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European Journal of Heart Failure 2004 6(1):101-107; doi:10.1016/j.ejheart.2003.07.008
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© 2004 European Society of Cardiology

Muscle strength as a predictor of long-term survival in severe congestive heart failure

Martin Hülsmanna,*, Michael Quittanb, Rudolf Bergera, Richard Crevennab, Christoph Springerc, Martin Nuhrb, Deddo Mörtla, Petra Moserc and Richard Pachera

a Department of Cardiology University of Vienna, Währinger Gürtel 18-20, A-1090 Vienna, Austria
b Department of Physical Medicine and Rehabilitation University of Vienna, Vienna, Austria
c LBI of Cardiovascular Research University of Vienna, Vienna, Austria

* Corresponding author. Fax: +43-1-408-1148. E-mail address: martin.huelsmann{at}univie.ac.at


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 References
 
Aims: The objective of the study was to test the relationship between isolated muscle strength and outcome, and its significance in the context of other exercise variables.

Methods and results: 122 consecutive patients (LVEF 21±7%) were enrolled in the study. Isokinetic strength testing of the knee extensor and flexor muscles were performed. A subset of 51 patients underwent additional upright bicycle testing with gas exchange analysis. The outcome up to 60 months was defined by event-free survival (group A, n=59) or death (group B, n=34). Patients who had been transplanted were excluded from further analysis. The peak strength of the quadriceps muscle was comparable in both groups (N.S.). In contrast, the index (value adjusted for weight) did reveal significant differences (P<0.04), similar to the peak torque of the knee flexor muscle (P<0.04), whose index was even more significant with regard to differences (P<0.01). Multivariate analysis including muscle strength variables, pVO2 and workload into one model show that the flexor strength index is the only independent variable (x2=9 P<0.003). A cut-off point of 68 Nmx100/kg in the strength index of the flexor muscles was used to establish a significant difference between groups with regard to outcome (P<0.01). Thus, the isokinetic strength of the knee flexor muscles is related to outcome. Moreover, this parameter is superior to variables such as peakVO2 and workload.

Key Words: Heart failure • Muscle • Strength • Prognosis • Exercise

Received November 26, 2002; Revised May 12, 2003; Accepted July 2, 2003


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 References
 
Exercise capacity is limited in patients with congestive heart failure [1–3]. Although presumed, correlations between exercise capacity and hemodynamics or blood flow are lacking [4]. A lack of oxygen supply is unlikely to play a major role [5]. Specific alterations of the muscle itself might be the main factor involved in exercise intolerance [6,7]. Indeed, alterations such as loss of mitochondria, muscle fiber shift and loss of muscle mass, which are in part disease specific, are known to occur in the presence of CHF [8]. The underlying mechanism remains unclear. The influence of neurohormones or cytokines is under investigation [9–11].

Tests such as workload or peakVO2 primarily focus on the endurance of patients, which are known to be reduced [1,2], whereas acute force production is initially preserved, [10,12]. This is attributed to a loss of type I fibers, which are responsible for endurance [13]. Despite a consecutive increase in type II fibers, strength decreases with the severity of disease. A good correlation between surrogate parameters of outcome, such as wasting [7] or TNF{alpha} [9] levels, are known to exist. Whether acute force production is directly related to outcome is yet unknown.

The aim of the study was to determine whether acute force production of isolated muscle groups is related to outcome, Moreover, the significance of these parameters in the context of different exercise parameters as peakVO2 and workload was tested.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 References
 
A total of 122 consecutive patients with congestive heart failure were enrolled. Inclusion criteria were as follows: patients in clinically stable condition, LVEF below 35%, and the ability to undergo exercise testing. Follow-up was evaluated at visits to the out-patient unit or by telephone. The mean follow-up period was 24±17 months (range, 0.5–60 months).

2.1. Patients were stratified according to their outcome
Group A comprised patients who were stable at the end of the study.

Group B consisted of those who died within the observation period.

Group C included patients who were transplanted within the observation period. (Group C was excluded from further outcome analysis to avoid bias secondary to elective transplantation).

All patients gave informed consent and the study was approved by the local ethics committee. The investigation conforms with the principles outlined in the Declaration of Helsinki.

