [12], II [17], or III [7], and eight healthy volunteers (mean age=39±13 years) were studied (age difference not statistically significant). The investigation conformed to the principles outlined in the declaration of Helsinki. All patients were clinically stable at the time of study. Patients were receiving diuretics, digoxin and ACE-inhibitors during the study period. Patients with recent myocardial infarction, respiratory insufficiency or other conditions affecting exercise capacity were excluded from the study. The diagnosis of CHF was based on clinical criteria and laboratory testing, including blood chemistry, echocardiography, right heart catheterization and radionuclide ventriculography. Coronary angiography or myocardial biopsy was also performed if indicated.

2.1. Cardiopulmonary exercise testing
CPET was performed on a Marquette 2000 treadmill (Marquette Electronics). A Bruce or modified Naughton exercise protocol [16] was chosen to limit exercise duration to 15 min. The 12-lead electrocardiogram was recorded every minute with a MAX 1 system (Marquette Electronics). Blood pressure was measured every 2 min with a standard cuff mercury sphygmomanometer. A pulse oxymeter was used to monitor peripheral blood O2 saturation throughout the test. Patients and normal volunteers self-graded their degree of dyspnea during CPET using the Borg scale [17]. Breath-by-breath O2 uptake (VO2), carbon dioxide output (VCO2), and air flow were measured with a Vmax 229 monitor for pulmonary and metabolic studies (Sensormedics). The system was calibrated with standard gas of known concentration before each test. These measurements were obtained in the upright position before and during exercise, and in the sitting position for the first 10 min of recovery. Subjects did not perform cool-down exercise after maximal exercise. Baseline VO2 was calculated by averaging the measurements made for 2 min before the beginning of exercise.

The VO2 peak was calculated as the average of measurements made for 20 s before the end of exercise. Anaerobic threshold was determined using the V slope technique [18] and the result was graphically confirmed by plotting respiratory equivalent for oxygen (VE/VO2) and carbon dioxide (VE/VCO2) simultaneously against time. To evaluate O2 uptake kinetics during recovery, the first degree slope of VO2 for the first minute of recovery (VO2/t-slope) was calculated by linear regression, using a dedicated computerized statistical program (Fig. 1a). The first minute was chosen to guarantee that the measurements reflected the alactic phase of the repayment of O2 debt [19,20]. The time required for a 50% fall from the VO2 peak (T1/2 of VO2) was also calculated. When it occurred in the middle of two sampling points, T1/2 of VO2 was set at the second point [13].


Figure 1
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  		Fig. 1 Oxygen kinetics in a representative patient with CHF: (a) during maximal and (b) during submaximal exercise.

 
Patients and normal volunteers were instructed to exercise until they reached general exhaustion, dyspnea, or leg weakness. Subjects whose CPET was terminated because of lightheadedness, chest pain, or ominous arrhythmias were excluded from the study.

After a 1-h rest period, patients and healthy volunteers underwent a graded submaximal exercise test using the same protocol that was used during maximal exercise. The test was terminated when O2 uptake approached 75% of the previously determined VO2 peak. To evaluate O2 uptake kinetics during recovery, the first-degree slope of VO2 decay was determined once more for the first minute of recovery (VO2/t-slope)sub (Fig. 1b).

The interobserver variability of VO2/t-slope measurements was examined in a subset of 25 patients with heart failure. Two physicians calculated independently VO2/t-slope after maximal and submaximal exercise in this subgroup. There was minimal interobserver variability (r=0.98, P<0.001) in the VO2/t-slope calculation. Additionally interobserver agreement was verified by the method of Bland and Altman [21].

2.2. Hemodynamic and ventricular function measurements
Right heart catheterization was performed within 48 h of CPET, and left ventricular ejection fraction was measured by radionuclide ventriculography.

