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European Journal of Heart Failure 2006 8(3):243-248; doi:10.1016/j.ejheart.2005.07.011
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© 2005 European Society of Cardiology

Maximum oxygen uptake corrected for skeletal muscle mass accurately predicts functional improvements following exercise training in chronic heart failure

John P. LeMaitre, Stuart Harris, Jim Hannan, Keith A.A. Fox and Martin A. Denvir*

Cardiology, Centre for Cardiovascular Science, University of Edinburgh United Kingdom

* Corresponding author. Cardiology, Western General Hospital Crewe Road, Edinburgh EH4 2XU. E-mail address: mdenvir{at}staffmail.ed.ac.uk


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Background: Skeletal muscle mass and peak oxygen uptake are important predictors of functional status and outcome in patients with stable chronic heart failure.

Aims: To assess changes in skeletal muscle mass and peak oxygen uptake following an exercise training program.

Methods: Thirty-six patients with moderate stable chronic heart failure were randomly allocated to either a bicycle ergometer (bike) or functional electrical muscle stimulators (FES) applied to quadriceps and gastrocnemius muscles to be used daily for six weeks. Dual-energy X-ray absorptionometry (DEXA) scanning was performed before and after training along with symptom limited cardiopulmonary exercise test, quadriceps strength and fatigue resistance, and 6-min walk test.

Results: Both exercise modalities resulted in improvements in treadmill exercise time, leg strength, 6-min walk test and peak oxygen uptake per kilogram of skeletal muscle. Despite significant improvements in functional capacity, there were no significant changes in body composition for total skeletal muscle mass, leg muscle mass or total body fat content. Skeletal muscle mass was strongly predictive of maximum oxygen uptake at baseline (r=0.61, p<0.001) and after exercise training (r=0.68, p<0.001).

Conclusions: In moderate stable chronic heart failure, exercise training using bicycle ergometer or FES results in favourable qualitative rather than quantitative changes in skeletal muscle. Correction of maximum oxygen uptake for skeletal muscle mass rather than total body mass is a more sensitive measure of changes associated with exercise training.

Key Words: Chronic heart failure • Dual energy X-ray absorptionometry • Body composition • Exercise training

Received March 5, 2005; Revised June 27, 2005; Accepted July 26, 2005


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 5. Conclusions
 References
 
Chronic heart failure is characterised by breathlessness, fatigue and poor exercise capacity. While circulatory insufficiency is the primary disorder it is now widely accepted that skeletal muscle in these patients has reduced strength and is more readily fatigued [1,2]. A number of histological abnormalities have been described in the skeletal muscle of chronic heart failure patients. Altered muscle fibre type distribution has been reported with a switch from slow twitch aerobic fibres to fast twitch glycolytic fibre types [3-6] although this has not been observed by all authors [7]. Molecular techniques have also linked changes in myosin heavy chain proteins to faster glycolytic myosin types [8] with reduced levels of enzymes involved in oxidative metabolism such as citrate synthase, succinate dehydrogenase and 3-hydroxyacyl CoA dehydrogenase [7,9,10]. Magnetic resonance techniques have demonstrated a reduced ability to replenish adenosine triphosphate (ATP), which appears to be a key metabolic abnormality [11,12]. The proposed mechanisms underlying these changes include reduced perfusion due to myocardial insufficiency, simple disuse atrophy and apoptosis induced by elevated local and circulating cytokines [13,14]. A number of exercise training programs have been shown to significantly improve functional capacity in CHF patients without significantly altering cardiac performance [15-18]. These studies have confirmed that although skeletal muscle has diminished function in CHF it can regain strength and power despite persistence of circulatory insufficiency.

