CLINICAL RESEARCH
Inspiratory Muscle Training in Patients With Heart Failure and Inspiratory Muscle Weakness
A Randomized Trial
Pedro Dall'Ago, PT, ScD*, ,
Gaspar R.S. Chiappa, PT, MSc ,
Henrique Guths, PT, MSc,
Ricardo Stein, MD, ScD and
Jorge P. Ribeiro, MD, ScD, ,*
* Department of Physiological Sciences, Fundação Faculdade Federal de Ciências Médicas de Porto Alegre, Porto Alegre, Brazil
School of Physical Therapy, UNILASALLE, Canoas, Brazil
Cardiology Division, Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil
Department of Medicine, Faculty of Medicine, UFRGS, Porto Alegre, Brazil
Manuscript received May 24, 2005;
revised manuscript received August 21, 2005,
accepted September 26, 2005.
* Reprint requests and correspondence: Dr. Jorge P. Ribeiro, Cardiology Division, Hospital de Clínicas de Porto Alegre, Rua Ramiro Barcelos 2350, 90035-007, Porto Alegre, RS, Brazil
(Email: jpribeiro{at}cpovo.net).
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Abstract
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OBJECTIVES: This study sought to evaluate the effects of inspiratory muscle training in inspiratory muscle strength, as well as in functional capacity, ventilatory responses to exercise, recovery oxygen uptake kinetics, and quality of life in patients with chronic heart failure (CHF) and inspiratory muscle weakness.
BACKGROUND: Patients with CHF may have reduced strength and endurance in inspiratory muscles, which may contribute to exercise intolerance and is associated with a poor prognosis.
METHODS: Thirty-two patients with CHF and weakness of inspiratory muscles (maximal inspiratory pressure [PImax] <70% of predicted) were randomly assigned to a 12-week program of inspiratory muscle training (IMT, 16 patients) or to a placebo-inspiratory muscle training (P-IMT, 16 patients). The following measures were obtained before and after the program: PImax at rest and 10 min after maximal exercise; peak oxygen uptake, circulatory power, ventilatory oscillations, and oxygen kinetics during early recovery ( O2/t–slope); 6-min walk test; and quality of life scores.
RESULTS: The IMT resulted in a 115% increment PImax, 17% increase in peak oxygen uptake, and 19% increase in the 6-min walk distance. Likewise, circulatory power increased and ventilatory oscillations were reduced. The O2/t–slope was improved during the recovery period, and quality of life scores improved.
CONCLUSIONS: In patients with CHF and inspiratory muscle weakness, IMT results in marked improvement in inspiratory muscle strength, as well as improvement in functional capacity, ventilatory response to exercise, recovery oxygen uptake kinetics, and quality of life.
Most patients with chronic heart failure (CHF) are limited in their physical activity by fatigue and dyspnea, and it has been suggested that respiratory muscle weakness and deconditioning may be involved in the increased work of breathing during hyperpnea (1). Some of these patients show reduced maximal inspiratory pressure (PImax) and endurance of inspiratory muscles, which are currently recognized as additional factors implicated in the limited exercise response and quality of life, as well as in their poor prognosis (2). Abnormal ventilatory response to exercise (3), periodic breathing (4), and delayed oxygen uptake kinetics during recovery of maximal effort (5) have also been associated with severity of and poor prognosis in CHF. The precise cause of this respiratory muscle dysfunction remains speculative, but diaphragm biopsies have shown a variety of histological abnormalities in CHF, including fiber type I atrophy (6), which have been implicated in a generalized skeletal muscle disorder in CHF (7).
Few studies have evaluated the effects of inspiratory muscle training in patients with CHF, and their results are contradictory (8–11). Nonrandomized trials (8,11) have shown improvement in maximal functional capacity after inspiratory muscle training, but these beneficial effects have not been confirmed by randomized studies (9,10). Moreover, the effects of inspiratory muscle training on several markers of prognosis obtained from cardiopulmonary exercise testing (CPET) have not been previously reported. Therefore, we conducted this randomized trial to test the hypothesis that a 12-week program of inspiratory muscle training could be associated with improvement in functional capacity, circulatory power, oscillatory ventilation, kinetics of oxygen consumption in the recovery period, and quality of life in patients with CHF and inspiratory muscle weakness.
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Methods
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Patients and design.