2.3. Statistical analyses
Results are presented as means±S.D. unless otherwise stated. The significance of differences between means was examined by paired or unpaired Student's t-test, as appropriate. One-way ANOVA was used to compare VO2/t-slope between groups classified according to Weber et al. [1]. Correlations were tested by Pearson's correlation coefficient. Equations were calculated by linear regression analysis. A P-value <0.05 was considered statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Study populations and...
 3. Results
4. Discussion
 References
 
Important baseline characteristics of CHF patients are presented in Table 1. Table 2 shows the results of CPET in patients vs. healthy volunteers. Eighteen patients were in Weber class A, 7 in class B, 10 in class C and 1 in class D. As expected, patients had a lower exercise capacity (measured as peak VO2) than healthy individuals (19.9±6.0 vs. 27.7±5.2 ml kg–1 min–1, P=0.003). Anaerobic threshold was found at a lower level of exercise in patients than control subjects (14.2±4.4 vs. 20.8±3.5 ml kg–1 min–1, P=0.001). Conversely, healthy volunteers reached a higher peak minute ventilation than CHF patients (88.3±29.3 vs. 62.0±18.6 l min–1, P=0.056) (borderline significance) although the slopes of VE/VCO2 and VE/VO2 indicated that patients with CHF hyperventilated. Patients with CHF also had a prolonged recovery of O2 uptake after exercise as evidenced by a lower VO2/t-slope (0.616±0.317 vs. 0.956±0.347 l min–1 min–1, P=0.029), and greater T1/2 of VO2 decay (1.28±0.30 vs. 1.05±0.15 min P=0.005) than healthy volunteers.


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  		Table 1 Baseline characteristics of 36 study patients

 


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  		Table 2 Cardiopulmonary exercise test parameters in patients with congestive heart failure vs. healthy volunteers

 
The correlation between the VO2/t-slope and the VO2 peak (r=0.84, P<0.001), or anaerobic threshold (r=0.79, P<0.001) was high (Fig. 2a). In addition VO2/t-slope correlated with T1/2VO2, a previously established estimate of recovery O2 kinetics (r=–0.59, P<0.001, Fig. 2b). In linear regression analysis, the VO2 peak as a function of VO2/t-slope was expressed as the VO2 peak (ml kg–1 min–1)=10.5+16.0 VO2/t-slope (l min–1 min–1). One-way ANOVA of VO2/t-slope in patients of different Weber classes showed a parallel decrease with exercise capacity (F=9.3, P<0.001).


Figure 2
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  		Fig. 2 (a) Scatter diagram of the VO2 peak as a function of VO2/t-slope. In linear regression analysis, the following equation was calculated: VO2 peak=10.5+16.0 VO2/t-slope, r=0.84, P<0.001. The VO2 peak=O2 uptake at peak exercise; VO2/t-slope=first degree slope of O2 uptake decay during the first minute of recovery. (b) Scatter diagram of T1/2VO2 as a function of VO2/t-slope (r=–0.59, P<0.001). T1/2VO2=half-time of O2 uptake decay during recovery; VO2/t-slope=first degree slope of O2 uptake decay during the first minute of recovery. (c) Scatter diagram of (VO2/t-slope)sub as a function of VO2/t-slope (r=0.87, P<0.001). VO2/t-slope=first degree slope of O2 uptake decay during first minute of recovery; (VO2/t-slope)sub=first degree slope of O2 uptake decay during the first minute of recovery after submaximal exercise. (d) Scatter diagram of the VO2 peak as a function of (VO2/t-slope)sub. In linear regression analysis, the following equation was calculated: VO2 peak=9.5+20.0 (VO2/t-slope)sub, r=0.87, P<0.001. The VO2 peak=O2 uptake at peak exercise; (VO2/t-slope)sub=first degree slope of O2 uptake decay during the first minute of recovery after submaximal exercise.