We have previously demonstrated that a home-based program using skeletal muscle training by functional electrical muscle stimulation (FES) of quadriceps and gastrocnemius or bicycle ergometer for 6 weeks results in enhanced exercise capacity in patients with chronic heart failure [19]. FES is clearly different from standard dynamic exercise training. This study aimed to examine whether FES results in a distinctive change in the quality of skeletal muscle or whether an increase in muscle mass or bulk is responsible for the observed improvements in functional capacity. We therefore used dual energy X-ray absorptionometry (DEXA) before and after exercise training to examine changes in body composition and assessed the findings along with detailed characterisation of functional status including cardiopulmonary exercise testing.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 5. Conclusions
 References
 
2.1. Study population
Thirty-six patients with stable chronic heart failure, New York Heart Association (NYHA) class II to III, were recruited from a hospital cardiology clinic and randomised to one of two different exercise-training modalities. All subjects were limited in their ability to perform exercise by either breathlessness or fatigue as a consequence of heart failure. All patients had documented left ventricular impairment by echocardiography and were on stable medical therapy which included angiotensin converting enzyme (ACE) inhibitors, diuretic, digoxin and beta-blockers (Table 1). There were no patients with clinical characteristics of cachexia [20]. Patients were excluded if they had co-existing respiratory, neurological, orthopaedic or peripheral vascular disease that would prevent a bicycle exercise training program. Written informed consent was obtained from all subjects and the local research ethics committee approved the protocol. Twenty healthy age-matched control patients (9 female, 11 males) with no history of cardiac disease underwent DEXA scanning and are used as a baseline comparison group.


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  		Table 1 Baseline patient characteristics (mean (SD), bike-bicycle ergometer training group, FES—functional electrical stimulation training group)

 
2.2. Exercise-training regimes
Patients were randomised to receive either a recumbent bicycle ergometer (bike) or a functional electrical muscle stimulator (FES) for home use over a 6-week period. Those patients assigned to the bicycle group underwent a 1-h training session and were provided with a chest-strap/wrist heart rate monitor (Polar). The bicycle was delivered to their home and they were instructed to use it 5 days per week for 30 min aiming for a target heart rate of 70% of their previously determined maximum heart rate. Patients allocated to use FES (Sports Pro, Boditek Ltd, UK) underwent a 1-h period of instruction. Adhesive electrodes were placed on the skin over quadriceps and gastrocnemius muscles of both legs. The device was configured to deliver a direct electrical current at 25 Hz for 5 s followed by 5 s of rest. Patients used FES at home for 30 min daily on each leg, 5 days per week for 6 weeks.

2.3. Patient assessment
Patients underwent 6-min walk test, cardiopulmonary treadmill exercise test and quadriceps strength and fatigue testing on two separate occasions at least 24 h apart prior to randomisation and a mean of these was used as the baseline value. Cardiopulmonary exercise data were obtained during a symptom-limited modified Bruce treadmill exercise test and analysed using a zirconium fuel-cell oxygen analyser and infrared carbon dioxide analyser (Benchmark, Morgan Medical Ltd, UK). Peak oxygen uptake (VO2) is presented as the mean of absolute values (ml/min) and is also expressed per kilogram of total body weight (ml/kg/min) and per kilogram of skeletal muscle mass (ml/kg/min) obtained by body composition measurement. Actual measurements of peak VO2 were expressed as a percentage of predicted peak VO2 using a standard equation [21]. Isometric quadriceps strength was measured by a piezoelectric strain gauge attached to an exercise bench and was calibrated to provide a measurement of the equivalent weight lifted. A protocol to fatigue the quadriceps muscle was used whereby patients applied a force to the isometric bench equivalent to 30% of the previously determined maximum every 2 s for 40 s of every minute over 20 min [13]. Maximum quadriceps strength was repeated at the end of this time and fatigability index expressed as the ratio between the first and second maximal measurements. All assessments were repeated after the 6-week period of exercise training.

2.4. Dual energy X-ray absorptiometry (DEXA) scanning
A whole-body dual energy fan-beam scanning technique was used (Hologic QDR 4500A, USA). Measurement of lean tissue mass and fat mass by this technique has been validated previously [22]. Results are expressed as mean values from 2 scans obtained on the same day using Hologic software version 11.1 thus improving the overall precision of detecting a change between two time points. Total radiation exposure for each pair of scans was approximately 7 µSv, which is equivalent to one day of normal background radiation in the UK. A series of age-matched men and women from the local population with no history of cardiac disease or other co-morbidity were included as controls (Table 1, n=20). Whole body densitometry was used to calculate proportion of body fat, total skeletal muscle mass and bone mineral density.