A prospective, randomized, controlled trial was conducted in patients with the diagnosis of CHF attributable to left ventricular systolic dysfunction (left ventricular ejection fraction <45%) who were recruited from the Heart Failure Clinic at the Hospital de Clínicas de Porto Alegre. Entry criteria for the study were a previous history of symptomatic heart failure caused by left ventricular systolic dysfunction, inspiratory muscle weakness (PImax <70% of the predicted), and clinical stability, including no change in medications for the past three months. Exclusion criteria were unstable angina, myocardial infarction, or cardiac surgery within the previous three months; chronic metabolic, orthopedic, or infectious disease; treatment with steroids, hormones, or cancer chemotherapy. Patients with previous pulmonary disease (forced vital capacity <80% of predicted and/or forced expiratory volume in 1 s <70% of predicted) (12), history of exercise-induced asthma, and smokers were not recruited. The protocol was approved by the Committee for Ethics in Research of the Hospital de Clínicas de Porto Alegre, and all subjects signed an informed consent form.
Eligible patients were initially evaluated by medical history, physical examination, resting electrocardiogram, two-dimensional echocardiogram, pulmonary function, and inspiratory muscle function. Patients were randomly assigned to inspiratory muscle training (IMT) or to placebo-inspiratory muscle training (P-IMT) for 12 weeks. Before and after the intervention, pulmonary function tests, inspiratory muscle function tests, cardiopulmonary exercise testing (CPET), 6-min walk test, and quality of life assessment were obtained. After finishing the intervention, none of the patients continued with inspiratory muscle training or with any formal exercise program. One year after entering the study, 11 patients in each group were re-evaluated for inspiratory muscle strength and quality of life. All evaluations were performed by investigators who were unaware of the allocation of patients to different interventions.
Inspiratory muscle training.
Patients received either IMT or P-IMT for 30 min 7 times per week, for 12 weeks using the Threshold Inspiratory Muscle Training device (Threshold Inspiratory Muscle Trainer, Healthscan Products Inc., Cedar Grove, New Jersey). During training, patients were instructed to maintain diaphragmatic breathing, with a breathing rate at 15 to 20 breaths/min. For the IMT group, inspiratory load was set at 30% of maximal static inspiratory pressure, and weekly training loads were adjusted to maintain 30% of the PImax. The P-IMT followed the same schedule, but with no inspiratory load. Each week, six training sessions were performed at home and one training session was supervised at the hospital.
Pulmonary function.
Measurements of forced vital capacity and forced expiratory volume in 1 s were obtained with a computerized spirometer (Eric Jaeger, GmbH, Wüerzburg, Germany) as recommended by the American Thoracic Society (12), and results were expressed as percentage of predicted (13).
Inspiratory muscle function testing was performed using a pressure transducer (MVD-500 V.1.1 Microhard System, Globalmed, Porto Alegre, Brazil), connected to a system with two unidirectional valves (DHD Inspiratory Muscle Trainer, Chicago, Illinois). Maximal static inspiratory pressure was determined in deep inspiration from residual volume against an occluded airway with a minor air leak (2 mm). The highest pressure of six measurements was used for analysis. The PImax measurement was performed at rest, and on the 5th and 10th minute after CPET. Predicted values were corrected for age, gender, and weight (14). Additionally, for the determination of inspiratory muscle endurance, an incremental test was used in which patients breathed continuously through a mouthpiece connected to a Threshold Inspiratory Muscle Trainer with an initial load of 50% of PImax, and increments of 10% of PImax were added every 3 min until the patient was unable to continue breathing. The greatest inspiratory pressure that the subject was able to sustain for at least 1 min (Pthmax) was taken as the measure for inspiratory muscle endurance, and was expressed as a percentage of maximal inspiratory pressure (Pthmax/PImax). In the second part of the protocol, subjects breathed against a constant inspiratory submaximal load equivalent to 80% Pthmax, and the time elapsed to task failure was defined as the inspiratory endurance time.
6-min walk test.
The maximum distance covered during the walk test was used to assess submaximal functional capacity (15). Patients self-graded their degree of dyspnea during the test using the Borg scale (16).
Cardiopulmonary exercise testing.