 
All study participants underwent submaximal exercise to 76.3±8.5% of the VO2 peak attained during the previous maximal exercise. CHF patients exercised to 76.6±9.1% and healthy volunteers to 75.1±5.6% of VO2 peak (P=NS). The (VO2/t-slope)sub was significantly lower in CHF patients than in healthy individuals (0.553±0.293 vs. 0.777±0.168 l min–1 min–1, P=0.009). Patients in Weber class A had a (VO2/t-slope)sub=0.750±0.285 l min–1 min–1, vs. 0.386±0.125 l min–1 min–1 in class B, vs. 0.338±0.109 l min–1 min–1 in class C/D (F=12.8, P<0.001). (VO2/t-slope)sub was highly correlated with indices of maximal exercise such as VO2/t-slope (r=0.87, P<0.001, Fig. 2c), VO2 peak (r=0.87, P<0.001, Fig. 2d) and T1/2 of VO2 (r=–0.62, P<0.001). In linear regression analysis, the VO2 peak (achieved at maximal exercise) as a function of (VO2/t-slope)sub was expressed by the equation VO2 peak (ml kg–1 min–1)=9.5+20.0 (VO2/t-slope)sub (l min–1 min–1). Correlation of (VO2/t-slope)sub with other indices of exercise capacity and hemodynamic measurements is presented in Table 3.


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  		Table 3 Correlation of VO2/t-slope after submaximal exercise with indices of maximal and submaximal cardiopulmonary exercise test and resting hemodynamic measurements

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Study populations and...
 3. Results
 4. Discussion
References
 
This study demonstrated that, compared to healthy volunteers, O2 uptake kinetics are prolonged after maximal and submaximal exercise in patients with CHF. Furthermore, the first degree slope of O2 uptake decay during the first minute of recovery from maximal and submaximal exercise was closely correlated with established indices of exercise capacity in patients with heart failure and in healthy volunteers.

The level of the VO2 peak attained depends on the patient's motivation, physical condition, familiarity with the procedures, and on encouragement by attending medical staff [7]. It has also been suggested that the peak VO2 is underestimated in obese patients, while it overestimates exercise capacity in the presence of muscle wasting [22]. These factors may have limited the accuracy of risk stratification and prognostic evaluation of a large subgroup of patients with a VO2 peak between 10 and 18 ml kg–1 min–1 [9]. Furthermore, exercise to exhaustion increases risk and discomfort in CHF patients. In contrast, submaximal exercise testing is suitable to evaluate heart failure by being more reflective of the patients’ daily activities. However, neither a standard submaximal exercise protocol, nor indices derived from submaximal protocols have been described.

On-line computer analysis and breath-by-breath studies of respiratory and metabolic parameters during exercise and recovery period have become widely available only recently, although the method was established earlier [23]. Using such data we have been able to study the early recovery (first minute) period, which constitutes the fast component of the repayment of the O2 debt [19,20]. This period is called the alactic phase because the O2 excess consumed is used to replete high-energy phosphate stores in skeletal muscle [19,24]. Assuming that the fall in VO2 during early recovery from exercise is linear, VO2 recovery in patients with CHF was examined in a linear regression model [15]. In the present study, VO2/t-slope and (VO2/t-slope)sub were significantly lower in CHF patients than in healthy volunteers. Severe exercise intolerance (class C/D in Weber classification) was associated with delayed recovery of resting O2 uptake. This is in agreement with observations by other investigators, who reported that recovery O2 uptake was significantly delayed in patients with CHF, and that the delay correlated with the degree of exercise intolerance [25]. Recently, recovery O2 kinetics was estimated using the slope of a single exponential relation between VO2 levels and time during the first 3 min of recovery [26]. It was found that VO2 recovery time was prolonged only in the presence of advanced heart failure [26].

In our study VO2/t-slope and (VO2/t-slope)sub despite a small difference, which did not reach statistical significance in CHF patients, showed similar correlation with indices of maximal exercise capacity (peak VO2). Koike et al. [11], using a submaximal constant-workload protocol, concluded that the time constant of VO2, during exercise and after recovery, is a useful and objective measure of exercise capacity. In heart failure patients, Cohen-Solal et al. [13], using graded exercise, showed that the kinetics of recovery O2 uptake did not change significantly whether patients exercised to 100 or 75% of peak workload. Additionally, investigators, using maximal and submaximal exercise [11,13,14,27], showed that the time constant of VO2 decay and concomitant T1/2VO2 were significantly prolonged in patients with CHF, and correlated well with peak VO2. A similar correlation was found in the present study (r=–0.63). The two indices used to estimate recovery O2 kinetics (VO2/t-slope and T1/2VO2) were correlated with an r=–0.59 value. The main limitation in the use of T1/2VO2 or time constant for the study of recovery period, is that such measurements encompass the whole period instead of the early alactic phase (early recovery). This may explain the relatively weak correlation between time constant and T1/2 of VO2 and VO2 peak in this and other studies [11]. VO2/t-slope describes O2 kinetics during the alactic phase and reflects more accurately the oxidative mechanisms of high-energy phosphate repletion during that period.

