Isokinetics and Exercise Science 13 (2005) 111â117. 111. IOS Press. Endurance training increases aerobic capacity but does not affect isokinetic leg muscle.
111
Isokinetics and Exercise Science 13 (2005) 111–117 IOS Press
Endurance training increases aerobic capacity but does not affect isokinetic leg muscle strength in chronic heart failure Francis Degache a,∗, Paul Calmelsb , Martin Gareta , Jean-Claude Barth´el´emya , Antoine Da Costac, Karl Isaazc, Fr´ed´eric Costesa and Fr´ed´eric Rochea a
Laboratoire de Physiologie, Groupe PPEH, Service d’Exploration Fonctionnelle CardioRespiratoire, CHU Nord, Facult´e de M´edecine Jacques Lisfranc, Universit e´ Jean Monnet, Saint-Etienne, France b Service de M´edecine Physique et R e´ e´ ducation, Groupe PPEH, CHU Bellevue, Facult e´ de M´edecine Jacques Lisfranc, Universit´e Jean Monnet, Saint-Etienne, France c Service de Cardiologie, CHU Nord, Facult e´ de M´edecine Jacques Lisfranc, Universit e´ Jean Monnet, Saint-Etienne, France
Abstract. Background: In patients with CHF, physical reconditioning improves exercise tolerance and endurance capacity. However, there is no evidence that endurance training programs affect skeletal muscle strength in such patients. Design: The present study investigates the effects of endurance training on isokinetic skeletal muscle strength and on aerobic capacity in chronic heart failure (CHF) patients. Methods: Eleven stable CHF patients (8 men, mean aged 54.3 yr and women, mean aged 49.3 yr) participated in a classical controlled inhospital 8-week endurance training program. Progressive incremental exercise tests with gas exchange analysis and isokinetic strength measurements of knee flexors and extensors were conducted in all subjects before and after training at different angular velocities (60, 180, 240◦ /s ). Results: After training, peak V˙ O2 improved significantly (from 16.3 ± 3.3 to 20.7 ± 4.0 ml/kg/min; p < 0.002) as did New York Heart Association (NYHA) functional class (2.2 ± 0.4 to 1.5 ± 0.5; p < 0.001). Conversely, isokinetic strength at all angular velocities studied was unchanged after the training program. Conclusion: Isokinetic muscle strength was not improved in CHF patients participating in a endurance training program. A combined endurance and resistance protocol might be helpful for these patients whose frequently altered muscle strength undoubtedly contributes to their poor quality of life for everyday activities. Keywords: Chronic heart failure, cardiac rehabilitation, isokinetic muscle strength
1. Introduction Congestive heart failure (CHF) patients suffer from fatigue, dyspnea with exercise intolerance and a poor quality of life [1]. Skeletal muscles studies demon∗ Address for correspondence:
Francis Degache, MSc, CHU Nord, Niveau 6, EFCR, F – 42055 Saint-Etienne Cedex 2, France. Tel.: +33 4 77 82 83 00; Fax: +33 4 77 82 84 47; E-mail: francisdegache@ hotmail.com.
strated changes in structure and metabolic activity, loss of mass and reduction of peripheral blood flow due to reduced cardiac output and impairment of flowdependent ability of arteries to dilate, which thus reduces exercise capacity [1]. Traditionally, CHF patients have been instructed to avoid exercise in order to limit O2 demand. However, inactivity and deconditioning may be one of the main factors aggravating the dyspnea and limb skeletal muscle abnormalities. Furthermore, training programs have been shown to improve exercise performance and more specifically to improve peak
ISSN 0959-3020/05/$17.00 © 2005 – IOS Press and the authors. All rights reserved
112
F. Degache et al. / Isokinetic muscle strength in CHF
oxygen consumption which is one of the more accurate prognosis indicators, and to reduce symptoms [2]. The goals of such exercise training programs in patients with chronic heart failure are to improve the ability to cope with daily living [3]. Meta-analysis of randomised trials to date gives no evidence that properly supervised medical training programmes for patients with heart failure might be dangerous, and indeed there is clear evidence of an overall reduction in mortality [4]. The demands of everyday physical activities (climbing stairs, hurrying short distances for the bus, walking up and down hill. . .) are intermittent and require both endurance capacity and muscle strength. Aerobic exercise training, such as treadmill or cycling ergometry, designed to improve peak oxygen consumption ( V˙ O2peak ), has long been a feature of cardiac rehabilitation programs. More recently, recommendations for inclusion of muscle strength (resistance) training have been proposed for patients with coronary artery disease for a number of reasons, including the need to train the upper body, increase muscle strength and lean body mass, and improve self-efficacy and independence. Until very recently, resistance exercise was not recommended in patients with chronic heart failure because of concerns about safety, but these have now been largely allayed in relation to acute and chronic effects of this mode of exercise. There is no scientific evidence of muscle strength modifications after classical aerobic exercise training in CHF populations [1]. The aim of the present study was thus to evaluate the effects of an endurance training program on isokinetic leg muscle strength parameters and on aerobic capacity in a group of patients with stable chronic heart failure.