Maximal functional capacity was evaluated with an incremental exercise test, with expired gas analysis, on a treadmill (INBRAMED 10200, Porto Alegre, Brazil), using a ramp protocol, starting at a speed of 2.4 km·h–1 and 2% slope, with 20-s increments of speed (0.1 to 0.2 km·h–1) and 60-s increments in slope (0.5% to 1.0%), to reach volitional fatigue at approximately 10 min. Twelve-lead electrocardiographic tracings were obtained every minute (Nihon Khoden Corp., Tokyo, Japan). Blood pressure was measured every 2 min with a standard cuff sphygmomanometer. Metabolic and ventilatory variables were measured during and after exercise by 20-s mean aliquots, by a computer-aided gas analyzer (Total Metabolic Analysis System, TEEM 100, Aero Sport, Ann Arbor, Michigan), previously validated (17). Peak oxygen uptake (O2peak) was considered the highest value of O2 calculated in a period of 20 s of exercise. Maximal circulatory power was calculated as the product of O2peak and peak systolic pressure (18).
Ventilatory efficiency was estimated using the relationship between minute ventilation (E) and carbon dioxide output (CO2), i.e., E/CO2–slope, by linear regression model using all data points obtained during CPET (3). The relative amplitudes of oscillations ( ) in E, O2, and CO2 were calculated for every 20-s period as the ratio between amplitude and its respective mean throughout the test. The ratio between metabolic (O2, CO2) and ventilatory oscillations (O2/E, CO2/E) were also calculated (19). The O2, CO2, and E kinetics during the first 3 min of the recovery period were calculated by a linear regression model adjusted to a simple exponential curve (O2/t, CO2/t, E/t – slope) (1). The time required for a 50% decrease from the O2peak (T1/2O2), CO2peak (T1/2CO2) and E peak (T1/2E) was calculated using the mathematical model of the minimum squares through the equation y = ae(–kt), where y corresponds to O2, CO2, or E in time, a corresponds to the slope, k is a constant, and t stands for the time.
Quality of life.
Quality of life was assessed with the Minnesota Living With Heart Failure Questionnaire (20). We analyzed overall scores as well as the separate effects of physical and psychological perceptions of quality of life.
Statistical analysis.
Data were analyzed on the Statistical Package for Social Sciences (version 10.0, SPSS, Chicago, Illinois). Based on the results of previous studies (8), we estimated that a sample size of 15 individuals in each group would have a power of 80% to detect a 10% difference in peak oxygen uptake, for an = 0.05. Descriptive data are presented as mean ± SD. Baseline data were compared by the Student t test for continuous variables or by the Fisher exact test for categorical variables. The Pearson correlation coefficient was used to evaluate associations. The effects of interventions on continuous variables were compared by two-way analysis of variance for repeated measures (ANOVA), and post-hoc analysis was conducted by the Tukey test. Categorical data were analyzed by the chi-square statistic.
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Results
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Patients.
Between August 2001 and November 2003, 144 patients with CHF were screened for the study. Ninety-six patients did not meet the inclusion or met the exclusion criteria, and therefore, 44 patients were randomized. For the 22 patients randomized to IMT, 1 had a myocardial infarction, 1 developed atrial fibrillation, and 4 were not able complete the training protocol. For the 22 patients allocated to P-IMT, 2 had to be excluded because of indication of coronary artery bypass graft surgery, 3 for the development of symptoms at rest, and 1 because of bleeding secondary to oral anticoagulation. Therefore, 16 patients completed the protocol in each group. Table 1 describes the clinical characteristics for both groups. Etiology of CHF was predominantly non-ischemic, and patients had mild to moderate left ventricular dysfunction as well as mild to moderate impairment in functional capacity. Patients received similar medications and maintained the same medical regimen throughout the study period. At one-year follow-up, three patients from the IMT group had died and five patients from the P-IMT group had died.
Pulmonary function and inspiratory muscle function tests.
After 12 weeks, spirometric evaluation did not show change in any of the groups (Table 2). The IMT induced marked improvement in PImax, which was apparent after the second week of training and reached an increment of 115% after 12 weeks (Fig. 1). Despite the fact that training was stopped after 12 weeks of intervention, patients in the IMT group maintained part of the effect one year after starting the program. Inspiratory muscle endurance, evaluated by the Pthmax, Pthmax/PImax, and time sustained in the inspiratory muscle function test, increased after IMT (Table 2). The IMT resulted in improvement in the recovery of PImax at 10 min after maximal exercise (Fig. 2).