2.2. Strength testing procedures
For measurement of isokinetic strength of the quadriceps muscle and the hamstring muscle, we used the leg extension apparatus of the Cybex 6000 dynamometer (Cybex, Henley, USA). The Cybex 6000 dynamometer was calibrated for torque and range of motion according to the manufacturer's specification. The method was adapted to patients with chronic heart failure, and is described elsewhere in detail [14]. In short, for the purpose of acclimatization, the device was explained to the patients and both isokinetic and isometric contractions were demonstrated until the patients felt confident about the maneuvers. During this period of acclimatization, only contractions with less effort were allowed. Warming up consisted of three sets of three submaximal isometric and isokinetic repetitions with increasing effort. After a relaxation period of a few minutes, the test series was started. The patients first performed three reciprocal knee extension and flexion movements with an angular speed of 60 degrees per second with maximal effort. The reciprocal pattern was selected because it seemed easier to perform for the patients and has been given preference in recent studies. The highest achieved value was regarded as the peak torque. Both legs were tested; the first leg was chosen randomly. The dominant leg was determined by asking the patients which leg they would use to kick a ball. Two complete tests as described above were performed, separated by a 15-min interval (tests 1 and 2). All tests were performed by the same technician; only moderate standardized verbal encouragement was given during the test. The peak torque of the knee extensor and hamstring muscles were adjusted by weight (strength index) according to the following formula: strength (Nm)x100/body weight (kg).

2.3. Cardiopulmonary exercise testing
Upright bicycle tests with gas-exchange analysis were performed. All patients were familiar with the method and had performed a qualifying exercise test prior to randomization. Heart rate was continuously monitored by ECG and blood pressure was measured at rest and every 2 min during exercise. A ramp pattern exercise protocol was calculated for each patient according to the formula of Wassermann et al. [14,15]. Workload was increased until volitional fatigue, dyspnea, leg pain or a drop in blood pressure was registered. Expired gas was analyzed with a commercially available Vmax metabolic measurement cart (Sensormedics Corp) that was calibrated before each test. Oxygen consumption at maximal exercise (peakVO2) was measured by the breath-by-breath method.

2.4. Neurohumoral measurements
At index evaluation, blood samples of a subset of 85 patients were drawn from an antecubital vein after 30 min of resting. The samples were centrifuged, transferred into chilled tubes and placed on ice. Plasma was frozen at –20 °C until it was assayed. N-ANP (by ELISA), and big-ET (by RIA) were determined using commercially available kits, all purchased from BIOMEDICA, Austria. BNP (by ELISA) was determined with a commercially available kit purchased from Biosite Diagnostics, San Diego, USA.

2.5. Statistics
Continuous variables are expressed as means±standard deviation. For group comparison of continuous variables, a two-tailed Student's t-test was used. Categorical variables were evaluated with Fisher's exact test. Cut-off points were estimated by a receiver operator curve.

Pearson's correlation coefficient was calculated to assess correlation between data.

A Cox proportional hazards regression analysis was performed to identify independent predictors of 1-year event-free survival. The model was built in a stepwise fashion; the P-value for entering and staying in the model was set at 0.05.

In the first model, the following variables were entered: isokinetic strength of the flexor muscle corrected for body weight, peakVO2, workload, and NYHA classification.

In the second model, the following variables were entered: isokinetic strength of the extensor muscles and their values corrected for body weight, isokinetic strength of the flexor muscles and their values corrected for body weight, and beta-blocker therapy.

In the third model, the following variables were entered: isokinetic flexor muscle strength corrected for body weight, BNP, N-ANP, and big-ET 1.

ROC: To compare different predictive values at the endpoint, areas under the curve for sensitivity and specificity was constructed. The best predictive cut-off for survival was defined as that which gave the highest product of sensitivity and specificity.

Kaplan–Meier survival analysis and the log-rank test were used to compare event-free survival over time between patients with an isokinetic strength corrected for body weight of the flexor muscles.


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 References
 
3.1. Demographics
Of 122 patients, 59 remained stable (group A), 34 died (group B), and 29 patients had to be excluded because of transplantation (group C).

RAAS antagonists were administered in 122 patients, beta-blockers in 63, digitalis in 101, and diuretics in 102. The mean LVEF was 21±7%, 108 patients were male, and 70 cases were of ischemic origin. The distribution of NYHA functional classes was as follows: NYHA I, 11 patients; NYHA II, 42; NYHA III, 46; NYHA IV, 23. There were no significant differences between groups with the exception of the prescription rate for beta-blockers (see Table 1).


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  		Table 1 Demographics

 
3.2. Isokinetic peak torque protocol
The peak torque of the quadriceps muscle was similar in both groups (A: 111±45 vs. B: 98±37 Nm N.S.). In contrast, the index did reveal significant differences (A: 132±47 vs. B: 112±35 Nmx100/kg P<0.04). The peak torque of the knee flexor muscle significantly differed between those who survived and those who died (A: 64±29 vs. B: 51±24 Nm; P<0.04). Adjusting the peak torque to weight increases the difference between groups (A: 79±30 vs. B: 62±25 Nmx100/kg; P<0.01) (Fig. 1).