2. Methods 2.1. Subjects Eleven patients (8 men, mean age 56.5 ± 10.6 and 3 women, mean age 49.3 ± 9.3) with chronic congestive heart failure (NYHA class II: n = 9, class III: n = 2) were included in this study during 6 months. Patients were on standard medical treatment consisting of angiotensin-converting enzyme inhibitor (n = 11), diuretic (n = 11) digoxin (n = 2) and beta adrenergic blockers (n = 10). Symptoms and medical therapy had been stable in all patients for at least 3 months. Inclusion criteria for these patients were symptoms of congestive heart failure (NYHA functional class II and III) for more than 6 months and left ventricular ejection
fraction (echographic or angiographic determination) below than 40%. Exclusion criteria were systemic hypertension, ventricular arrhythmia, pulmonary hypertension. 2.2. Fat free mass analysis Fat mass (FM) and fat free mass (FFM) were evaluated by Bioelectrical Impedance Analysis (BIA) in all patients. Resistance and reactance were measured with the BIA generator and used to mathematically derive FFM and FM, according to the formula V = ρ * ht 2 /R, (where the conductive volume (V) is assumed to represent FFM, ρ is the specific resistivity of the conductor, height (ht) is the length of the conductor, and where the body resistance (R) is measured with four surface electrodes placed on the right wrist and ankle). Briefly, an electrical current of 50 kHz and 0.8 mA was produced by a generator (Bio-Z 2 , Spengler, Paris, France) and applied to the skin with adhesive electrodes (3 M Red Dot, 3 M Health Care, Borken, Germany) with the subject lying in the supine position. The skin was cleaned with 70 ◦ alcohol. Technical characteristics of the Bio-Z2 generator were: impedance, 100 to 900 Ω; angle phase, 1 to 18 ◦ ; accuracy ± 3 Ω and ± 0.2 ◦ , respectively [5]. FFM and FM were expressed in Kg. 2.3. Body Mass Index (BMI) The BMI was calculated with the classic formula: weight/height2 for all the population (Table 2). 2.4. Exercise test with gas exchange analysis Patients sat on an electronically calibrated cycle ergometer and pedaled at an imposed rate of 60 rpm. Starting with a workload of 10 W, resistance power was progressively increased every 1-minute by 10-W. Standard 12-lead electrocardiograms were obtained at rest, each minute during exercise and in the recovery phase. Blood pressure was monitored using a standard sphygmomanometer, at rest and each 2 minutes during exercise and recovery. Levels of mixed expired oxygen (O2 ), mixed expired carbon dioxide (CO 2 ), and expired volume were analyzed at rest and every 15 seconds during the protocol using the Medical Graphic Corporation Metabolic cart gas analyzer (Saint Paul, MN, USA). All measurement instruments were calibrated before each test. Peak V˙ O2 was defined as the average V˙ O2 obtained during the last 30 seconds of maximal exercise, and the anaerobic threshold was defined according to
F. Degache et al. / Isokinetic muscle strength in CHF
the Beaver protocol [6]. Maximal lactate concentration was evaluated 3 min after the end of exercise test using capillary finger blood sample [7]. A minimum of 3 min was allowed before starting each test to ensure that stable resting measurements were recorded. Each subject was encouraged to exercise to exhaustion and none of them stopped exercise due to angina or claudication. Maximal effort achievement confirmation criteria were physical exhaustion and/or dyspnea. 2.5. Isokinetic strength analysis Measurement of isokinetic strength of knee flexors and extensors were made on an isokinetic dynamometer Cybex 6000 within the following week. The test was performed on the dominant leg. Torque, was determined with Cybex 6000 by taking the cross-product of the length of the lever arm, measured from the axis of rotation to the point of application of the force, and the force component perpendicular to the lever arm [8]. The isokinetic tests were performed at different angular velocities (60, 180 and 240 ◦/s). The subjects sat on the dynamometer bench with the back fully supported at 15 ◦ inclination and the hip at 75–80 ◦ flexion. The thigh was stabilized with a strap belt. The subject’s knee and the dynamometer input shaft were concentrically aligned. The tibial pad was placed on the distal third of the tibia and held firmly in place with a strap. Patients were secured with belts at the trunk level. Torque was measured in newton-meter (Nm). Heart rate was continuously monitored during the test. Patients were asked to repeat 3 successive flexionextension movements and were verbally encouraged all along the exercise. Each angular velocity session was followed by a rest period of at least 1 min in order to obtain the baseline pre-exercise heart rate.
