Pediatr Cardiol (2011) 32:910–916 DOI 10.1007/s00246-011-0013-x
ORIGINAL ARTICLE
Pulmonary Limitation to Exercise After Repair of D-Transposition of the Great Vessels: Atrial Baffle Versus Arterial Switch Lauren E. Sterrett • Eric S. Ebenroth • Gregory S. Montgomery • Marcus S. Schamberger Roger A. Hurwitz
•
Received: 4 January 2011 / Accepted: 17 May 2011 / Published online: 4 June 2011 Ó Springer Science+Business Media, LLC 2011
Abstract This study evaluated resting pulmonary function and its impact on exercise capacity after atrial baffle (BAFFLE) and arterial switch (SWITCH) repair of D-transposition of the great vessels (DTGV). Previously decreased exercise capacity in DTGV patients has been primarily attributed to cardiovascular limitations, whereas pulmonary limitations have largely been overlooked. Resting flow volume loops were compared for BAFFLE (n = 34) and SWITCH (n = 32) patients. Peak exercise variables were compared for BAFFLE (n = 30) and SWITCH (n = 25). Lung disease (restrictive and/or obstructive) was present in 53% of DTGV patients (BAFFLE 62% and SWITCH 44%; p = 0.14). BAFFLE patients had a normal breathing reserve, whereas that of SWITCH patients was decreased (27.3 ± 28.3 vs. 13.0 ± 19.2; p = 0.04). BAFFLE patients attained a lower percent of predicted peak oxygen pulse (82.7 ± 20.5% vs. 94.7 ± 19.3%; p = 0.04) and peak oxygen consumption (VO2peak) (26.6 ± 6.7 ml/kg/min vs. 37.3 ± 8.5 ml/kg/min; p \ 0.01) than SWITCH patients. Patients after surgical repair for DTGV have an underappreciated occurrence of lung disease, even post-SWITCH. SWITCH patients have diminished breathing reserves, suggesting a pulmonary limitation to VO2peak. BAFFLE patients have lower VO2peaks, greater breathing reserves, and lower oxygen pulses than SWITCH patients, suggesting a cardiac
L. E. Sterrett (&) E. S. Ebenroth M. S. Schamberger R. A. Hurwitz Department of Pediatric Cardiology, Riley Hospital for Children at Indiana University Center, 702 Barnhill Drive, RR 127, Indianapolis, IN 46202-5225, USA e-mail:
[email protected] G. S. Montgomery Department of Pediatric Pulmonology, Riley Hospital for Children at Indiana University Center, Indianapolis, IN, USA
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limitation to peak aerobic capacity with probable secondary pulmonary limitations. Treating underlying lung disease in symptomatic patients after repair of DTGV may improve functional status. Keywords Pulmonary function D-transposition of the great vessels Exercise
Introduction Patients born with D-transposition of the great vessels (DTGV) were first given a chance for long-term survival after the Mustard and Senning venous baffle procedures (BAFFLE) were successfully performed during the mid1960s [14]. Concerns about the long-term complications of these procedures arose because many patients developed atrial arrhythmias and systemic right-ventricular failure. A favorable alternative arose in 1977 when the first successful arterial switch (SWITCH) operation was performed by Jatene [15]. The SWITCH technique became routine during the early-to-mid 1980s and has almost completely replaced the BAFFLE for patients with simple DTGV. Patients post-BAFFLE repair are known to have diminished exercise capacities [7, 11, 12, 21], whereas patients post-SWITCH repair have been shown to have mildly diminished to normal exercise capacities [16, 20]. Some of these studies demonstrated diminished lung function at rest in BAFFLE patients, which may contribute to their decreased exercise capacity. Limited data in SWITCH patients suggest near-normal resting pulmonary function in the majority of patients [9, 16]. The primary purpose of this investigation was to assess exercise capacity and prevalence of lung disease in DTGV patients post-BAFFLE and post-SWITCH repair. Our secondary
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purpose was to define cardiovascular and pulmonary limiting factors to peak exercise capacity in DTGV patients.
