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(Chest. 2001;120:816-824.)
© 2001 American College of Chest Physicians

Cardiopulmonary Exercise Testing in Children With Heart Failure Secondary to Idiopathic Dilated Cardiomyopathy*

Guilherme Veiga Guimarães, PhEd; Giovanni Bellotti, MD; Amilcar Oshiro Mocelin, MD; Paulo Roberto Camargo, MD and Edimar Alcides Bocchi, MD

* From the Heart Institute, University of São Paulo, Medical School, São Paulo, Brazil.

Correspondence to: Guilherme Veiga Guimarães, PhEd, Instituto do Coração, Rua Dr. Baeta Neves, 98–05444-050, São Paulo, SP, Brazil; e-mail: gvguima{at}usp.br


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Study objective: To determine and compare the cardiopulmonary responses of healthy children and children with heart failure due to idiopathic dilated cardiomyopathy (IC) to progressive treadmill exercise testing.

Setting: University teaching hospital specializing in cardiology.

Patients or participants: Twenty-six children with stable, chronic heart failure (left ventricular ejection fraction < 45%) caused by IC (IC group) and 12 healthy children (control group).

Interventions: After 12-lead resting ECG, all children underwent progressive treadmill exercise testing using a modified Naughton protocol. Tests were performed in a controlled-temperature exercise facility, at least 2 h after a light meal.

Measurements and results: Cardiopulmonary parameters were assessed at rest, at anaerobic threshold (AT), and at peak exercise. At rest, the tidal volume (VT) and O2 consumption (O2) for heart rate (O2 pulse) were lower, while the heart rate, respiratory rate, and ventilatory equivalent for O2 (minute ventilation [E]/O2) were higher in the IC group compared with the control group. At AT, the systolic BP, O2 pulse, VT, exercise duration, O2, CO2 production (CO2), and E were lower, while the E/O2 and ventilatory equivalent for CO2 (E/CO2) were higher in the IC group (p < 0.05). At peak exercise, the IC group had a significantly lower systolic BP, O2 pulse, E, VT, exercise duration, O2, and CO2, but higher E/O2 and E/CO2 than the control group (p < 0.05). The E/CO2 slope was significantly higher for the IC group. No correlation existed between variables evaluated at rest vs during exercise.

Conclusions: Gas exchange analysis performed during exercise successfully differentiated children with heart failure from healthy children.

Key Words: children • exercise • heart failure • oxygen consumption


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusions
 References
 
Most methods used to evaluate left ventricular function in patients with heart failure, such as symptom grading, physical signs, radiologic evaluation, echocardiography, and radionuclide methods, are usually performed with the patient at rest. As symptoms are frequently related to physical exercise, they often poorly correlate with indexes of left ventricular function obtained at rest. These factors reinforce the need to also evaluate heart function during physical exercise.

The intolerance to exercise observed in patients with heart failure is correlated with the prognosis.1 2 Adult patients with heart failure have greater metabolic and respiratory responses than normal individuals for the same degree of effort.3 Cardiopulmonary exercise testing is frequently used to evaluate several physiologic variables that include the respiratory, cardiac, and metabolic responses to progressive exercise. Besides measuring the functional capacity during exercise, cardiopulmonary evaluation can also identify factors that limit this physiologic variable.2

Until now, the use of this method in children with heart failure has not been reported in the literature. Thus, the objective of this investigation was to evaluate the cardiopulmonary responses of children with heart failure to progressive exercise.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusions
 References
 
Study Population
We studied 26 children (15 girls and 11 boys; mean ± SD age, 8.2 ± 1.9 years) with left ventricular systolic dysfunction and heart failure of > 6 months in duration (idiopathic dilated cardiomyopathy [IC] group); all patients had IC. According to the New York Heart Association (NYHA) criteria,4 16 children were in functional class I, 5 children were in functional class II, 3 children were in functional class III, and 2 patients were in functional class IV. The mean left ventricular ejection fraction (LVEF) at rest, as determined by the radionuclide method, was 25.4 ± 9.9%. The children were being treated with digoxin, angiotensin-converting enzyme inhibitors, and diuretics, in addition to having received general instructions about sodium and water restriction. All patients were in clinically stable condition, with no signs or symptoms of worsening heart failure, and their medications had remained unchanged during the last month. Thus, inclusion criteria for the IC group can be summarized as follows: (1) clinically stable chronic congestive heart failure of at least 3 months in duration, (2) unchanged medications during the preceding month, (3) LVEF <= 45% in the 3 months preceding the study, and (4) a diagnosis of IC.5