2.5. Statistical analysis
Statistical analysis was performed using SPSS for Windows, version 11. A paired t-test and one way ANOVA were used to compare data with a normal distribution, a Mann-Whitney U test was used to compare data with uneven distribution. Data are presented as mean (standard deviation (SD)) unless otherwise stated. Correlations are expressed as univariate analyses and include 95% Confidence Intervals (95% CI). Chi-square (c2) was also used to compare groups. Significance was accepted at the 5% level (p<0.05).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 5. Conclusions
 References
 
The clinical characteristics of patients and controls are summarised in Table 1. Exercise groups were well matched for a range of clinical features. Healthy controls were also well matched for age.

There were no significant differences observed in the body composition of male and female CHF patients at baseline compared with age matched healthy controls for body fat, lean muscle mass and leg muscle mass (Table 2). CHF patients did have slightly lower total skeletal muscle mass and leg muscle mass but these differences did not reach statistical significance. There were similar improvements in treadmill exercise time, 6-min walk test, quadriceps muscle strength and fatigue resistance index in both exercise groups (Table 3). Correcting absolute oxygen uptake values for total body weight, there was no significant change in peak oxygen uptake (peak VO2) in either group comparing before and after training. At baseline, total body weight was not related to peak VO2 (r=–0.27, p=0.71) but was more closely linked with peak VO2 after exercise training (r=0.67, p=0.02). Peak VO2 expressed as a percentage of age-predicted peak VO2 was slightly lower in the Bike group at baseline and improved by only 4% after training while the FES group started slightly higher and demonstrated only a 1.5% improvement. However, when values for oxygen uptake were corrected for total skeletal muscle mass this revealed a significant improvement in peak VO2 in the bike group (49.5(14.7) to 57.2(13.6) ml/kg/min, p=0.01) and a trend for an increase in the FES group (48.6(15.4) to 54.0(14.1) ml/kg/min, p=0.06). Peak VO2 was strongly associated with total skeletal muscle mass both before (r=0.61, 95% CI 0.33 to 0.80) and after (r=0.68, 95% CI 0.41 to 0.84) exercise training for all CHF patients (Fig. 1). There was no clear relationship between improvements in peak VO2 and improvements in quadriceps muscle strength (r=0.11) or fatigue resistance (r=0.05). There was a negative association between baseline peak VO2 and the absolute change in peak VO2 after training (Fig. 2) suggesting that patients with lowest baseline peak oxygen uptake had a greater increase in peak VO2 following exercise training. Improvements in 6 min walk test were not associated with improvements in peak VO2 (r=0.17, 95% CI –0.13 to 0.44) but skeletal muscle mass-corrected peak VO2 was correlated with 6 min walk time at baseline (r=0.53, p<0.001, 95% CI 0.33 to 0.68) and this relation strengthened after training (r=0.60, p<0.001, 95% CI 0.36 to 0.77).


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  		Table 2 Baseline body composition: male and female CHF patients and controls

 


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  		Table 3 Change in functional assessment and body composition after training

 


Figure 1
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  		Fig. 1 Association between lean body mass and absolute VO2 after training (r=0.68, p<0.001).

 


Figure 2
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  		Fig. 2 Relation between baseline peak VO2 and absolute increase in peak VO2 (corrected for total skeletal muscle mass) r=–0.43, p=0.01, 95% CI –0.67 to –0.12.

 
There were no significant changes in total body skeletal muscle mass or leg muscle mass and no significant change in total body fat after the period of exercise training in either training group or when all CHF patients were analysed together. There was no significant change in bone mineral density in either group or when all patients (n=36) were considered together (1.072(0.025) to 1.077(0.026) g/cm2, p=0.25).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
5. Conclusions
 References
 