Materials and Methods Approval for this study was obtained from the Indiana University Institutional Review Board. This was a retrospective study reviewing exercise tests from 2002 to 2009 involving patients post-BAFFLE or -SWITCH repair. Patients included were referred for routine exercise stress testing, with the exception of one BAFFLE patient, who was referred for chest pain and five SWITCH patients who were referred for exercise-related symptoms. This study does not include all DTGV patients from our institution but only those referred for exercise testing. All demographic information, including medication and pacemaker status, was recorded at the date of exercise testing. Surgical information was retrieved from chart reviews.
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not classified. Minute volume ventilation (MVV) was calculated using FEV1.0 9 40 to allow direct comparisons with breathing reserve in other populations with congenital heart disease [13, 16–18]. Breathing reserve was calculated using the equation (MVV—maximal minute ventilation (VEmax)/MVV). Peak Exercise Testing All patients underwent maximal exercise treadmill testing according to the standard Bruce protocol. Handrail support for balance was permitted. Gas exchange measurements were collected during exercise with a Sensormatics V29 metabolic cart using breath-by-breath expired gas collection with 20-s averages for analysis. Rate of carbon dioxide elimination and oxygen consumption was measured continuously during exercise. Oxygen pulse, as an approximation of oxygen consumption per heart beat, was calculated as (VO2peak(ml/min)/peak heart rate).
Inclusion and Exclusion Criteria Statistical Analysis Subjects were only included in the study if their pulmonary function flow volume loops met American Thoracic Society criteria for validity. Exercise tests were excluded if they did not meet criteria for a valid test. A valid peak aerobic capacity (VO2peak) test was defined when a patient had a respiratory exchange ratio (RER) [1.00 and reached volitional exhaustion. No tests were terminated due to arrhythmias or ischemia. Resting Pulmonary Testing Pulmonary function testing was performed immediately before peak exercise evaluation. Baseline flow volume loop pulmonary function testing was conducted, and forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1.0), FEV1.0/FVC ratio, and forced mid-expiratory flow rates (FEF25–75%) were calculated. One pediatric pulmonologist interpreted all flow volume loops using normal values established from the Third National Health and Nutrition Examination Survey [5, 6]. The pulmonologist categorized each patient as having restrictive, obstructive, both restrictive and obstructive lung disease, or normal lungs. A patient was classified with restrictive airway disease if he or she had an FVC \ 80% of predicted for age with a normal FEV1/FVC ratio ([80%). A patient was classified with obstructive airway disease if he/she had an FEV1.0 and/or FEF25–75% \ 80% of predicted for age, as well as an FEV1.0/FVC ratio \ 80%. A patient was classified with both restrictive and obstructive airway disease if he or she had an FVC \ 80% of predicted for age with an FEV1.0/ FVC ratio \ 80%. The severity of lung abnormality was
Results are reported as raw mean values ± SDs. Variables were expressed as a percent of predicted values, based on age or size when appropriate, to account for anthropometric differences between groups. Age and size differences were examined as potential covariates for each of the exercise and pulmonary responses and they were included in the multivariate model when significant. Student t test for continuous and Chi-square test for categorical variable were used to compare anthropometic data between groups. Fisher’s exact test was used to analyze categorical lung function and sex differences between groups. Analysis of variance (ANOVA) models were used to test the association of airway function and exercise markers between the groups, either univariately or multivariately, if covariates were identified. ANOVA models were used to identify possible covariates for all pulmonary function and peak exercise markers. Variables significant at p = 0.15 were included in multivariate models. Model building used both stepwise and forward-selection with entry and exit criteria set at p = 0.05 to identify final parsimonious models for each outcome. The number of sternotomies and interaction between the number of sternotomies and groups were included for both lung function and exercise markers in each of the final ANOVA models. The number of sternotomies was analyzed as a dichotomous variable with the groups being 1 sternotomy versus [ 1 sternotomy. If the interaction was significant, the number of sternotomies was includes in the multivariate model. Data were analyzed using the statistical analysis package, SPSS PASW, version 17 (SPSS, Chicago, IL).