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Table 2. Pulmonary Function and Inspiratory Muscle Function Tests Before and After Intervention for Patients Randomized to P-IMT or IMT
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Figure 1 Weekly values of maximal inspiratory pressure (PImax, mean ± SD) for the placebo-inspiratory muscle training group (P-IMT) and for the inspiratory muscle training group (IMT). After 12 weeks in the program, all training was stopped, and 11 patients from each group were re-evaluated at 48 weeks. *Two-way ANOVA for repeated measures: p < 0.01 for group, training, and interaction effects. Significantly (p < 0.05) different from baseline evaluation by the Tukey test.
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Six-minute walk test.
The IMT resulted in a longer distance covered during the 6-min walk test (IMT, 449 ± 17 m before and 550 ± 17 m after; P-IMT, 432 ± 41 m before and 411 ± 60 m after [ANOVA <0.002 for group, training, and interaction effects]). Perception of dyspnea rated by the Borg scale during the 6-min walk test also improved after IMT (IMT, 3.7 ± 2.0 before and 1.5 ± 1.4 after; P-IMT, 3.1 ± 1.3 before and 3.0 ± 1.4 after [ANOVA <0.002 for group, training, and interaction effects]).
Cardiopulmonary exercise testing.
Before intervention, O2peak did not correlate with PImax (r = 0.08; p = 0.32; n = 32). The IMT resulted in improvements in O2peak and E peak, whereas the peak respiratory exchange ratio (R) was not changed by intervention in either group (Table 3). The change in O2 peak after intervention correlated with the change in PImax (r = 0.62; p < 0.001; n = 32). Maximal circulatory power also increased only in the IMT group (Table 3).
Consistent with improvement in ventilatory efficiency, the E/CO2 slope was reduced after IMT. The relative size of the oscillations in E (E) was reduced after IMT. The relative size of the oscillations in O2 (O2) and CO2 (CO2) was not changed by either intervention. However, the ratio between the relative oscillations of E and CO2 increased after IMT.
Before the intervention, O2/t–slope at the first minute in the recovery did not correlate with PImax at 5 min after maximal exercise (r = 0.18; p = 0.15; n = 32). During recovery, T1/2 of O2, CO2, and E were faster after IMT (Table 3). Likewise, O2/t–slope in the first minute of recovery was higher after IMT (Table 3, Fig. 3). The change in O2/t–slope at the first minute in the recovery after intervention correlated with the change PImax at 5 min after maximal exercise (r = 0.70; p < 0.001; n = 32).
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Figure 3 Values of the oxygen uptake kinetics during the first 3 min of recovery (mean ± SD) after maximal cardiopulmonary exercise test before (A) and after (B) intervention for the placebo inspiratory muscle training group (P-IMT) and the inspiratory muscle training group (IMT). Overall two-way ANOVA for repeated measures: p < 0.001 for group, training, and interaction effects. *Significantly different between groups (p < 0.05) by the Tukey test.
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Quality of life.
The Minnesota Living With Heart Failure Questionnaire scores improved after IMT (IMT, 27 ± 4 before and 6 ± 2 after; P-IMT, 30 ± 13 before and 30 ± 13 after [ANOVA <0.001 for group, training, and interaction effects]). The global improvement was attributed to a change in physical dimension from 6 ± 3 to 3 ± 5 because no changes were observed in the psychological dimension of the score. Despite the fact that IMT was stopped after 12 weeks of intervention, patients who participated in the IMT program maintained part of the effect on quality of life scores one year after starting the program, from 27 ± 8 to 14 ± 3 (ANOVA <0.05 for group, training, and interaction effects).
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Discussion
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In this randomized trial, a home-based, three-month IMT program improved inspiratory muscle strength and endurance as well as quality of life and functional capacity in patients with CHF and weakness in inspiratory muscles. Moreover, IMT improved peak circulatory power, ventilatory efficiency, and oscillations during incremental exercise, as well as oxygen uptake kinetics during recovery, which are all markers of poor prognosis in CHF. The efficacy of IMT was tested against a similar program with no inspiratory load, which served as a placebo intervention, and outcomes were blindly evaluated. Interestingly, part of the effect on PImax and quality of life was sustained after one year, even though the patients did not continue training after four months. These data provide the first evidence showing that the effects of IMT are consistent and are partially maintained after one year of follow-up in patients with CHF and weakness of inspiratory muscles.
