Chest Email Content Delivery
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (10)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mitchell, S. H.
Right arrow Articles by Levy, W. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mitchell, S. H.
Right arrow Articles by Levy, W. C.
(Chest. 2003;124:572-579.)
© 2003 American College of Chest Physicians

Oxygen Cost of Exercise Is Increased in Heart Failure After Accounting for Recovery Costs*

Steven H. Mitchell, MD; Natalie P. Steele, MD; Kenneth M. Leclerc, MD; Mark Sullivan, MD, PhD and Wayne C. Levy, MD

* From the Division of Cardiology (Drs. Mitchell, Steele, Sullivan, and Levy), Department of Medicine, University of Washington School of Medicine, Seattle; and Madigan Army Medical Center (Dr. Leclerc), Tacoma, WA.

Correspondence to: Wayne C. Levy, MD, Division of Cardiology, Box 356422, 1959 NE Pacific St, Seattle, WA 98195; e-mail: levywc{at}u.washington.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: The oxygen cost during exercise has been reported to be decreased in patients with congestive heart failure (CHF), implying an increased efficiency (lower oxygen uptake [O2] per Watt [O2/W]); however, these studies ignored the oxygen debt that is increased in heart failure.

Subjects: The primary aim of this research was to evaluate the total oxygen cost (work O2/W) during exercise and recovery in patients with heart failure as compared with healthy adults.

Design and patients: We performed a retrospective analysis comparing the exercise O2/W, the recovery O2/W, the work O2/W, and the O2/W relationship above and below the ventilatory threshold (VT) in 11 healthy control subjects and 45 patients with CHF.

Results: The exercise O2/W was decreased by 29% (p < 0.0001) in patients with CHF; however, the recovery O2/W was increased by 167% (p < 0.0001) and the work O2/W was increased by 14% in patients with CHF (p = 0.014). The O2/W slope increased above the VT (+ 27%, p = 0.0017) in both normal subjects and patients with CHF, suggesting a decrease in efficiency above the VT. There was an inverse correlation (r = 0.646, p < 0.0001) between exercise O2/W and recovery O2/W, implying that subjects with a low exercise O2/W were not efficient but rather accumulated a large oxygen debt that was repaid following completion of exercise.

Conclusions: Heart failure is associated with lower exercise O2/W; however, the patient with heart failure is not efficient, but rather accumulating a large oxygen debt (recovery O2/W) that is repaid following exercise. In addition, the work O2/W (including both exercise and recovery) is increased in patients with heart failure in comparison to control subjects, and correlates inversely with the percentage of predicted O2. The large recovery O2/W is likely due to impaired oxygen delivery to exercising muscle during exercise. The increase in the work O2/W is probably due to changes in skeletal muscle fiber type that occur in patients with heart failure (type I to type IIb).

Key Words: congestive heart failure • exercise • oxygen cost • oxygen uptake • recovery kinetics


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Congestive heart failure (CHF) is a syndrome characterized by abnormal gas exchange and ventilatory responses to exercise secondary to impaired cardiac performance. Patients with CHF have significant functional impairment and a poor prognosis. Recently, the kinetics of oxygen consumption during graded maximal exercise in patients with heart failure have been studied.1 Peak oxygen consumption is reduced, the ventilatory threshold (VT) appears earlier, and the slope of the increase in oxygen consumption vs time is reduced in parallel with the severity of circulatory failure.2 3 The oxygen uptake (O2) per Watt (O2/W) during exercise was found to be a powerful predictor of mortality.4 The oxygen cost during exercise has also been reported to be decreased with advancing CHF.3 5 6 This has been interpreted to mean that patients with CHF have an increased efficiency (lower O2/W); however, a significant oxygen debt (the O2 above resting O2 during the first 6 to 8 min of recovery) has been shown to develop in patients with CHF during exercise and must be repaid during the 5 to 10 min of recovery from exercise.1

The kinetics of O2 during recovery have been studied far less. Recovery O2 has been demonstrated to be prolonged in steady-state exercise for the same absolute and relative work rate in heart failure, and associated with fatigue and heart failure severity.7 8 A further increase in O2 in early recovery is associated with impaired exercise tolerance, lower peak O2, and a higher peak ventilatory efficiency (minute ventilation [E]/carbon dioxide output [CO2]).9 The slope of the decline of O2 is decreased and the half-time (T1/2) and time constant of recovery O2 prolonged with increasing heart failure severity.1 10 11