113
Table 1 Baseline characteristics of the population (n = 11) Sex ratio (M:W) Age (yrs) Weight (kg) Height (cm) LVEF (%) Etiology of heart failure Dilated cardiomyopathy Ischemic cardiomyopathy Medications ACE – inhibitor Diuretics Digoxin Beta adrenergic blockers Amiodarone Associated troubles Diabetics PVD Hypertension Valvular abnormalities Biventricular pacing
Training group 8:3 54.5 ± 10.4 74.0 ± 16.5 168.2 ± 8.4 33.1 ± 5.2 6 5 11 11 2 10 1 1 2 5 2 0
M – men, W – women, ACE – angiotensin converting enzyme, LVEF – Left Ventricular Ejection Function, PVD – Peripheral Vascular Disease.
2.7. Statistical analysis Data are given as mean ± standard error of the mean. Findings relating to both sexes were pooled. To evaluate the training effects, we used the paired t test for repeated measurements. Linear correlation was tested to evaluate correlation between isokinetic muscle strength, V˙ O2 peak and anthropometric data. A p value of < 0.05 was considered significant.
3. Results 3.1. Anthropometric and clinical characteristics
2.6. Training protocol Patients exercised three times a week, for a total duration of 3 h. The training session was commenced and concluded with 5 min warming-up or cooling-down. Training involved 35 min of cycling and/or jogging and 15 min of arm ergocycling. Endurance training intensity was aimed at a target heart rate, defined by the initial cardiopulmonary exercise test, as the heart rate reached at 65% maximal aerobic workload. Heart rate was continuously monitored throughout the duration of the training sessions (n = 24).
All subjects completed the inhospital rehabilitation program under medically-supervised conditions. None required hospitalization or therapy adjustment during the training period. None of the patients experienced medical complications during the clinical tests. Baseline anthropometric data for the study population are listed in Table 1. Body composition and body weight was unaltered by training program. Specifically, there was no significant modification in dry fat free mass, in fat free mass and in fat mass.