Inspiratory muscle strength and endurance.
In accordance with previous studies (8–11), IMT did not affect resting pulmonary function test results but had a major impact on all measures of inspiratory muscle strength and endurance. The magnitude of improvement in PImax (115%) in our patients is larger than described in previous studies (8–11), a finding that may be related to the fact that we used a linear pressure resistance device with weekly adjustments in load, resulting in possible training of other inspiratory muscles in addition to the diaphragm. Moreover, daily exercises and the presence of inspiratory muscle weakness in all patients may also have contributed to this increment. The improvement in PImax after maximal exercise is consistent with delayed development in diaphragmatic fatigue (1).
Functional capacity and quality of life.
Patients who participated in the IMT presented improvement in functional capacity as shown by a 19% increase in 6-min walk distance, which was also accompanied by a reduction in the perception of dyspnea. Likewise, there was a 17% increase in O2peak and a 24% increase in circulatory power, consistent with clinically significant improvement in cardiovascular and respiratory response to maximal exercise. The improvement in functional capacity and the reduction in perception of dyspnea were probably responsible for the changes in the physical dimension of quality of life scores, which was partially maintained at the 12-month evaluation, several months after IMT had been stopped.
The IMT can delay the development of diaphragmatic fatigue in patients with CHF, leading to a reduction in the recruitment of accessory respiratory muscles, increasing ventilatory efficiency, and/or reducing the blood flow required by the respiratory muscles during exercise (21). In CHF, there is enhanced ventilatory sensitivity to both central and peripheral chemoreceptor stimulation (22), which can reflexively induce sympathetic vasoconstriction and reduce blood flow to skeletal muscles during exercise. Therefore, diaphragm fatigue may elicit sympathetically mediated vasoconstriction in limb muscles, a reflex that can be attenuated by whole-body aerobic exercise training (23). By improving ventilatory muscle strength and endurance, IMT may also delay the development of fatigue of the diaphragm, consequently reducing sympathetic activation, improving the perfusion of the peripheral muscles, and increasing functional capacity.
Ventilatory response to exercise.
The present study confirms that three months of IMT causes substantial improvement in the ventilatory efficiency, as shown by a reduction in the E/CO2–slope. Patients with CHF present hyperventilation during exercise, with increased breathing rate and decreased tidal volume, resulting in larger pulmonary dead space (3). Recent studies have indicated a putative role of an exaggerated chemoreceptor reflex originating from the exercising muscle and explaining the hyperventilatory response in CHF (23). Indexes reflecting the chemoreceptor stimulation correlate with E/CO2–slope and ventilatory oscillations during exercise, variables with prognostic value in CHF patients (4,24). To our knowledge, this is the first study to show attenuation in ventilatory oscillation during exercise by IMT. Therefore, improvement in ventilatory muscle strength and endurance may also attenuate the exaggerated chemoreflex and improve ventilatory control during exercise.
Oxygen uptake kinetics during recovery.
The effects of an IMT program on oxygen kinetics during the recovery from CPET have not been previously studied. Results of the present study show a faster T1/2O2 and an increase in the O2/t–slope after IMT. Nanas et al. (1) have shown a relationship between inspiratory muscles weakness 10 min after maximal CPET and the reduced magnitude or prolonged O2 recovery time. Therefore, the delay in the recovery of blood flow to the fatigued diaphragm could contribute to prolonged kinetics of recovery of O2. In contrast to our findings, Myers et al. (25) showed that two months of high-intensity whole-body aerobic training improved O2peak but had no significant effect on O2 kinetics in the recovery period in patients with reduced ventricular function. Therefore, our findings underscore the role of strength and endurance of inspiratory muscles as determinants of oxygen uptake kinetics in the recovery period.
Study limitations.