VO2 peak is an established prognostic index in CHF patients [3,4,28]. Recent reports suggest that peak VO2 depends on muscle mass [22], and that wasting and cachexia may affect survival in these patients [29]. Opasich et al. [9] have suggested that, in patients with peak VO2 in the range of 10–18 ml kg–1 min–1, indices such as recovery O2 kinetics may help improving risk stratification. In patients with moderate exercise intolerance (peak VO2>40% predicted), it was observed that the ratio between total O2 uptake during exercise and recovery was an independent prognostic marker [25]. Additionally, Scrutinio et al. [30] have shown that T1/2VO2 during recovery was an independent predictor of survival. In our study, the correlation of VO2/t-slope and (VO2/t-slope)sub with indices of maximal exercise capacity such as peak VO2 suggests that the more delayed the recovery of total body O2 uptake, the worse the cardiac performance, hence its prognostic value. This suggestion is supported by the correlation of VO2/t-slope and (VO2/t-slope)sub with indices of ventilatory response to exercise (VE/VCO2-slope), another independent prognostic factor in CHF patients [10]. In a recent study, a prolonged, >10% decrease in maximal inspiratory pressure in late recovery, among CHF patients with low exercise capacity and significantly prolonged recovery of O2 uptake was observed [15]. This is concordant with an inverse correlation of VO2/t-slope and (VO2/t-slope)sub with VE/VCO2-slope observed in the present study, meaning that when VO2 recovery is prolonged, the VE/VCO2-slope is steep, indicative, in these patients, of exercise-induced hyperventilation [31].

The prolonged recovery of total body oxygenation after maximal and submaximal exercise observed in our study may be attributable to slower recovery of muscle energy stores in CHF patients [13,15]. Recently Belardinelli et al. [27] reported that, after submaximal exercise, recovery of muscle oxygenation is prolonged. The slower recovery of muscle energy stores, seemingly independent of the exercise level, has been attributed to intrinsic histologic and biochemical muscle alterations [32], impaired O2 delivery to skeletal muscles during recovery from exercise [33], and vascular dysfunction in patients with CHF [34,35].

4.1. Clinical implications
Measurements made during the early recovery period, such as VO2/t-slope, may be used in the evaluation of exercise intolerance in CHF patients. Such measurements, derived from a submaximal exercise test, are independent of patient motivation and expose the subject to fewer risks.

4.2. Study limitations
The results of the present study apply mainly to patients with moderate exercise intolerance. The equations used to predict the VO2 peak from the VO2/t-slope will only be applicable to the whole population of patients with heart failure after a larger number of patients in NYHA class III and IV, and Weber class D have been studied. There are also no data concerning the prognostic significance of VO2/t-slope. Therefore data of prospective studies regarding risk stratification of patients with CHF would be of great value.

In summary, early recovery O2 kinetics after maximal and submaximal exercise are prolonged in patients with CHF, and are closely correlated with established indices of exercise capacity in patients as well as in healthy volunteers. These findings support the use of submaximal, instead of maximal, exercise tests in the evaluation of CHF patients.


   Acknowledgements
 
This study was funded by a grant from the special account for research grants of the National and Kapodestrian University of Athens.


   References
Top
 Abstract
 1. Introduction
 2. Study populations and...
 3. Results
 4. Discussion
 References
 

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K. K. Witte, W. C. Levy, K. A. Lindsay, and A. L. Clark
Biomechanical efficiency is impaired in patients with chronic heart failure
Eur J Heart Fail, August 1, 2007; 9(8): 834 - 838.
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