114
F. Degache et al. / Isokinetic muscle strength in CHF Table 2 Maximal exercise tests. Results before and after 8 weeks of exercise training (n = 11) Peak V˙ O2 (ml.kg−1 .min−1 ) (min/max) V˙ O2 at VT (ml.kg−1 .min−1 ) (min/max) VE/VCO2max (min/max) VE/VO2max (min/max) Peak lactate (mMol.l−1 ) (min/max) P max (watt) (min/max) HR max (bpm) (min/max) HR at VT (bpm) (min/max) % Theoretical HR max (min/max) NYHA functional class (min/max) Free fat mass (kg) (min/max) Fat Mass (kg) (min/max) BMI (kg.m−2 ) (min/max)
Pre-training
Post-training
p-value
16.3 ± 3.3 (11.6/23.6) 9.9 ± 2.1 (7.6/14.9) 36.0 ± 7.8 (25.0/54.0) 42.5 ± 9.0 (31.0/61.0) 5.6 ± 3.1 (2.0/12.5) 102.9 ± 28.0 (70.0/150.0) 128.4 ± 21.6 (95.0/158.0) 98.2 ± 14.7 (77.0/119.0) 75.1 ± 12.7 (51.0/90.5) 2.2 ± 0.4 (2.0/3.0) 15.2 ± 3.9 (10.2/20.9) 56.0 ± 11.2 (39.4/69.0) 26.1 ± 4.3 (19.0/33.6)
20.7 ± 4.0 (15.2/27.7) 12.8 ± 2.9 (8.2/17.6) 34.5 ± 7.1 (21.0/49.0) 39.0 ± 7.0 (29.0/51.0) 6.5 ± 2.1 (3.5/10.2) 117.5 ± 26.7 (80.0/160.0) 128.4 ± 14.7 (100.0/146.0) 100.0 ± 13.0 (79.0/121.0) 74.4 ± 10.4 (54.0/85.0) 1.5 ± 0.5 (1.0/2.0) 15.4 ± 5.5 (7.5/22.3) 55.1 ± 13.8 (39.0/74.2) 26.1 ± 4.3 (19.0/33.6)
0.0017 0.0050 0.039 0.014 NS 0.0036 NS NS NS 0.0004 NS NS NS
VT – Ventilatory Threshold, HR – Heart Rate, NYHA – New York Heart Association, BMI – Body mass index.
creased after training. There was no significant change in maximal heart rate (128.36 ± 21.61 vs 128.45 ± 14.68 bpm; p = NS). Peak plasmatic lactate level was non-significantly modified after training (from 5.56 ± 3.10 to 6.49 ± 2.11 mMol.L −1; p = NS). Maximal workload was significantly enhanced (from 102.91 ± 27.99 to 117.50 ± 26.67 Watts; p < 0.005). There was a significant improvement in NYHA functional class after the endurance program (Table 2). 3.3. Isokinetic strength test Fig. 1. Changes in individual peak V˙ O2 before and after endurance training (∗ p < 0.05).
3.2. Cardiopulmonary exercise test After the 8-week training period, the patients showed significant improvement in maximal aerobic capacity (Table 2). Peak V˙ O2 improved approximately 20% (Fig. 1). Mean peak V˙ O2 increased from 16.30 ± 3.33 to 20.73 ± 4.04 ml.kg −1.min−1 (p < 0.01). Adaptation of ventilation at the end of exercise test was ameliorated: V˙ E/V˙ CO2 and V˙ E/V˙ O2 significantly de-
There was no significant change in isokinetic muscle strength at all angular velocities tested as well for knee flexor than extensor muscle (Table 3, Fig. 2). No significant correlation was found between the degree of improvement of the aerobic capacity and the baseline isokinetic muscle strength or change in isokinetic muscle strength at the end of the endurance program. 4. Discussion While the present findings confirmed that a 8-week medically-supervised endurance training program has
F. Degache et al. / Isokinetic muscle strength in CHF
115
Table 3 Isokinetic muscle strength characteristics at baseline and after endurance training (n = 11) PT at 60◦ /s (extensor) (min/max) PT at 180◦ /s (extensor) (min/max) PT at 240◦ /s (extensor) (min/max) PT at 60◦ /s (flexor) (min/max) PT at 180◦ /s (flexor) (min/max) PT at 240◦ /s (flexor) (min/max)
Pre-training 125.2 ± 43.8 (75.0/213.0) 80.0 ± 28.7 (41.0/125.0) 70.2 ± 25.2 (39.0/111.0) 75.9 ± 23.3 (52.0/118.0) 60.7 ± 19.9 (33.0/98.0) 55.1 ± 18.9 (33.0/81.0)
Post-training 120.7 ± 44.8 (69.0/201.0) 74.8 ± 33.8 (39.0/136.0) 66.5 ± 28.2 (38.0/121.0) 80.5 ± 26.2 (56.0/122.0) 60.0 ± 18.5 (35.0/88.0) 52.8 ± 19.8 (26.0/84.0)
p-value NS NS NS NS NS NS
PT – Peak Torque (Nm).