As a control group, we used 12 children (8 boys and 4 girls; mean age, 9.6 ± 2.2 years) without known diseases, who had normal physical examination and resting ECG findings (control group). None of the children in the control group participated in organized physical activities. We excluded children who did not adapt to the ergospirometric evaluation (ie, those who did not adapt to the nose clip, mouthpiece, or breathing valve necessary for measurements, or who cried while walking on a treadmill during their previous visit). Children who did not reach their maximal level of effort (respiratory exchange ratio [RER] of > 1.0) or who were < 5 years of age were also excluded from the study. The values for body weight, stature, and body surface area for the control group and IC group, respectively, were 35.6 ± 7.3 kg vs 26.1 ± 7.5 kg, 1.4 ± 0.1 m vs 1.2 ± 0.1 m, and 1.17 ± 0.17 m2 vs 0.96 ± 0.1 m2 (all p < 0.05). The Committee on Ethics of our institute approved this investigation, and the parents or custodians of the study subjects provided informed consent.

Study Design
All children with heart failure who underwent cardiopulmonary exercise testing between August 1996 and May 1998 were considered for study inclusion. All of these children had received outpatient care at the Heart Institute Heart Failure Clinics. The subjects underwent cardiopulmonary testing 1 week before evaluation to familiarize them with the technique and the study protocol. All of the evaluations were performed during the morning, by the same team. The control group was composed of relatives of employees of the Heart Institute. All examinations were performed using the same criteria and procedures.

Cardiopulmonary Exercise Testing
The children underwent 12-lead resting ECG and a progressive treadmill exercise test, with continuous monitoring of the ECG, systemic BP, ventilation, and gas exchange during the test, including the recovery period.6 All children were encouraged to exercise until exhaustion and the RER was > 1.0.7 All patients were studied in a controlled-temperature (21°C to 23°C) exercise facility, at least 2 h after a light meal. The exercise tests were performed on a programmable treadmill (Q = 65; Quinton Instrument; Bothell, WA) according to a modified Naughton protocol.8 Ventilatory and gas exchange data were determined on a breath-by-breath basis with a computerized system (model CAD/Net 2001; Medical Graphics Corporation; St. Paul, MN). The peak O2 consumption (O2) was considered to be the maximum O2 value reached during the test.9 The anaerobic threshold (AT) was determined by analysis of expired gases, performed independently by two investigators. In the event of a disagreement, a third investigator performed this analysis. The following criteria were used for determining the AT: (1) time when the ventilatory equivalent for O2 (minute ventilation [E]/O2) and the end-tidal O2 reached minimum values, before beginning curve ascension; and (2) the time at which the relationship between CO2 production (CO2) and O2 was no longer linear.5 10

Statistical Analysis
Cardiopulmonary variables were compared between groups at rest, AT, and peak exercise using Student’s t test for independent samples. The relative difference (percentage) between two values was calculated as the end value minus the initial value, divided by the initial value, and expressed as a percentage. For both groups, the relative differences were calculated for the cardiopulmonary variables, heart rate, systolic BP, O2/heart rate (O2 pulse), E, O2, and CO2, for the intervals between rest and AT, AT and peak exercise, and rest and peak exercise. The relationship between CO2 and E was studied by fitting a random-effects model and estimating regression line coefficients using 95% confidence intervals. Pearson’s correlation coefficient between peak O2 and the ventilatory equivalent for CO2 (E/CO2) slope was calculated for both groups; it was also calculated between the peak O2 and LVEF and between the E/CO2 slope and LVEF for the IC group. Values of p < 0.05 were considered statistically significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusions
 References
 
Seven children with heart failure were excluded from the study because they did not reach maximum effort (RER of > 1.0).11 Five of these children were in NYHA functional class I, one child was in functional class II, and one child was in functional class IV. Three children in the control group were excluded from the study for the same reason.