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Results
Table 2 Surgical interventions Interventions
Patients Patients after BAFFLE (n = 43) and SWITCH (n = 45) repairs were tested, and valid pulmonary function test data were identified and analyzed in 34 BAFFLE and 32 SWITCH unique patients. Valid peak exercise data were analyzed in 30 BAFFLE and 25 SWITCH patients who all had valid pulmonary function tests. BAFFLE patients were 16.8 ± 13.2 months old, and SWITCH patients were 3.0 ± 12.4 months old (p \ 0.01) at the time of their surgical DTGV correction (Table 1). All SWITCH patients underwent repair during the first 3 months of life, with the exception of 1 patient, who underwent SWITCH at 5.3 years of age. He had complex coronary anatomy, a ventricular septal defect, and an atrial septal defect. He was palliated with a pulmonary arterial band to allow for growth before repair. BAFFLE patients, as expected, were significantly older and larger than SWITCH patients at the time of testing (Table 1). A subset of patients in both groups, some of whom required repeat stenotomy, underwent additional thoracic surgeries (Table 2). Medication and Pacemakers A small number of patients in both groups were taking medications that may influence peak exercise variables and pulmonary function testing. Two BAFFLE patients were on beta-blockers, seven BAFFLE patients were on ace-inhibitors, one was on digitalis, one was on a diuretic, and one was on a rescue bronchodilator inhaler. Two SWITCH patients had rescue bronchodilator inhalers and were on preventive steroids for obstructed lung disease. One of these patients had a normal baseline flow volume loop, and the other was still mildly obstructed when the exercise test was conducted. Six BAFFLE patients had pacemakers at the time of the tests. Resting Pulmonary Testing BAFFLE patients attained lower values for FVC than SWITCH patients and tended to have lower FEV1.0 Table 1 ANOVA and Chi-square results: demographics Demographics
BAFFLE (n = 34)
SWITCH (n = 32)
Male (% of total subjects)
23 (67)
24 (75)
Age (year)
23.9 ± 4.4
11.8 ± 2.6
\0.01
Age at DTGV repair (month)
16.8 ± 13.2
3.0 ± 12.4
BAFFLE (n = 34)
SWITCH (n = 32)
Surgery requiring sternotomy BAFFLE revision
9
Coarctation of the aorta
1
1
Pulmonary artery band
1
Attempted SWITCH
1
Ventricular septal defect closure
1
Other procedures before DTGV repair Blalock-Taussig shunt by lateral thoracotomy
4
Balloon of coarctation of the aorta
1
2
1
(Table 3). FEV1.0/FVC and FEF25–75% were similar between groups. The flow volume loops were used to classify each patient according to normal airway, restrictive pulmonary disease (decreased FVC), obstructed pulmonary disease (decreased FEV1.0 and/or FEV1.0/FVC ratio), or combined restrictive and obstructive pulmonary disease. Abnormal airways were found in 62% of BAFFLE patients and 44% of SWITCH patients. There were no differences in the occurrence of restrictive, obstructive or restrictive, and obstructive pulmonary disease between surgical repair groups (p = 0.22). Restrictive pulmonary disease occurred in 47% of BAFFLE patients compared with 28% of SWITCH patients; this includes four BAFFLE patients and two SWITCH patients who were both restricted and obstructed. Obstructive pulmonary disease was identified in 26% of BAFFLE patients and 22% of SWITCH patients, which again includes the patients who were both restricted and obstructed. Peak Exercise Testing BAFFLE patients obtained a significantly lower percentage of predicted VEmax than SWITCH patients after adjusting for body mass index (BMI), FVC, and FEV1.0 (p = 0.001) (Fig. 1). BAFFLE patients had a significantly greater breathing reserve than SWITCH patients after adjusting for age at surgery, weight, and BMI (p = 0.04) (Fig. 1).