In this small clinical trial, we showed that a 12-week program of IMT has a consistent effect on several prognostic markers in CHF. However, this study was designed only to evaluate the efficacy of IMT on functional variables and not on survival. Our findings are limited to patients with mild CHF caused by left ventricular systolic dysfunction and weakness in inspiratory muscle, but a recent trial of IMT, including patients with more advanced CHF and with a higher baseline PImax, found similar results (11). The training period was maintained for only 12 weeks, which does not allow us to conclude that the effect on functional capacity and quality of life is long-term. However, one-year follow-up showed that the effects on quality of life are partially maintained. We have suggested that part of the beneficial effects of IMT could be mediated by a reduction in sympathetic vasoconstrictor activity to peripheral muscle, but no assessment of sympathetic nerve activity was made, and mechanistic studies should be conducted to test this hypothesis.
Because whole-body aerobic exercise training is currently indicated for patients with CHF for improvement in functional capacity and possibly for reduction in mortality (26), it is not known whether the beneficial effects of IMT would further improve the functional capacity of patients with CHF who perform aerobic exercise regularly. However, Vibarel et al. (27) showed that aerobic exercise training has no significant effect on the strength of inspiratory muscles, suggesting that the two programs may result in complementary effects, a hypothesis that should be addressed by a controlled trial isolating the effects of both interventions.
Clinical implications.
Our findings indicate that a simple and inexpensive home-based IMT program results in clinically relevant increments of improvement in submaximal and maximal functional capacity, with reduction of perception of dyspnea and improvement in quality of life. Although the sample size is not appropriate to assess survival, these results, together with the observations of other small trials (8–11), suggest that IMT is a safe intervention that can be considered for the management of patients with CHF, particularly those with weakness in inspiratory muscles. Our results also raise the question of whether routine screening for weakness of inspiratory muscle should be performed in patients with CHF.
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Conclusions
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This randomized, placebo-controlled trial shows that a short-term, home-based program of IMT results in marked improvement in inspiratory muscle strength and endurance, which results in clinically relevant increments of improvement in submaximal and maximal functional capacity, as well as in quality of life in CHF patients with inspiratory muscle weakness. Moreover, IMT also improves ventilatory efficiency and oscillations during exercise, peak circulatory power, and oxygen uptake kinetics during recovery in this patient population.
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Acknowledgments
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We are thankful to Nadine Clausell, MD, PhD, Luis E. Rohde, MD, ScD, and Eneida Rabello, RN, ScD, from the Heart Failure Clinic of Hospital de Clínicas de Porto Alegre, for their support during the development of this study.
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Footnotes
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Supported by grants from: CAPES and CNPq, Brasília, Brazil, and FIPE-HCPA, Porto Alegre, Brazil.
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References
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1. Nanas S, Nanas J, Cassiotis C, et al. Respiratory muscle performance is related to oxygen kinetics during maximal exercise and early recovery in patients with congestive heart failure Circulation 1999;100:503-508.[Abstract/Free Full Text]2. Meyer FJ, Mathias M, Zugck C, et al. Respiratory muscle dysfunction in congestive heart failure: clinical correlation and prognostic significance Circulation 2001;103:2153-2158.[Abstract/Free Full Text] 3. Clark AL, Poole-Wilson PA, Coats AJ. Relation between ventilation and carbon dioxide production in patients with chronic heart failure J Am Coll Cardiol 1992;20:1326-1332.[Abstract] 4. Corra U, Giordano A, Bosimini E, et al. Oscillatory ventilation during exercise in patients with chronic heart failure: clinical correlates and prognostic implications Chest 2002;121:1572-1580.[Abstract/Free Full Text] 5. Scrutinio D, Passantino A, Lagioia R, et al. Percentage achieved peak exercise oxygen uptake and kinetics of recovery of oxygen uptake after exercise for risk stratification in chronic heart failure Int J Cardiol 1998;64:117-124.