a favorable effect on maximal aerobic capacity in heart failure patients, the endurance training program used in this study did not induce any significant improvement in muscle strength evaluated with isokinetic tests of knee flexors and extensors. Neither age nor physiological parameters (peak V˙ O2 , maximal HR, left ventricular EF) allowed prediction of the increase in isokinetic muscle strength after exercise training. Spruit et al. [9] recently reported significant increases in knee flexion and extension strength following endurance training in chronic obstructive pulmonary disease patients. These authors concluded that resistance and endurance training have similar effects on peripheral muscle force. Their conclusion appears somewhat surprising since such an effect is not classically reported in healthy or aged populations after a pure endurance protocol, but the methodology used presented some limitations. It should be underlined that isometric or isokinetic dynamometry of knee extension and flexion muscle strength may exhibit a certain degree of discordance, particularly at higher speeds (>120 ◦/s). Delagardelle et al. [10] recently reported significant increases in left ventricular function, muscular strength and aerobic capacity after combined strength/endurance training in CHF patients. This study confirms our results in increasing NYHA class and working capacity after endurance training. However, this study reports an unchanged peak V˙ O2 following endurance training. This principal difference with our results could be explained by a difference in the endurance training program and the age of the population. While endurance training improves the oxygen transport system (number of capillaries per fiber, oxidation enzyme activity, rise in mitochondria volume density) [12,13], the previous study reported positive results regarding the effects of endurance training pro-
Fig. 2. Changes in individual isokinetic muscle strength after endurance training (angular velocity: 180◦ /s).
grams on the exercise tolerance, anaerobic threshold, peak leg blood flow, peak central arteriovenous oxygen difference and decreasing lactate accumulation [11]. Physical reconditioning has been introduced only recently as a valid treatment modality for patients with CHF. Endurance training programs improve exercise capacity, peripheral vascular reactivity and probably left ventricular systolic function parameters [6,14–17]. It has been suggested that both systemic and local inflammations played an important role in the pathogenesis and progression of the disease [18]. Moreover, circulating levels of cytokines and cytokine receptors have acquired prognostic significance [19,20]. Numerous studies recently reported on the anti-inflammatory effect of a 3-month home-based bicycle training program in patients with moderate to severe CHF [21]. In a similar approach, Larsen et al. [23] were able to demonstrate that aerobic exercise training reduced increased TNF-alpha levels in patients with symptomatic CHF.
116
F. Degache et al. / Isokinetic muscle strength in CHF
Resistance training exercise is strongly recommended for implementation in primary and secondary cardiovascular disease-prevention programs. Moreover, resistance training can be beneficial in the prevention and management of other chronic conditions, e.g., low back pain, osteoporosis, obesity and weight control, sarcopenia (i.e., a loss of skeletal muscle mass that may accompany aging), diabetes mellitus, susceptibility to falls, and impaired physical function in frail and elderly persons [3,24]. Cardiac patients also require a minimal amount of resistance exercise to be able to perform activities associated with daily living. It should be emphasized, however, that the resistance training prescription for patients with cardiovascular disease may differ slightly depending on the degree of left ventricular dysfunction, concomitant comorbid conditions (e.g., hypertension or diabetes), and associated neurological, vascular, or orthopedic limitations. As opposed to resistance training, which combines isometric and dynamic exercise, pure isometric exercise is not recommended for patients with cardiovascular disease [24]. Furthermore, recent studies have demonstrated that isometric or isokinetic strength training is safe and isokinetic tests reliable in CHF patients [25–28]. Adding resistance training to exercise rehabilitation of patients with CHF is indicated in order to: 1. increase skeletal muscle strength and endurance; 2. partly reverse skeletal muscle atrophy and metabolic deficits that are common in these patients; 3. provide interesting, alternative forms of exercise training to aerobic training; 4. enable activities of daily living to be performed at lower and therefore safer levels of intensity than prior to the exercise training [24]. Isokinetic training can also be planned as endurance training, using a circuit training protocol with isokinetic exercise of different muscle groups. Such programs can increase aerobic power (maximal oxygen uptake) as shown by Gettman et al. [29] after a 20-week program, with however, a lesser improvement than usually seen after running or cycling programs of similar duration [30]. Numerous investigations have reported the absence of cardiovascular events during rehabilitation in cardiac patients free of exercise-induced myocardial ischemia or complex ventricular arrhythmia [6,24,31]. In our experience, adding medically-supervised isokinetic strength evaluations does not lead to any increase in arrhythmic or hemodynamic risk.