Gender
The statistical analysis did not show any gender-based differences in study variables among children in the IC group. The heart rate, O2, and O2 pulse at rest, at AT, and at peak exercise in the boys and girls with heart failure were, respectively, as follows: heart rate, 100 ± 12/min and 107 ± 12/min, 127 ± 23/min and 130 ± 17/min, and 157 ± 23/min and 161 ± 18/min; O2, 4 ± 1.2 mL/kg/min and 6.3 ± 1.5 mL/kg/min, 12 ± 5.8 mL/kg/min and 13 ± 3.4 mL/kg/min, and 18 ± 7 mL/kg/min and 21 ± 5 mL/kg/min; and O2 pulse, 1.1 ± 0.6 and 1.4 ± 0.4, 2.7 ± 1.6 and 2.4 ± 0.8, and 3.4 ± 1.9 and 3 ± 0.9. Due to the small number of girls, similar statistical analysis was not possible in the control group of healthy children.

Rest
The heart rate, respiratory rate, and E/O2 were significantly higher in the IC group. However, the O2 pulse and tidal volume (VT) were significantly lower in this group (Table 1 ).


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  		Table 1.. Cardiopulmonary Variables at Rest in Heart Failure and Control Groups*

 
Exercise
AT: Table 2 shows the results observed at AT. Systolic BP, O2 pulse, E, VT, exercise duration, O2, CO2, E/O2, E/CO2, and functional estimate of dead space (VD/VT) significantly differed between the groups. Peak Exercise: The IC group had significantly lower systolic BP, O2 pulse, E, VT, exercise duration, O2, and CO2. However, the E/O2, E/CO2, and VD/VT were greater in this group (Table 3 ).


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  		Table 2.. Cardiopulmonary Variables at AT in Heart Failure and Control Groups*

 

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  		Table 3.. Cardiopulmonary Variables at Peak Exercise in Heart Failure and Control Groups*

 
Relative Differences in Cardiopulmonary Variables: Figure 1 shows the changes in cardiopulmonary variables between rest and AT, AT and maximum effort (peak exercise), and rest and maximum effort. Statistical analysis showed that the percentage in O2 pulse, E, O2, and CO2 between rest and AT was significantly smaller in the IC group. For the interval between AT and peak exercise, the percentage in heart rate, systolic BP, and E was statistically smaller in the IC group. Statistical analysis also showed the percentage in systolic BP, O2 pulse, E, O2, and CO2 between rest and maximum effort was smaller in the IC group (p < 0.05).



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  		Figure 1.. Percentage difference between rest and AT (rest/AT), AT and maximum effort (AT/max), and rest and maximum effort (rest/max) for the healthy children (control) and children with heart failure due to IC (IC group).

 
E/CO2Slope: Figure 2 shows the relationship between E and CO2 for both groups. The E/CO2 slope for the IC group (slope, 44) was significantly greater than that for the control group (slope, 33) [p < 0.001].



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  		Figure 2.. Relationship between E and CO2 for the control group and heart failure (IC) group.

 
Peak O2 vs E/CO2 Slope: The relationship between peak O2 and the E/CO2 slope for both groups is shown in Figure 3 . The regression line through the data points shows a correlation between the E/CO2 slope and peak O2 in the IC group.



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  		Figure 3.. Relationship between peak O2 and E/CO2 slope for the IC group ({blacktriangleup}, heart failure) and control group ({circ}, control).

 
LVEF vs Peak O2 and E/CO2 Slope: Figure 4 , left, A, and right, B, show dispersion plots for the E/CO2 slope and peak O2, respectively, as a function of the IC group LVEF. No significant correlation was found between these variables.



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  		Figure 4.. Dispersion plots for the E/CO2 slope (left, A) and peak O2 (right, B) as a function of the LVEF for the heart failure (IC) group.

 
Functional Classification vs Peak O2: Figure 5 shows how stratification by the NYHA classification compares with grading according to the peak O2 using the scale of Weber and Janicki.12 The NYHA classification by peak O2 shows that 9 of the 11 children in NYHA class I would be classified as Weber’s class A and that 2 children would be classified as Weber’s class B. Of the four children classified as NYHA class II, one child would be classified as Weber’s class A, one child would be classified as Weber’s class B, one child would be classified as Weber’s class C, and the remaining child would be classified as Weber’s class D. Of the three children in NYHA class III, one would be classified as Weber’s class B, while the other two would be classified as Weber’s class C. The only child in NYHA class IV would be compatible with Weber’s class C.