[CrossRef][Web of Science][Medline] 6. Lindsay DC, Lovegrove CA, Dunn MJ, et al. Histological abnormalities of muscle limb, thorax and diaphragm in chronic heart failure Eur Heart J 1996;17:1239-1250.[Abstract/Free Full Text] 7. Coats AJS. The "muscle hypothesis" of chronic heart failure J Mol Cell Cardiol 1996;28:2255-2262.[CrossRef][Web of Science][Medline] 8. Mancini DM, Henson D, La Manca J, et al. Benefit of selective respiratory muscle training on exercise capacity in patients with chronic congestive heart failure Circulation 1995;91:320-329.[Abstract/Free Full Text] 9. Johnson PH, Cowley AJ, Kinnear WJM. A randomized controlled trial of inspiratory muscle training in stable chronic heart failure Eur Heart J 1998;19:1249-1253.[Abstract/Free Full Text] 10. Weiner P, Waizman J, Magadle R, et al. The effect of specific inspiratory muscle training on the sensation of dyspnea and exercise tolerance in patients with congestive heart failure Clin Cardiol 1999;22:727-732.[Web of Science][Medline] 11. Laoutaris I, Dritsas A, Brown MD, et al. Inspiratory muscle training using an incremental endurance test alleviates dyspnea and improves functional status in patients with chronic heart failure Eur J Cardiovasc Prev Rehabil 2004;11:489-496.[CrossRef][Web of Science][Medline] 12. American Thoracic Society Standardization of spirometry, 1994 update Am J Respir Crit Care Med 1995;152:1107-1136.[Web of Science][Medline] 13. Knudson RJ, Slatin RC, Lebowitz MD, et al. The maximal expiratory flow-volume curveNormal standards, variability, and effects of age. Am Rev Respir Dis 1976;113:587-600.[Web of Science][Medline] 14. Neder JA, Andreoni S, Lerario MC, Nery LE. Reference values for lung function testsII. Maximal respiratory pressures and voluntary ventilation. Braz J Med Biol Res 1999;32:719-727.[Web of Science][Medline] 15. Guyatt GH, Sullivan MJ, Thompson PJ, et al. The six-minute walk: a new measure of exercise capacity in patients with chronic heart failure Can Med Assoc J 1985;132:919-923.[Abstract] 16. Wilson RC, Jones PW. A comparison of the visual analogue scale and modified Borg scale for the measurement of dyspnea during exercise Clin Sci 1989;76:277-282.[Medline] 17. Novitsky S, Segal KR, Chatr-Aryamontri B, et al. Validity of a new portable indirect calorimeter: the AeroSport TEEM 100 Eur J Appl Physiol Occup Physiol 1995;70:462-467.[CrossRef][Web of Science][Medline] 18. Cohen-Solal A, Tabet JY, Logeart D, et al. A non-invasively determined surrogate of cardiac power ("circulatory power") at peak exercise is a powerful prognostic factor in chronic heart failure Eur Heart J 2002;23:806-814.[Abstract/Free Full Text] 19. Francis DP, Davies C, Piepoli, et al. Origin of oscillatory kinetics of respiratory gas exchange in chronic heart failure. Circulation 1999;100:1065–70.. 20. Rector TS, Cohn JN. Assessment of patient outcome with the Minnesota Living With Heart Failure Questionnaire: reliability validity during a randomized, double-blind, placebo-controlled trial of pimobendanPimobendan Multicenter Research Group. Am Heart J 1992;124:1017-1025.[CrossRef][Web of Science][Medline] 21. Harms CA, Babcock MA, McClaran SR, et al. Respiratory muscle work compromises leg blood flow during maximal exercise J Appl Physiol 1997;82:1573-1583.[Abstract/Free Full Text] 22. Chua TP, Ponikowski P, Webb-Peploe K, et al. Clinical characteristics of chronic heart failure patients with augmented peripheral chemoreflex Eur Heart J 1997;18:480-486.[Abstract/Free Full Text] 23. Piepoli M, Volterrani M, Clark AL, et al. Contribution of muscle afferent to the hemodynamic, autonomic, and ventilatory responses to exercise in patients with chronic heart failure: effects of physical training Circulation 1996;93:940-952.[Abstract/Free Full Text] 24. Gitt AK, Wasserman K, Kilkowski C, et al. Exercise anaerobic threshold and ventilatory efficiency identify heart failure patients for high risk of early death Circulation 2002;106:3079-3084.[Abstract/Free Full Text] 25. Myers J, Gianrossi R, Schwitter J, et al. Effect of exercise training on postexercise oxygen uptake kinetics in patients with reduced left ventricular function Chest 2001;120:1206-1211.[Abstract/Free Full Text] 26. ExTraMATCH Collaborative Exercise training meta-analysis of trials in patients with chronic heart failure BMJ 2004;328:189-192.[Abstract/Free Full Text] 27. Vibarel N, Hayot M, Ledermann B, et al. Effect of aerobic exercise training on inspiratory muscle performance and dyspnoea in patients with chronic heart failure Eur J Heart Fail 2004;4:745-751.
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Abstract
Methods