In conclusion, while peak aerobic capacity ( V˙ O2peak ), the best predictor of survival in patients with CHF [32], is drastically improved after endurance training, knee flexor and extensor muscles strength appears to be unchanged by this training modality. Adding a resistance component to the protocol might help reverse the trend to altered isometric/isokinetic muscular strength frequently encountered as CHF advances.
References [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8] [9]
[10]
[11] [12]
[13]
[14]
A. Maiorana, G. O’Driscoll, C. Cheetham, J. Collis, C. Goodman, S. Rankin et al., Combined aerobic and resistance exercise training improves functional capacity and strength in CHF, J Appl Physiol 88 (2000), 1565–1570. A.I. Larsen, T. Aarsland, M. Kristiansen, A. Haugland and K. Dickstein, Assessing the effect of exercise training in men with heart failure, Eur Heart J 22 (2001), 684–692. K. Meyer, L. Samek, M. Schwaibold, S. Westbrook, R. Hajric, M. Lehmann et al., Physical responses to different modes of interval exercise in patients with chronic heart failure – application to exercise training, Eur Heart J 17 (1996), 1040– 1047. M.F. Piepoli, C. Davos, D.P. Francis and A.J. Coats, Exercise training meta-analysis of trials in patients with chronic heart failure (ExTraMATCH), BMJ 328 (2004), 189–196. C. Pichard, U.G. Kyle, D. Bracco, D.O. Slosman, A. Morabia and Y. Schutz, Reference values of Fat-Free and Fat Masses by bioelectrical impedance analysis in 3393 healthy subjects, Nutrition 16 (2000), 245–254. Working group report, Recommendations for exercise training in chronic heart failure patients, Eur Heart J 22 (2001), 125– 135. P. Foxdal, B. Sj¨odin, H. Rudstam, C. Ostman, B. Ostman, G.C. Hedenstierna et al., Lactate concentration differences in plasma, whole blood, capillary finger blood and erythrocytes during submaximal graded exercise in humans, Eur J Appl Physiol 61 (1990), 218–222. C.E. Laird and C.K. Rozier, Toward understanding the terminology of exercise mechanics, Phys Ther 59 (1979), 287–292. M.A. Spruit, R. Gosselink, T. Troosters, K. De Paepe and M. Decramer, Resistance versus endurance training in patients with COPD and peripheral muscle weakness, Eur Respir J 19 (2002), 1072–1078. C. Delagardelle, P. Feiereisen, P. Autier, R. Shita, R. Krecke and J. Beissel, Strength/endurance training versus endurance training in congestive heart failure, Med Sci Sports Exerc 34 (2002), 1868–1872. P. Rossi, Physical training in patients with congestive heart failure, Chest 5(101) (1992), 350S–353S. M. Riley, J. McParland, C.F. Stanford and D.P. Nicholls, Oxygen consumption during corridor walk testing in chronic cardiac failure, Eur Heart J 13 (1992), 789–793. R.T. Hepple, S.L.M. Mackinnon, J.M. Goodman, S.G. Thomas and M.J. Plyley, Resistance and aerobic training in older men: effects on VO2peak and the capillary supply to skeletal muscle, J Appl Physiol 82 (1997), 1305–1310. R.P. Wielenga, I.A. Huisveld, E. Bol, P.H. Dunselman, R.A. Erdman, M.R. Baselier et al., Safety and effects of physical training in chronic heart failure – Results of the Chronic Heart
F. Degache et al. / Isokinetic muscle strength in CHF
[15] [16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