In this study, exercise training using static bicycle and functional electrical muscle stimulation in patients with chronic heart failure produced no measurable change in skeletal muscle mass, body fat content or bone mineral density. However, there was clear evidence of improvements in quadriceps muscle strength and fatigue resistance, and significant improvements in treadmill exercise time, 6 min walk test and peak maximum oxygen uptake corrected for skeletal muscle mass. In addition, we demonstrated that skeletal mass was closely associated with peak VO2 and that training-induced increases in peak VO2 were greatest in those patients with the lowest baseline peak oxygen uptake. These findings suggest that exercise training can result in significant improvements in functional capacity without increasing muscle mass and further confirms the close coupling of these two important prognostic markers, peak VO2 and skeletal muscle mass [20,23,24]. The findings suggest that patients with low baseline functional status and low skeletal muscle mass are able to benefit from exercise training. The question remains unanswered as to whether improvements in either of these parameters, muscle mass or peak VO2, by exercise training could alter mortality. There has been only one previous study suggesting that exercise training can improve prognosis [25] although a more recent meta-analysis of 9 studies has also supported this possibility [26]. Our study would suggest that, at least, short term exercise training will improve maximum oxygen uptake but that this can occur without a concomitant increase in total skeletal muscle mass suggesting the potential for uncoupling of these two factors. Furthermore it confirms the findings of other groups that patients with low baseline peak VO2 can gain more from exercise training [27] and could therefore potentially achieve more prognostic benefit compared with CHF patients with higher baseline VO2.

Bicycle training resulted in significant improvements in VO2 in keeping with a greater haemodynamic response to this form of training while FES resulted in a smaller increase of borderline significance. We were able to detect a change in peak VO2 by expressing absolute oxygen uptake per kilogram of skeletal muscle mass when there was no significant difference observed when this was estimated using total body mass. The reason for this difference is likely to relate to the accuracy of the DEXA scan in measuring the tissue contributing greatest to oxygen consumption during exercise, namely skeletal muscle mass. Since we demonstrated a strong relationship between muscle mass and peak VO2 both at baseline and after training (Fig. 1), while total body mass was only related to peak VO2 after training, this method is clearly a more sensitive way to detect change in oxygen consumption following training. This way of describing peak VO2 is not widely used mainly because accurate measurement of skeletal mass is only possible with DEXA or magnetic resonance imaging. Other workers have suggested it as a more accurate way of assessing cardiopulmonary function [28] and there is some evidence that it may also have stronger prognostic value [29]. Bicycle training is more likely to result in improvement in peak VO2 compared to FES because of the larger muscle groups recruited, such as gluteus maximus and rectus femoris. While there was no statistically significant difference in various measures of functional capacity between the two forms of training, bicycle training did result in slightly greater improvements in 6 min walk test and treadmill exercise time. This is likely to be a reflection of the greater improvement in peak VO2 in the Bike group. However, muscle specific assessments of function such as quadriceps strength and fatigue resistance, demonstrated very similar improvements for Bike and FES. The patients in our study had a wide range of functional baseline classification with most in NYHA class II and some having a peak VO2 close to that predicted for their age. Such patients are less likely to increase peak VO2 after exercise training and this may also partly explain why we did not see a significant improvement in this parameter when corrected for total body weight.

Since there was no significant change in body or leg muscle mass, the predominant change responsible for improved functional capacity must be related to qualitative changes in existing skeletal muscle. This further supports the notion of adaptability of skeletal muscle despite persistent circulatory insufficiency in CHF. Previous studies both in humans and in numerous animal models have demonstrated qualitative improvements in oxidative metabolism and high energy phosphate supplies [13] resulting from exercise training in heart failure. Our findings suggest that FES may also be able to influence these processes but possibly to a lesser degree than bicycle training. A limitation of our study is that it included younger CHF patients than are typical of a heart failure population. This may partly explain why our patients had a slightly higher peak VO2 than that reported in other similar studies [24]. Further larger trials including more elderly patients would be needed to confirm our findings.

One additional important finding is that despite the potential risk of extended rest while using the FES there was no significant reduction in bone mineral density in patients randomised to this treatment modality. This was probably related to the short duration of daily use and improved activity levels in all patients during the study as reflected by the improvements in functional performance.


   5. Conclusions
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Conclusions
References
 
This is the first study using DEXA scanning to follow-up heart failure patients that have undergone an exercise training program. The lack of change in body composition observed in our study could reflect the short time period for training, the relatively low intensity home-based program, the relatively young age and the small number of patients included. However, clear improvement in functional capacity observed for both forms of exercise, despite no increase in muscle mass, suggests the possibility for skeletal muscle to undergo qualitative adaptation during exercise training in CHF.


   Acknowledgements
 
This study was funded by the British Heart Foundation.


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

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