The purpose of this study was to evaluate the total oxygen cost in patients with CHF during graded maximal cycle ergometer exercise by examining the kinetics of the O2/W slope and the kinetics of the recovery O2. In addition, we sought to characterize the CO2 per Watt (CO2/W) slope and the kinetics of the recovery CO2. The hypothesis was that patients with heart failure would have a decrease in the O2/W during exercise, but an increase in O2/W during recovery and an overall increase in oxygen cost per Watt (decreased biomechanical efficiency) when the oxygen debt (recovery O2) is accounted for.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Healthy adult volunteers (n = 11) were recruited from the Seattle area. Normal subjects were not trained athletes and were not receiving any medicines. Patients with heart failure (n = 45) were referred for clinical exercise testing from the End Stage Heart Failure Clinic (Table 1 ). All subjects signed an informed consent form approved by the Human Subjects Committee at the University of Washington. Subjects were between the ages of 23 years and 65 years. Criteria for heart failure were referral to the End Stage Heart Failure Clinic, a previous ejection fraction <= 35%, and New York Heart Association functional class II-IV symptoms of heart failure. Exclusion criteria included recent (< 2 months) history of unstable angina, recent myocardial infarction or stroke, pregnancy, or any other medical or orthopedic condition that would limit exercise testing. Subjects were allowed to eat a light breakfast before testing.


View this table:
[in this window]
[in a new window]

  		Table 1.. Baseline Characteristics*

 
Exercise Testing
Subjects sat on the ergometer to obtain resting O2 for at least 2 min. Unloaded pedaling at 60 revolutions per minute for 2 min preceded the initiation of the ramp exercise. The ramp was a continuous 5 to 20 W/min (mean, 13.1 ± 3.6 W/min) in all patients with heart failure and 10 to 20 W/min (mean, 19.8 ± 3.1 W/min) in the control subjects. At the completion of exercise, subjects were allowed to pedal slowly (20 to 30 revolutions per minute) for the first 60 s of recovery but then sat quietly on the ergometer. O2 measurements continued for 2 to 6 min after peak exercise to allow for the determination of oxygen debt.

Gas Analysis
Data were obtained with a metabolic cart (Sensormatics 229C; Yorba Linda, CA; or Quinton QMC; Quinton Instrument; Seattle, WA) coupled to an electronically braked cycle ergometer. Gas and volume calibrations were performed prior to each test. Resting O2 was a 2-min average at rest. Unloaded O2 was the average during the last minute of unloaded pedaling. Peak O2 and peak workload (Watts) was defined as the highest 60-s average. Calculation of the oxygen debt used all O2 for 6 min following peak exercise until the O2 approached the baseline resting O2. As the tests were performed for clinical reasons, not all subjects had 6 min of recovery data. To evaluate the recovery respiratory kinetics for the first 6 min of recovery, the O2 and CO2 data were fitted to a monoexponential curve (O2 or CO2 = AeB(t - TD) + C, where t = time after peak exercise, TD = time delay before the O2 or CO2 decreases, A = amplitude, B = recovery time constant for O2 or CO2, and C = peak O2)11 using Microsoft Excel 5, Solver add-in (Microsoft Corporation; Redmond, WA). The T1/2 is the time from the end of exercise until the O2 is halfway from the peak to the resting O2. It was defined as T1/2 = time delay + 0.693 x B (recovery time constant). The oxygen debt is expressed as a percentage of the total oxygen cost of exercise (recovery O2/W)/(work O2/W) x 100. VT was estimated by the V-slope method. With the onset of exercise, there is a time delay before the O2 and CO2 begin to increase. The slope of the O2/W has traditionally been measured from this increase to approximately 75% of peak exercise due to a nonlinear fit at high workloads. We observed an inflection point occurring at the VT for both O2 and CO2 and elected to solve for the O2/W and CO2/W slope above and below VT. The O2 and CO2 kinetics during exercise were measured using the last minute of unloaded pedaling (to determine the time delay of the increase in O2 and CO2 with the start of exercise). The slopes of the O2/W and CO2/W relationships were calculated above and below the VT using linear regression. Three simultaneous equations were used to solve for the time delay after the onset of exercise, the slope below VT, and the slope above VT. The equations used the same time delay for both O2 and CO2 and were forced to meet at both inflection points for the time delay and the VT (Microsoft Excel 5, Solver add-in).12 For comparison with previous reports, the O2/W slope was also calculated using all exercise O2 data from 1 min after the start of exercise until peak exercise.