p Table 3 ANOVA results: pulmonary variables by surgery type Variables
BAFFLE (n = 34)
SWITCH (n = 32)
p
\0.01
FVC (% of predicted value)
79.2 ± 13.5
85.9 ± 11.8
0.04
0.51
Weight (kg)
76.0 ± 20.1
45.9 ± 16.8
\0.01
FEV1.0 (% of predicted value)
80.2 ± 14.9
86.4 ± 13.8
0.09
Height (cm)
171 ± 11
153 ± 15
\0.01
FEV1.0/FVC
85.7 ± 8.5
87.1 ± 7.1
0.49
BMI
26 ± 6
19 ± 5
\0.01
FEF25–75% (% of predicted value)
89.3 ± 28.0
85.3 ± 26.2
0.26
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Fig. 1 Analysis for breathing reserve for 25 BAFFLE and 18 SWITCH patients. Breathing reserve was adjusted for the confounding variables of age at surgery, weight, and BMI. Percent of predicted VE was adjusted for the confounding variable of BMI
BAFFLE patients had a significantly lower VO2peak (ml/kg/ min) than SWITCH patients after adjusting for height and BMI (p \ 0.001) (Table 4). BAFFLE patients reached their VO2peak at a lower percent of predicted than SWITCH patients (p \ 0.001) (Fig. 2). BAFFLE patients had lower absolute peak heart rates than SWITCH patients, but this difference disappeared when heart rate was expressed as a percentage of their age-predicted maximal heart rate (Fig. 2). BAFFLE patients attained a lower percent of predicted peak oxygen pulse (p = 0.04) (Fig. 2). RER tended to be greater in the BAFFLE group versus the SWITCH group, but all patients had RER [ 1.0. There were no significant two-way interactions between groups and the number of sternotomies on any of the pulmonary or exercise variable.
Discussion The prevalence of obstructive pulmonary disease in the healthy United States population is 7.3% in adults and 9.1% in children, with a rare occurrence of restrictive pulmonary disease [2]. In contrast to this, we showed that patients after surgical repair for DTGV have a high occurrence of pulmonary disease at rest, with 62% of BAFFLE patients and 44% of SWITCH patients being affected.
Fig. 2 Percent of predicted oxygen pulse for 28 BAFFLE and 25 SWITCH patients. Percentage of predicted peak heart rate was 27 BAFFLE and 20 SWITCH patients VO2peak (ml/kg/min) was adjusted for the confounding variables of height and BMI
Resting Pulmonary Function The majority of our BAFFLE patients, now 22 years after surgical repair, displayed decreased pulmonary function at rest (62%). Restrictive pulmonary disease alone occurred in 35%, obstructive pulmonary disease alone was identified in 15%, and both restricted and obstructed pulmonary disease were found in 12% of patients. Hruda et al. examined lung function in BAFFLE patients 10 years after repair and identified restrictive disease in 32.1% [12]. Samanek et al. examined pulmonary function in BAFFLE patients 4 years after repair and found decreased FVC values in 60% of BAFFLE patients and decreased total lung capacities in 34% [21]. Hechter et al. identified mildly decreased values for FVC (81% of predicted) and FEV1.0 (86% of predicted) in BAFFLE patients [11]. There was a surprisingly high rate of pulmonary disease in our SWITCH patient population 11 years after repair. A total of 44% of our SWITCH patients had abnormal lung function, with 22% of patients having isolated restrictive pulmonary disease, 16% having isolated obstructive pulmonary disease, and 6% having both restricted and obstructed disease. Two other investigations that mentioned resting pulmonary function in SWITCH patients describe a much lower occurrence of pulmonary disease. Mahle et al. found that 20 of 22 patients had normal flow
Table 4 ANOVA model results: exercise variables by surgery type Variables
BAFFLE (n = 30)
SWITCH (n = 25)
p
Peak heart rate (bpm)
170 ± 18
189 ± 11
\0.01
64 ± 15
85 ± 19
\0.01
Peak oxygen pulse (ml/beat)
11.7 ± 4.6
9.7 ± 3.7
0.08
RER
1.11 ± 0.06
1.09 ± 0.04
0.06
% of Predicted VO2peak (ml/kg/min) obtained (%)