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  		Figure 5.. Stratification by NYHA classification compared with grading according to the peak O2 in the control children ({circ}) and children with heart failure ({blacktriangleup}) in functional classes I, II, III, or IV.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusions
 References
 
Rest
Our findings demonstrate that the ventilatory abnormalities observed at rest in the children with heart failure were not predictive of tolerance to physical exercise. Factors potentially implicated in the increased ventilatory response in the IC group at rest include changes in respiratory muscle performance, increased pulmonary dead space, stimulation of pulmonary receptors, and alterations in ventilatory control.13

Exercise
AT: Our study found that the relative difference (percentage) between O2 at rest and at AT was significantly smaller in the IC group relative to the control group. This smaller difference in O2 may reflect a reduction in the stroke volume at AT. It has been shown that adult patients with heart failure increase their stroke volume until 40 to 50% of peak O2 is reached. After this time, the stroke volume remains stable or even decreases until maximum (peak) exercise is reached. This is a distinctly different response than that observed in normal individuals.10 14 15 16 In the present study, the relative difference between heart rate at rest and at the AT was similar between groups; however, the heart rate at the AT was significantly higher in the IC group. This finding shows that, in patients with this condition, the heart rate constitutes a fundamental determinant of cardiac performance during exercise. This fact is corroborated by the observation that the relative difference between the O2 pulse at rest and at AT was significantly smaller in the IC group.

Peak Exercise: The children in the control group and IC group attained 84% and 80% of the average maximal heart rate, respectively. These findings are similar to those observed in the studies of healthy children5 6 17 and adult patients.1 18

Mechanisms involved in the heart rate response to physical exercise may include tonic sympathetic nervous system alterations and baroreflex dysfunction at the pulmonary or systemic level.19 20 Down-regulation of ß-adrenergic receptors by chronic exposure to high catecholamine levels might be involved in the blunted chronotropic response to maximal exercise.21 22

Adult patients with heart failure interrupt exercise for O2 values smaller than those observed in normal individuals.3 In the present study, we demonstrated that children with heart failure have smaller peak O2 values than control (healthy) children, and that they are comparable to peak O2 values observed in adults with heart failure.

In adult patients with heart failure, the reduction in peak O2 is related to some parameters but not to LVEF.2 23 We made similar findings in our study of children with heart failure. The decrease in cardiac output associated with heart failure provokes a redistribution of blood flow that is mediated by neurohormonal systems (sympathetic nervous system, renin-angiotensin system, and vasopressin) and local mediators (endothelin). These mechanisms make the tissues extract more O2 from any regional blood and rely on anaerobic metabolism to a greater extent. This is especially true during physical exercise,18 24 when greater O2 extraction occurs, therefore accentuating the arteriovenous O2 difference. With disease aggravation, the blood flow reduction causes the tissues to quickly reach their O2 extraction limit.

The significant difference in O2 pulse observed in the present study is compatible with previous reports25 26 that showed a blunted increase in O2 delivery during exercise in adult patients with cardiac failure. The relationship between heart rate and O2 was not linear in the group of patients with heart failure. The O2 pulse was correlated with O2 uptake but not heart rate.

The systolic BP values were significantly lower in the children with heart failure compared with the healthy control subjects, possibly reflecting depressed myocardial contractility or medication use. This depressed BP response to the exercise has also been noted in previous studies15 16 of adults with heart failure. It is likely attributable to inflammatory processes involving myocytes and the extracellular matrix, progressive degeneration of cardiac fibers, and dysfunction of the autonomic nervous system due to fibrosis, together causing a decrease in the force of cardiac contraction.15 16

Abnormal ventilatory patterns are common in adult patients with heart failure, even at rest. Similar alterations were seen in children with heart failure in this study.27 28 Our patients with heart failure had higher respiratory rates and smaller VTs than the control group at rest, and VT difference was accentuated by exercise. Among factors potentially implicated in the development of pulmonary hyperventilation in heart failure patients during exercise, several factors should be considered: an increase in the pulmonary dead space, altered perfusion dynamics, complacency and intrinsic changes in the respiratory musculature, a decrease in respiratory resistance, decreased hemoglobin saturation, and histochemical alterations.29 30 Another mechanism, however secondary, that can change ventilation during exercise is an increase in the sensitivity of peripheral receptors to muscle-derived mediators.31 The increased chemosensitivity seems to be due to a more intense activation of the sympathetic nervous system. However, the mechanisms involved in respiratory control in patients with heart failure are complex and have yet to be fully clarified.