Measures of Oxygen Cost
The oxygen cost of exercise during exercise was defined as the exercise O2/W. It was calculated using the sum of O2 during exercise above the unloaded O2 divided by the sum of Watts during exercise. Recovery O2/W was calculated by using the sum of O2 during recovery above rest O2 divided by the sum of Watts during exercise. This data were obtained from the monoexponential fitted curve using the first 6 min of recovery. Work O2/W was the exercise O2/W plus recovery O2/W. Statistics are by unpaired t test and linear regression using Statview 5 (Abacus Concepts; Berkeley, CA). Significance was defined as p <= 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Table 1 outlines subject characteristics. The patients with heart failure were on average 13 years older than the healthy subjects, and most were male. The patients with heart failure were 9 kg heavier but similar in height. At peak exercise, the patients with heart failure had a 29% lower peak heart rate, a 60% lower peak oxygen consumption, a 60% lower peak workload, and a 34% lower oxygen pulse compared to control subjects (Table 2 ). Peak ventilatory efficiency (E/CO2) was 23% higher, but the peak respiratory exchange ratio was not significantly different. Moreover, there was no significant difference in resting or unloaded O2.


View this table:
[in this window]
[in a new window]

  		Table 2.. Ramp Protocol Data

 
Figure 1 depicts the O2/W slope for the heart failure and control groups. Both groups displayed significant changes in the O2/W slope at the VT. Both the control subjects and the patients with heart failure had an approximate 27% increase above the VT, indicating a decrease in skeletal muscle efficiency above the VT. Although the increase was similar, the absolute values were lower in the patients with heart failure. The patients with heart failure had a 17% lower slope below the VT and a 26% lower slope above the VT compared to the control subjects. If the inflection at the VT is ignored (similar to previous investigators), the patients with heart failure had an 18% lower slope of the O2/W relationship during exercise (Table 2) . Each group exhibited an increase of approximately 94% in the CO2/W slope at the VT. The slope of the CO2/W relationship was similar in the two groups (Table 2) .



View larger version (21K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Ramp exercise below VT (BVT) and above VT (AVT) from the onset of pedaling to peak exercise.

 
Recovery O2 kinetics were considerably delayed in the patients with heart failure (Fig 2 ). The O2 time delay, measured from the point of peak exercise until the O2 starts to fall, was significantly prolonged in patients with heart failure (20 s vs 4 s) and correlated directly with percentage of predicted O2 (r = 0.462, p = < 0.0001; Table 3 ). The recovery O2 time constant displayed a 56% increase in patients with heart failure (48 s vs 76 s; Table 2 ) consistent with the substantially greater oxygen debt in heart failure. The T1/2 was 95% greater (p < 0.0001; Table 2 ) and inversely correlated with percentage of predicted peak O2 (r = - 0.529, p < 0.0001; Table 3 ). The oxygen debt was 96% higher in the patients with heart failure and inversely correlated with percentage of predicted peak O2 (r = - 0.816, p < 0.0001; Table 3 ) despite the respiratory exchange ratio being essentially the same for both groups. The patients with heart failure showing a low O2/W relationship above the VT appeared to be more aerobically efficient, but this was because of greater reliance on anaerobic metabolism that was reflected by a greater oxygen debt. This reiterates the necessity of measuring both the O2 during exercise and recovery to determine the total oxygen cost of exercise.



View larger version (18K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2.. Time delay and recovery O2 following peak exercise.

 

View this table:
[in this window]
[in a new window]

  		Table 3.. Regression Data

 
Measures of oxygen cost revealed a 29% lower exercise O2/W in the patients with heart failure; however, the recovery O2/W was increased by 167% and the total oxygen cost of exercise (work O2/W) was increased by 14% (Table 2) . There was an inverse correlation (r = - 0.646, p < 0.0001; Fig 3 , Table 3 ) between exercise O2/W and the recovery O2/W, implying that subjects with a low exercise O2/W were not efficient but rather accumulated a large oxygen debt that was repaid after the completion of exercise. The percentage of predicted O2 correlated directly with exercise O2/W (r = + 0.696, p < 0.0001) and inversely with recovery O2/W (r = - 0.756, p < 0.0001) and work O2/W (r = - 0.303, p = 0.023) [Figs 4 , 5 ; Table 3 ].