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volume loop variables when tested 10 years after SWITCH repair: one patient was restricted and another was obstructed [16]. Giardini et al. found that their 60 SWITCH patients had average values for FVC (93 ± 12% of predicted) and FEV1.0 (90 ± 14% of predicted) [9]. These averages fall within the normal range, but individual patients with abnormal pulmonary function were not mentioned. The explanation for the relatively high occurrence of abnormal pulmonary function in DTGV patients is unclear. Previous research examining pulmonary function in BAFFLE patients suggests that their airway issues may be caused by prerepair hemodynamic conditions, residual pulmonary stenosis, and/or multiple surgical procedures requiring sternotomy [10, 16, 19, 21]. In any DTGV patient, the heart may dominate the intrathoracic space due to cardiomegaly before surgery, thus decreasing available space for developing lungs. Abnormal pre-repair hemodynamic conditions, including increased pulmonary blood flow and increased pulmonary pressures, may impact lung development and thus long-term lung function. The combination of increased blood flow and pulmonary pressures decreases lung compliance and may blunt lung development [20]. The BAFFLE patients in our investigation were 6 months to 4 years old before they underwent BAFFLE repair. These patients lived with increased pulmonary blood flow and pulmonary pressures for an extended period of time during a crucial period of alveolar development (1–2 years of age) [1]. The lower FVC and trend toward a lower FEV1.0 in our BAFFLE compared with SWITCH patients is consistent with the hypothesis that the timing of DTGV repair may impact lung development. Most SWITCH patients undergo surgical repair during their first 30 days of life. Infants are known to have decreased lung compliance, suggesting that the impact of surgical repair early in life may also be detrimental to lung development [20, 21]. Cardiac surgery can also result in diaphragm hemiparesis, weakened inspiratory muscles, or decreased chest wall compliance, which all can decrease lung function [20]. No patients in our investigation were known to have diaphragm paresis. Chest wall compliance and inspiratory muscle strength would likely be decreased after multiple sternotomies, but these variables were beyond the scope of this study. Our investigation found no effect of the number of sternotomies on resting lung function measures or exercise variables; however, our population with repeat sternotomies was small. A study by Sulc et al. examined pulmonary function and lung stiffness in 26 atrial septal defect patients before and after surgical correction [22]. There was no significant change in pulmonary function after cardiac surgery in these patients; however, there was a high rate of lung disease in these patients both before and after surgery compared with the general population. The
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findings by Sulc et al. suggest that pulmonary disease in cardiac patients may be a function of the effects of the cardiac abnormality itself instead of a result of the surgical repair. The advancements in surgical technique and postoperative care during the period of time these patients were surgically repaired is also a potential confounding variable. A larger cohort must be evaluated to further understand the impact of timing and number of sternotomies on resting pulmonary function and peak exercise values. Limiting Factors to Peak Aerobic Capacity Our BAFFLE patients had significantly lower peak aerobic capacities and attained a lower percentage of their age- and sex-predicted peak aerobic capacity than SWITCH patients. This was anticipated because the BAFFLE procedure limits peak cardiac output due to the systemic right ventricle and an intra-atrial baffle limiting the atrial ‘‘kick.’’ Patients after the BAFFLE procedure often present with sick sinus syndrome, which limits their heart rate response to exercise. Six of 34 BAFFLE patients had pacemakers, and 1 was on a selective b-blocker, both of which can limit peak heart rates. Our investigation found mildly blunted peak heart rates in both BAFFLE and SWITCH patients when expressed as the percentage of age-predicted maximal heart rate attained. Fredriksen et al. found lower peak aerobic capacities, along with lower peak heart rates, in BAFFLE versus SWITCH patients [7]. Other studies have examined peak aerobic capacity in BAFFLE patients and consistently found diminished aerobic capacities and blunted peak heart rates [7, 10–12]. A few studies, with discrepancies in their findings, have examined peak aerobic capacities and peak heart rates in SWITCH patients. The