Figure 1
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  		Fig. 1 Differences in knee muscle strength dependent on outcome. Light bars=survivor, black bars=death. Units for extensor and flexor strength=Nm. Units for extensor and flexor strength index=Nmx100/body weight (kg).

 
3.3. Receiver operator curve and Kaplan–Meier life time analysis
A cut-off point of 68 Nmx100 /kg in the strength index of the flexor hamstring muscles-was calculated by a ROC (Fig. 2) as the best value to distinguish between group A and B. Specificity was 72% and sensitivity 60%. This cut-off value was used to determine a significant difference between those patients who died within a follow-up period of 60 months (P<0.01) (Fig. 3).


Figure 2
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  		Fig. 2 Mortality predictive accuracy of flexor strength index is illustrated with ROC for sensitivity and specificity.

 


Figure 3
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  		Fig. 3 Kaplan Meier lifetime analysis of survival stratified by peak torque index of the knee flexor muscles at a cut-off point of 68 Nmx100/kg body weight.

 
3.4. Correlation between systemic exercise performance and muscle strength
Fifty-one patients underwent upright bicycle exercise and measurement of peak VO2. Mean values were remarkably low (pVO2 12±4 ml/kg per min, workload 75±28 watts). There was no significant difference between groups (pVO2: group A 12±4 vs. group B 13±4 ml/kg per min; workload: group A 80±28 vs. 69±26 watts). Workload (W) and strength parameters are significantly correlated (W vs. extensor strength 0.3, P<0.01; W vs. extensor strength index 0.4, P<0.002; W vs. flexor strength 0.4, P<0.002; W vs. flexor strength index 0.4, P>0.002). This was also true for peak VO2 and strength (pVO2 vs. extensor strength 0.5, P<0.0001; pVO2 vs. extensor strength index 0.3, P<0.02; W vs. flexor strength 0.5, P<0.0001; W vs. flexor strength index 0.6, P>0.0001).

Multivariate analysis, including muscle strength, pVO2 and workload into one model revealed that only the flexor strength index is an independent predictor of outcome (flexor strength index x2=8 P<0.005) (Table 2)


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  		Table 2 Univariate and multivariate predictors of outcome

 
3.5. Neurohormones and muscle strength
Mean levels of big-endothelin 1 (4.8±7 fmol/ml), N-ANP (16 116±18 215 fmol/ml) and BNP (600±554 fmol/ml), as assessed in a subgroup of 64 patients, are at or above the cut-off point of poor outcome known from the literature [21].

The above mentioned parameters did not correlate with any parameter of muscle strength. N-ANP (17 062±18 881 vs. 13 411±16 370 fmol/ml N.S.), BNP (669±634 vs. 494±433 fmol/ml N.S.) and big-ET-1 (5.7±9.5 vs. 3.8±2.7 fmol/ml N.S.) are comparable in patients with a flexor muscle strength index below or above the cut-off point of 68 Nmx100/kg.

Multivariate analysis, including the flexor strength index, BNP, N-ANP and big-ET-1 in the model, reveal that N-ANP and flexor muscle strength are independent predictors of outcome (N-ANP x2=11, P<0.001; flexor index x2=6, P<0.02).

3.6. Beta-blockers and muscle strength
As the groups differed significantly in terms of beta-blocker therapy, and beta-blocker therapy is related to outcome (Table 1), we investigated the interrelationship between therapy and strength. Mean values of the flexor strength index were comparable in patients who received beta-blockers (72±29 Nmx100/kg) and those who did not (67±27 Nmx100/kg). Patients with flexor strength index values below the cut-off point of 68 Nmx100/kg received similar beta-blocker therapy as did those above the cut-off point of poor outcome. Moreover, multivariate analysis, including flexor and extensor strength as well as beta-blocker therapy reveal that flexor strength and beta-blocker therapy are independent variables of outcome (flexor index x2=12 P<0.007, beta-blocker x2=6 P<0.02).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
References
 
Fatigue and the inability to undergo exercise, expressed as NYHA functional class, peak VO2 [1] or workload [2] were clearly shown to be major symptoms of CHF and also are good predictors of survival.