View larger version (18K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 3.. Inverse correlation between exercise O2/W and recovery O2/W.

 


View larger version (19K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 4.. Correlation between percentage of predicted O2 and exercise O2/W. The patients with heart failure and greater impairment had lower exercise O2.

 


View larger version (20K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 5.. Inverse correlation between percentage of predicted O2 and recovery O2/W. Patients with heart failure and impaired exercise had lower exercise O2 but accumulated a large recovery O2/W.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Previous investigators have reported that patients with heart failure have a lower O2 at a given workload during maximal ramp exercise. They suggested that patients with heart failure were more efficient than normal subjects2 3 5 6 ; however, none to our knowledge have accounted for the increase in recovery O2 in the evaluation of efficiency. We found total oxygen cost is greater when oxygen consumption during recovery is included for New York Heart Association class II-IV patients with heart failure. Our study confirms the slope of the O2/Watt relationship is lower in patients with heart failure and decreases with percentage of predicted peak O2. When evaluating the O2/W slope without regarding the inflection at the VT, we observed an 18% decrease in patients with heart failure. Normal values for the O2/W slope have ranged between 10.0 ± 1.1 to 12.3 ± 1.6, consistent with that observed in our normal group.2 3 5 The O2/W slope has been reported to be lower in men with circulatory disorders (8.3) and with increasing heart failure severity (6.7 to 8.8).2 3 4 5 12 Both are slightly lower than our results (9.4). In addition, Koike et al4 found the O2/W slope to be an independent predictor of mortality in heart failure.

Whipp13 first described and Gaesser and Poole14 later established the presence of a slow component of O2 that increases the O2/W slope above VT. An increase in recruitment and blood flow to type II glycolytic (inefficient) muscle fibers at higher levels of exercise are believed to be a major contributor.15

To our knowledge, this article is the first to report on the changes in the O2/W and CO2/W slope at the VT during maximal ramp exercise in patients with heart failure. The ratio of O2 and CO2 above and below the VT was nearly identical in each group at 27% and 94%, respectively; however, we discovered significant differences when comparing the slopes between our populations. The patients with heart failure had a lower slope compared to control subjects at each section examined on the O2/W slope. The decreased slope was more significant above the O2 VT (- 26%) than below the O2 VT (- 17%). The inverse correlation (r = - 0.646) between exercise O2/W and recovery O2/W implies that subjects with a low exercise O2/W were not efficient but rather were accumulating a large oxygen debt due to reliance on anaerobic metabolism that was repaid after the completion of exercise (Fig 3) .

The CO2/W slope did not differ significantly between the groups. There was nearly a doubling of the CO2 after VT in both the control and heart failure groups. This would be expected with the increase in bicarbonate buffering of lactate that accompanies greater reliance on anaerobic metabolism following VT.1 Nevertheless, the similarity in the CO2/W slope following VT most likely does not correspond to the tissue carbon dioxide production expected with the significant oxygen debt demonstrated by the O2 data.

Recovery kinetics following graded maximal exercise tests in patients with heart failure have not been characterized extensively. Recovery O2 has been shown to be prolonged for the same absolute and relative work rate during constant work rate exercise.7 In maximal graded exercise, the T1/2 of O2 is delayed. The O2 time constant is prolonged and inversely correlated with peak O2, anaerobic threshold, and the increase in O2 per rate of work.1 8 10 11 16 Our data confirm a prolonged O2 recovery time constant (48 s vs 76 s) and a significant time delay between the cessation of exercise and the beginning of the decline of O2 (4 s vs 20 s).