SWITCH patients in our investigation had mildly diminished peak aerobic capacities and heart rates compared with age-matched reference values, which agrees with findings by Fredriksen et al. and Koning et al. [3, 7, 8]. The investigation by Mahle et al. found that most patients had normal peak aerobic capacities and heart rates [16]. Mixed-sex control patients (9–17 years of age) in our laboratory had peak aerobic capacities of 40.1 ± 9.5 ml/kg/min. The SWITCH patients in our investigation attained 88% of their age-predicted maximal heart rate, which is lower than the 90–95% generally accepted for normal patients. Peak oxygen pulse, along with peak heart rate, provides additional information of cardiac-limiting factors to peak aerobic capacity. Oxygen pulse estimates oxygen consumption per heart beat, providing insight into stroke volume and arterial-venous oxygen difference (a-VO2difference). Peak oxygen pulse is calculated by dividing VO2peak by peak heart rate. Normal arterial oxygen saturation
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(assuming normal hemoglobin concentration and function) with a low peak oxygen pulse reflects a low peak stroke volume, poor oxygenation in the lungs, and/or decreased oxygen extraction in the peripheral muscles. Our patients maintained normal arterial oxygen saturations and had no known hemoglobin or metabolic abnormalities, suggesting adequate pulmonary oxygenation and a normal a-VO2difference. BAFFLE patients attained a lower percent of predicted peak oxygen pulse than our SWITCH patients (Fig. 2), suggesting a diminished peak stroke volume in BAFFLE patients. The SWITCH patients had a mildly diminished VO2peak, a mildly diminished peak heart rate, but a preserved peak oxygen pulse, suggesting a normal peak stroke volume and no apparent cardiac limitation to VO2peak. Breathing reserve at peak exercise is useful to evaluate pulmonary limitations to peak aerobic capacity. Breathing reserve is calculated using resting FEV1 and VEpeak values. A normal breathing reserve is between 20 and 40%, but a low breathing reserve suggests that the lungs limit peak exercise [23]. The effect of a pulmonary limitation at rest may be exacerbated with exercise as ventilatory demand increases with increasing exercise intensity [4]. Our investigation found normal breathing reserves in BAFFLE patients. SWITCH patients had diminished breathing reserves, suggesting a primary pulmonary limitation to peak exercise. Mahle et al. found diminished breathing reserves in 27% of SWITCH patients; however, 9% of patients had pulmonary disease at rest [16]. Peak exercise tolerance is limited by the weakest functioning system (cardiac, pulmonary, or musculoskeletal). Our BAFFLE patients were primarily cardiac limited, but their high rate of pulmonary disease at baseline and diminished VEmax suggests a secondary pulmonary limitation to peak exercise. Our SWITCH patients had a predominant pulmonary limitation to peak exercise as demonstrated by their high rate of pulmonary disease at baseline and low breathing reserve.
Conclusion This study had three primary findings: 1. 2.
3.
A large percentage of DTGV patients, despite the type of surgical repair, have significant lung disease at rest. The high rate of ventilatory limitations at rest and diminished breathing reserve appear to limit VO2peak in SWITCH patients. Patients with a primary cardiac limitation, such as BAFFLE patients, may not be significantly limited by an underlying pulmonary problem but may still have functional benefit from treatment of an underlying lung disease.
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Clinicians should be aware of the high rate of occurrence of obstructive and/or restrictive lung disease in all DTGV patients, regardless of the type of surgical repair. Identification of lung disease in this population may lead to appropriate pulmonary treatment and improved functional capacity. Acknowledgments The authors appreciate the generous financial support from the Susan B. Murphy Fund of the Riley Children’s Foundation, Indianapolis, IN, which made this research possible. This research was conducted at Riley Hospital for Children at Indiana University Medical Center.
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