As confirmed by our data there is a good correlation between systemic (pVO2 and workload) and local exercise performance (muscle strength). Moreover, several authors have detected an interrelationship between muscle strength or fatigue and surrogate parameters of outcome such as wasting [7] and TNF-{alpha} [9,11]. Thus, a correlation between muscle strength and outcome is evident. Our data are the first to show the good predictive value of muscle strength in patients with severe chronic heart failure. More importantly, flexor strength index is a better predictor of long-term outcome than workload or peakVO2 and they do not give any additional information.

4.1. Muscle: mass or morphology
Two major components of the muscle are abnormal in CHF. The obvious phenomenon is the reduction of muscle mass. In healthy individuals, muscle mass is correlated to exercise performance. Measurements of muscle diameter demonstrate a reduced muscle bulk even in mild CHF, and an association with the severity of disease [6] and exercise performance [4]. However, several publications conclude, that muscle mass only in part influences endurance [6] and strength [7] in CHF. This is in accordance with our data, which showed that the isokinetic strength of extensor and flexor muscles corrected for body weight, increases the significance of the association between peak torque and the severity of disease. Alterations in mitochondrial content, reduced cytochrome oxidase activity [8] and succinate dehydrogenase [12,13] might lead to decreased energy turnover and, subsequently, to premature exhaustion and weakness. Conversely, training is shown to resolve those abnormalities in patients with CHF [16] and thereby increase exercise tolerance [17].

Another important finding in recent years was a shift of muscle fiber from slow-twitch type I to fast-twitch type II in congestive heart failure [13]. The first fiber type is predominantly responsible for endurance, whereas the latter mainly alters strength. This alteration, which appears to be specific for heart failure patients, reduces endurance. In patients with mild to moderate heart failure, Massie [12] showed a reduction in exercise capacity—both systemic and local—but registered similar strength as in healthy controls. With advancing disease, strength is significantly reduced in patients compared to controls. Patients with various severities of CHF were found to be similar in terms of the endurance of local muscle, but differed in extensor strength [7]. Thus, the reduction in oxygen activity in type II fibers might be primarily blunted by an increase in the quantity of fibers, and only when severity of the disease increase strength will be also affected.

4.2. Extensor and flexor strength
The above mentioned investigations were focused on extensor muscle strength. Interestingly, in contrast to flexor strength our population does not differ in respect to extensor strength. Moreover, the predictive value of the former is superior to the latter. The reason for this is unknown and can only be hypothesized.

Daily activity and physical training affect predominantly the extensor muscle groups. Thus, the amount of flexor muscle strength might mirror the degree of the disease not influenced by different physical behavior of the patients.

Differences in muscle composition offer a further explanation. The knee extensor muscle is mainly composed of slow-twitch antigravity muscles, whereas knee flexor muscles belong to the fast-twitch fiber group. The ratio of type I/type II fibers is 45%/55% in the former, whereas it is approximately 65%/35% in hamstring muscles [18]. Buller [19] compared the quadriceps and the adductor pollicis in heart failure patients. He found a significant decrease of force production in the slow-twitch fiber muscle, but no changes in the adductor pollicis. The authors attributed this difference to reduced blood flow, which is primarily seen in a large muscle mass. Although they registered a significant decrease in measured fatigue after circulatory occlusion of the adductor pollicis, they report no data regarding alterations in acute force production. The fact that the strength of this muscle did not decrease may also have been due to its different fiber composition.

4.3. Neurohormones and strength
The association between a decrease in muscle work and chronic heart failure remains unclear. Our data suggest that neurohormones are not primarily involved in this process. This is underlined by the fact that workload or pVO2 are independent markers of outcome when compared with several neurohumoral parameters [2,20]. Niebauer [10] found no correlation between insulin-like growth factor and exercise or muscle variables. However, TNF-{alpha} levels were negatively correlated with strength [9] and muscle fatigue [11]. Thus, the influence of cytokines on muscle strength warrants further investigation.

4.4. Limitations of the study
As our patient group differed in respect to beta-blocker therapy, it may be presumed that this therapy influences muscle strength. This would be in accordance with previous reports [21], which state that distinct beta-blockers increase exercise capacity. However, no correlation was found between the administration of beta-blockers and the level of muscle strength. Moreover, the patients did not differ in respect to muscle strength, regardless of whether or not they received beta-blocker therapy. Multivariate analysis revealed that beta-blocker therapy and flexor strength are independently related to outcome.


   Acknowledgements
 
We thank Doris Sponner for attending to the patients, Eva Moser for the determination of neurohumoral values and data collection and Monika Knötig for support of the determination of the exercise variables.


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

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