Causes for the increase in oxygen cost and subsequently larger oxygen debt appear to be multifactorial. In patients with heart failure, there are known changes in skeletal muscle, which include a decrease in efficient type I fibers, a decrease in oxidative enzymes, a decrease in mitochondrial density, a decrease in pH, and an increase in inefficient type IIb fibers.17 18 19 Additionally, there are changes in recruitment, blood flow, and sensitivity of skeletal muscle fiber types to exercise and norepinephrine. These changes may significantly contribute to the decreased slope of the O2/W slope found following VT and the significant oxygen debt found in patients with heart failure. These changes would be expected to prolong peripheral muscle O2 during recovery and have been demonstrated with near-infrared spectroscopy.20 Other factors that may be implicated are a decreased blood velocity resulting in increased transit time between oxygen consumption at the peripheral muscle and the mouth.1 8 21

The T1/2 of recovery CO2 is prolonged compared to normal subjects and with increasing severity of heart failure.1 22 Our data affirmed the delay in CO2 kinetics with a marked increase in the CO2 time delay (4 s vs 21 s) and the recovery time constant (80 s vs 123 s). Several possible mechanisms include lactic acid retention in muscle, diminished blood flow that limits carbon dioxide return to the lungs, and the increased cost of breathing.1

Potential limitations to our study include the estimation of the oxygen consumption during recovery. However, it is likely that the true recovery O2/W is even greater then estimated as the recovery time, T1/2, and time constant is prolonged in heart failure.1 7 8 10 16

In conclusion, our findings suggest that the more limited the heart failure patient is, the lower the O2/W is during exercise. However, the patient with heart failure is not efficient, but rather is accumulating an extremely large oxygen debt that is repaid after the completion of exercise. In addition, the total oxygen cost of exercise (work O2/W, which includes exercise and recovery) is increased in patients with heart failure in comparison to control subjects and correlates inversely with the percentage of predicted O2. It is likely the large recovery O2/W is due to impaired oxygen delivery to exercising muscle and a greater reliance on anaerobic metabolism. The increase in total oxygen cost is probably due to changes in oxygen utilization at the skeletal muscle as demonstrated by the changes in fiber type that occur in heart failure (type I to type IIb).


   Footnotes
 
Abbreviations: CHF = congestive heart failure; T1/2 = half-time; CO2 = carbon dioxide output; CO2/W = carbon dioxide output per Watt; E = minute ventilation; O2 = oxygen uptake; O2/W = oxygen uptake per Watt; VT = ventilatory threshold

Dr. Mitchell and Dr. Steele are supported by a grant from the American Federation for Aging Research.

Dr. Levy is supported by National Institutes of Health grant K12 AG00503.

Supported in part by the Geneva Foundation.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (e-mail: permissions{at}chestnet.org).