The relationship between E and CO2 was approximately linear in both groups; however, the E/CO2 slope was significantly different between the patients with heart failure and the control subjects, a finding that correlated with the decrease in functional capacity. A previous study24 in adult patients with heart failure suggested that hyperventilation is not a result of increases in the PCO2, hypoxia, or lactate production during exercise. Mechanisms potentially implicated in the excessive ventilatory response observed in such patients during exercise, and, consequently, the displacement of the E/CO2 slope to the left, could include the following: (1) increases in the physiologic dead space caused by pulmonary ventilation/perfusion mismatches, (2) dysfunction of the respiratory muscles, and (3) abnormalities of peripheral muscle metabolism.24 26 32

The correlation between the E/CO2 slope and peak O2 in the IC group was weak, similar to the results reported33 for adult patients with heart failure. Our results also demonstrate that the first parameter cannot be used to predict maximal physical capacity in patients with heart failure.

The peak O2, E/CO2 slope, LVEF, and NYHA functional classification are frequently used to evaluate both the functional capacity and effectiveness of therapy and as prognostic indicators in adult patients with heart failure. However, a correlation between cardiopulmonary variables at rest and exercise capacity has not been demonstrated.34 The capacity to exercise can be relatively preserved in some patients with left ventricular systolic or diastolic dysfunction, possibly due to the activation of neurohormones.23 In fact, we demonstrated a weak correlation between peak O2 and LVEF, which is consistent with results observed in a study12 of adult patients with heart failure. The LVEF was weakly correlated with the E/CO2 slope; however, the reasons for this relationship are not entirely clear.

The functional classification is often used in the clinical evaluation of a patient with heart failure. Yet, despite a strong correlation with the prognosis, the functional classification has important limitations, such as its poor reproducibility and subjective nature.35 On the other hand, peak O2 constitutes an objective measurement of cardiopulmonary reserve. As it is used in adult patients with heart failure, this measure may allow more objective evaluation of heart failure in children based on exercise capacity.36

Study Limitations: Analysis of our study showed some limitations, with the main limitation being the limited number of children with heart failure (study subjects) and the anthropometric differences between the groups. Another possible limitation is that children may be less willing to undergo cardiopulmonary testing than adults, thereby potentially distorting the test results.

Clinical Implications: Assessment of the cardiopulmonary responses of children with heart failure to progressive exercise on a treadmill yielded similar results to those described in the literature1 2 7 24 25 for adult patients with the same clinical characteristics. From these studies, it is known that there exists a relationship between some variables obtained with cardiopulmonary testing (eg, peak O2) and the patients’ prognosis. The availability of such information also makes the choice of therapy, clinical or surgical, more adequate. Thus, prospective studies, including those with larger numbers of children, must be carried out to determine the importance of using this technique in children with heart failure.


   Conclusions
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
References
 
Cardiopulmonary exercise testing seems to be an important means of evaluating exercise capacity in children with heart failure. The cardiopulmonary abnormalities observed in these children at rest, AT, and peak exercise seem to be the same as those observed in adult patients with the same clinical characteristics. Rest variables did not correlate with values achieved during maximal exercise, which may add important data to the clinical evaluation. Gas exchange analysis during exercise testing may be clinically relevant, as it can identify children with heart failure and differentiate them from healthy children.


   Footnotes
 
Abbreviations: AT = anaerobic threshold; IC = idiopathic dilated cardiomyopathy; LVEF = left ventricular ejection fraction; NYHA = New York Heart Association; RER = respiratory exchange ratio; CO2 = CO2 production; VD/VT = functional estimate of dead space; E = minute ventilation; E/CO2 = ventilatory equivalent for CO2; E/O2 = ventilatory equivalent for O2; O2 = O2 consumption; VT = tidal volume; O2 pulse = O2 consumption for heart rate

Received for publication May 31, 2000. Accepted for publication February 27, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusions
 References
 

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