Failure and Graded Exercise study (CHANGE), Eur Heart J 20 (1999), 872–879. A.J.S. Coats, Review: Exercise training in heart failure, Curr Control Trials Cardiovasc Med 1 (2000), 155–160. R. Hambrecht, J. Niebauer, E. Fiehn, B. Kalberer, B. Offner, K. Hauer et al., Physical training in patients with stable chronic heart failure: effects on cardiorespiratory fitness and ultrastructural abnormalities of leg muscles, J Am Coll Cardiol 25 (1995), 1239–1249. R. Hambrecht, S. Gielen, A. Linke, E. Fiehn, J. Yu, C. Walther et al., Effects of exercise training on left ventricular function and peripheral resistance in patients with chronic heart failure. A randomized trial, JAMA 283 (2000), 3095–3101. A.M. Feldman, A. Combes, D. Wagner, T. Kadakomi, T. Kubota, Y.Y. Li et al., The role of tumor necrosis factor in the pathophysiology of heart failure, J Am Coll Cardiol 35 (2000), 537–544. A. Deswal, N.J. Petersen, A.M. Feldman, J.B. Young, B.J. White and D.L. Mann, Cytokines and cytokine receptors in advanced heart failure, An analysis of the cytokine database from vesnarinone trial (VEST), Circulation 103 (2001), 2055– 2059. M. Rauchhaus, W. Doehner, D.P. Francis, C. Davos, M. Kemp, C. Liebenthal et al., Plasma cytokine parameters and mortality in patients with chronic heart failure, Circulation 102 (2000), 3060–3067. S. Adamopoulos, J. Parissis, C. Kroupis, M. Georgiadis, D. Karatzas, G. Karviolas et al., Physical training reduces peripheral markers on inflammation in patients with chronic heart failure, Eur Heart J 22 (2001), 791–797. V.M. Conraads, P. Beckers, J. Bosmans, L.S. De Clerk, W.J. Stevens, C.J. Vrints et al., Conmbined endurance/resistance training reduces plasma TNF- receptor levels in patients with chronic heart failure and coronary artery disease, Eur Heart J 23 (2002), 1854–1860. A.I. Larsen, P. Aukrust, T. Aarsland and K. Dickstein, Effect of aerobic exercise training on plasma levels of tumor necrosis
[24]
[25]
[26]
[27]
[28]
[29]
[30] [31]
[32]
117
factor alpha in patients with heart failure, Am J Cardiol 88 (2001), 805–808. M.L. Pollock, B.A. Franklin, G.J. Balady, B.L. Chaitman, J.L. Fleg, B. Fletcher et al., Resistance exercise in individuals with and without cardiovascular disease, Circulation 101 (2000), 828–833. F. Degache, F. Costes, P. Calmels, M. Garet, J.C. Barth´el´emy and F. Roche, Determination of isokinetic muscle strength in chronic heart failure patients and in patients with chronic obstructive pulmonary disease, Isokinetics Exercise Science 11 (2003), 31–35. M. Quittan, G.F. Wiesinger, R. Crevenna, M.J. Nuhr, A. Sochor and R. Pacher, Isokinetic strength testing in patients with Chronic Heart Failure – A reliability study, Int J Sport Med 22 (2001), 40–44. G. Magnusson, B. Isberg, K.E. Karlberg and C. Sylven, Skeletal muscle strength and endurance in chronic congestive heart failure secondary to idiopathic dilated cardiomyopathy, Am J Cardiol 73 (1994), 307–309. C. Delagardelle, P. Feiereisen, R. Krecke, B. Essamri and J. Beissel, Objective of 6 months’ endurance and strength training program in outpatients with congestive heart failure, Med Sci Sports Exerc 31 (1999), 1102–1107. L.R. Gettman, L.A. Culter and T.A. Strathman, Physiologic changes after 20 weeks of isotonic vs. isokinetic circuit training, J Sports Med 20 (1980), 265–274. G. Grimby, Isokinetic training, Int J Sports Med 3 (1982), 61–64. A.C. Fry, R.J. Schmidt, G.O. Johnson, G.D. Tharp and W.J. Kraemer, Recovery heart rate and blood pressure responses to a graded exercise test and heavy resistance exercise, Isokinetics Exercise Science 3 (1993), 74–84. D.M. Mancini, H. Eisen, W. Kussmaul, R. Mull, L.H. Edmunds and J.R. Wilson, Value of peak exercise oxygen consumption for optimal timing of cardiac transplantation in ambulatory patients with heart failure, Circulation 85 (1991), 1364–1373.