Received for publication June 10, 2002. Accepted for publication December 13, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Cohen-Solal, A, Laperche, T, Morvan, D, et al (1995) Prolonged kinetics of recovery of oxygen consumption after maximal graded exercise in patients with chronic heart failure: analysis with gas exchange measurements and NMR spectroscopy. Circulation 91,2924-2932[Abstract/Free Full Text]
  2. Cohen-Solal, A, Chabernaud, JM, Gourgon, R Comparison of oxygen uptake during bicycle exercise in patients with chronic heart failure and in normal subjects. J Am Coll Cardiol 1990;16,80-85[Abstract]
  3. Itoh, H, Taniguchi, K, Koike, A, et al Evaluation of severity of heart failure using ventilatory gas analysis. Circulation 1990;81,I31-I37
  4. Koike, A, Itoh, H, Kato, M, et al Prognostic power of ventilatory responses during submaximal exercise in patients with chronic heart failure. Chest 2002;121,1581-1588[Abstract/Free Full Text]
  5. Itoh, H, Nakamura, M, Ikeda, C, et al Changes in oxygen uptake-work rate relationship as a compensatory mechanism in patients with heart failure. Jpn Circ J 1992;56,504-508[Medline]
  6. Solal, AC, Chabernaud, JM, Gourgon, R Comparison of oxygen uptake during bicycle exercise in patients with chronic heart failure and in normal subjects. J Am Coll Cardiol 1990;16,80-85[Abstract]
  7. Sietsema, KE, Ben-Dov, I, Zhang, YY, et al Dynamics of oxygen uptake for submaximal exercise and recovery in patients with chronic heart failure. Chest 1994;105,1693-1700[Abstract/Free Full Text]
  8. Cohen-Solal, A, Geneves, M, Laperche, T Kinetics of recovery of ventilation and oxygen uptake after maximal exercise test in heart failure: a new index of functional impairment? Circulation 1993;88(suppl),I-591
  9. Daida, H, Allison, TG, Johnson, BD, et al Further increase in oxygen uptake during early active recovery following maximal exercise in chronic heart failure. Chest 1996;109,47-51[Abstract/Free Full Text]
  10. Pavia, L, Myers, J, Cesare, R Recovery kinetics of oxygen uptake and heart rate in patients with coronary artery disease and heart failure. Chest 1999;116,808-813[Abstract/Free Full Text]
  11. Hayashida, W, Kumada, T, Kohno, F, et al Post-exercise oxygen kinetics in patients with left ventricular dysfunction. Int J Cardiol 1993;38,63-72[CrossRef][ISI][Medline]
  12. Hansen, JE, Sue, DY, Oren, A, et al Relation of oxygen uptake to work rate in normal men and men with circulatory disorders. Am J Cardiol 1987;59,669-674[CrossRef][ISI][Medline]
  13. Whipp, BJ The slow component of oxygen uptake kinetics during heavy exercise. Med Sci Sports Exerc 1994;26,1319-1326[ISI][Medline]
  14. Gaesser, GA, Poole, DC The slow component of oxygen uptake kinetics in humans. Exerc Sport Sci Rev 1996;24,35-71[Medline]
  15. Segal, SS, Kurjiaka, DT Coordination of blood flow control in the resistance vasculature of skeletal muscle. Med Sci Sports Exerc 1995;27,1158-1164[ISI][Medline]
  16. deGroote, P, Millaire, A, Decoulx, E, et al Kinetics of oxygen consumption during and after exercise in patients with dilated cardiomyopathy. J Am Coll Cardiol 1996;28,168-175[Abstract]
  17. Mancini, DM, Ferraro, N, Tuchler, M, et al Detection of abnormal calf muscle metabolism in patients with heart failure using phosphorous-31 nuclear magnetic resonance. Am J Cardiol 1988;62,1234-1240[CrossRef][ISI][Medline]
  18. Clark, AL, Poole-Wilson, PA, Coats, AJ Exercise limitation in chronic heart failure: central role of the periphery. J Am Coll Cardiol 1996;28,1092-1102[Abstract]
  19. Mancini, DM, Coyle, E, Coggan, A, et al Contribution of intrinsic skeletal muscle changes to 31P NMR skeletal muscle metabolic abnormalities in patients with chronic heart failure. Circulation 1989;80,1338-1346[Abstract/Free Full Text]
  20. Belardinelli, R Muscle oxygenation kinetics measured by near-infrared spectroscopy during recovery from exercise in chronic heart failure. G Ital Cardiol 1998;28,866-872[Medline]
  21. Mancini, DM, Henson, D, LaManca, J, et al Respiratory muscle function and dyspnea in patients with chronic congestive heart failure. Circulation 1992;86,909-918[Abstract/Free Full Text]
  22. Tanabe, Y, Takahashi, M, Suzuki, K, et al Prolonged recovery of cardiac output after maximal exercise in patients with chronic heart failure. J Am Coll Cardiol 2000;35,1228-1236[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 J Am Coll CardiolHome page
J. S. Woo, C. Derleth, J. R. Stratton, and W. C. Levy
The Influence of Age, Gender, and Training on Exercise Efficiency
J. Am. Coll. Cardiol., March 7, 2006; 47(5): 1049 - 1057.
[Abstract] [Full Text] [PDF]

Home page
 J Am Coll CardiolHome page
M. Guazzi, G. Tumminello, F. Di Marco, C. Fiorentini, and M. D. Guazzi
The effects of phosphodiesterase-5 inhibition with sildenafil on pulmonary hemodynamics and diffusion capacity, exercise ventilatory efficiency, and oxygen uptake kinetics in chronic heart failure
J. Am. Coll. Cardiol., December 21, 2004; 44(12): 2339 - 2348.
[Abstract] [Full Text] [PDF]

Home page
 Exp PhysiolHome page
P. McDonough, B. J. Behnke, T. I. Musch, and D. C. Poole
Effects of chronic heart failure in rats on the recovery of microvascular PO2 after contractions in muscles of opposing fibre type
Exp Physiol, July 1, 2004; 89(4): 473 - 485.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (10)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mitchell, S. H.
Right arrow Articles by Levy, W. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mitchell, S. H.
Right arrow Articles by Levy, W. C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS