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J Thorac Cardiovasc Surg 2007;133:1533-1539
© 2007 The American Association for Thoracic Surgery

Surgery for Congenital Heart Disease

Late cardiopulmonary and musculoskeletal exercise performance after repair for total anomalous pulmonary venous connection during infancy

^a Division of Cardiology, The Children’s Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pa
^b Division of Cardiothoracic Surgery, The Children’s Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pa
^c Division of Biostatistics and Epidemiology, The Children’s Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pa
^d Division of Neurology, The Children’s Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pa
^e Division of Psychology, The Children’s Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pa
^f Division of Cardiothoracic Surgery, Emory University, Atlanta, Ga
^g Department of Kinesiology, Temple University, Philadelphia, Pa.

Received for publication October 18, 2006; accepted for publication December 13, 2006.

^_* Address for reprints: Michael G. McBride, PhD, Division of Cardiology, Children’s Hospital of Philadelphia, 34th and Civic Center Blvd, Philadelphia, PA 19104. (Email: mcbride{at}email.chop.edu).

	Abstract

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Objectives: We evaluated cardiopulmonary function at rest and during exercise in children after surgical repair for total anomalous pulmonary venous connection.

Background: Long-term assessment of cardiopulmonary function during exercise in children after repair for total anomalous pulmonary venous connection during infancy is limited.

Methods: Resting lung function and cardiopulmonary function during maximal ramp cycle ergometry were evaluated in 27 patients (age = 11 ± 4 years, 20 were male). Peak oxygen consumption, ventilatory anaerobic threshold, and physical working capacity were compared with normal reference values. Neurologic assessment included neuromuscular function, inattentiveness, and hyperactivity. Patient- and procedure-related variables were assessed for association with peak oxygen consumption, ventilatory anaerobic threshold, and physical working capacity.

Results: Compared with healthy children, peak oxygen consumption (88% ± 16% of predicted) and ventilatory anaerobic threshold (91% ± 21% of predicted) were mildly reduced. Chronotropic impairment was observed in 7 patients (32%). Patients with impaired resting lung mechanics were more likely to have impairment in peak oxygen consumption (P < .05). Breathing reserve was normal. Specific anatomy and all operative factors did not have a significant impact on overall exercise performance. Composite score for fine and gross motor function was associated with lower ventilatory anaerobic threshold (P < .05).

Conclusions: Exercise performance is mildly impaired at long-term follow-up after total anomalous pulmonary venous connection repair during infancy. Residual pulmonary abnormalities are common and associated with lower exercise performance. Neurologic abnormalities are evident in a subgroup, but the impact on late exercise performance is inconclusive.

	Introduction

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Total anomalous pulmonary venous connection (TAPVC) presents with several anatomic variants that subject patients to different risks and potential complications. Improvements in surgical techniques, preoperative stabilization, and postoperative care have resulted in lower mortality and increased short- and long-term survival over the past 30 years.¹ However, the majority of studies report early surgical and long-term hemodynamic outcomes by cardiac catheterization or resting echocardiography. Assessment of cardiovascular, pulmonary, and musculoskeletal systems during exercise has been limited. Residual cardiopulmonary abnormalities undetected at rest may result in impaired function during exercise.² Although these abnormalities seem to be well tolerated, no data exist that describe the long-term impact of isolated TAPVC surgically repaired during infancy on indices of exercise performance.

The purpose of this study was to evaluate long-term cardiac, pulmonary, and musculoskeletal function at rest and during exercise in children after surgical repair for TAPVC during infancy, and to estimate the impact of perioperative and specific neurologic factors on long-term cardiopulmonary exercise performance.

	Materials and Methods

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Patient Population
Children eligible to participate in this study included all patients with simple TAPVC admitted to The Children’s Hospital of Philadelphia between November 1983 and November 1996. Simple TAPVC is defined as TAPVC with no other cardiac anomalies except for patent foramen ovale, atrial septal defect, coarctation of the aorta, or patent ductus arteriosus.³ A total of 104 children were identified as candidates for inclusion in the study, 4 of whom died before surgical intervention; of this total, 100 survived to surgery. The hospital mortality rate was 14%, and 2 children died long-term postoperatively. Ten patients were lost to follow-up. Of the 74 late survivors, 60 were surgically repaired during infancy and at least 6 years of age at the time of this study. The parents/guardians of 42 of these 60 children were successfully contacted. Of these 42 families, 27 agreed to participate in this study. Before testing, each patient and a parent/guardian signed an informed assent/consent in accordance with The Children’s Hospital of Philadelphia Institutional Review Board, Committee for the Protection of Human Subjects.

Resting Lung Mechanics
Pulmonary function was evaluated before the exercise test using standard methods for spirometry, lung volumes, and conductance.⁴ Forced vital capacity (FVC), forced expiratory volume in 1 second (FEV₁), forced expiratory flows at 25% to 75% of FVC (FEF_25-75), and the ratio FEV₁/FVC were measured and compared with appropriate reference values.⁵ Maximal voluntary ventilation (MVV) was used to calculate the breathing reserve (BR) at peak exercise using the formula: BR = [1–(VE/MVV)] x 100, where VE equals the minute ventilation (VE) at maximal exercise.⁶

Cardiovascular Monitoring
Cardiac rhythm was monitored continuously and recorded intermittently during each study using standard electrocardiography. A peak heart rate response less than 2 standard deviations from the normal value (heart rate < 185 beats/min) was used as criteria for chronotropic impairment.^7,8 Blood pressure was measured by auscultation at rest and every 3 minutes during exercise and recovery.

Exercise Capacity
Patients were exercised to maximal volition (respiratory exchange ratio > 1.10) using a 1-minute incremental ramp cycle ergometer protocol.⁷ Metabolic and ventilatory data were obtained on a breath-by-breath basis using a metabolic cart (SensorMedics, Yorba Linda, Calif). Parameters measured included minute oxygen consumption (VO₂), minute carbon dioxide production (VCO₂), VE, respiratory exchange ratio, respiratory rate (f), tidal volume (TV), dead space-to-tidal volume ratio (DS/TV), and the ventilatory equivalents for oxygen and carbon dioxide (VE/VO₂, VE/VCO₂). The oxygen pulse (O₂P) for each patient was calculated by dividing the VO₂ by the simultaneous measured heart rate and indexed to height (centimeters).⁹ The ventilatory anaerobic threshold (VAT) was measured by the V-slope method.¹⁰ Ventilatory efficiency during exercise was assessed by calculation of the slope of the increase in VE versus VCO₂ from the onset of workup to the inflection point in the V-slope. Mechanical work efficiency was determined by calculating the change in work rate, measured in Watts (W), over the change in oxygen consumption (W/VO₂) measured at an respiratory exchange ratio of 0.95 or less.¹¹ Metabolic and ventilatory data were compared with healthy age- and gender-matched children using the same exercise protocol.^9,12

Echocardiography
Resting echocardiograms included a complete 2-dimensional echocardiogram with Doppler evaluation and were recorded on videotape and/or digital transfer medium. Echocardiography assessed the presence of a residual atrial septal defect and the presence of obstruction within the pulmonary veins. Specific measurements during the echocardiogram included right ventricular pressure estimate, when observable from the tricuspid insufficiency jets, and left ventricular shortening fraction.

Neurologic Examination
The developmental history and neurologic examinations were conducted by a single, senior, board-certified pediatric neurologist who is familiar with the neurodevelopmental issues in children who have undergone infant heart surgery. The protocol for the neurologic examination has been described.¹³ Briefly, the examination assessed muscle tone, strength, symmetry, reflexes, and coordination of fine and gross motor activities. All findings are recorded on case report forms. Abnormal motor abnormalities included those with a diagnosis of cerebral palsy or obvious impairments of motor function. Suspect scores were coded for those with more subtle disturbances, such as impaired hand or finger-tapping sequences, uncoordinated rapid alternating movements of the hands, or inability to hop repetitively on 1 foot. The composite score reflected any abnormality of fine or gross motor ability. The impression of hyperactivity or attention deficit was based on parental interview and clinical observation but not by a formal psychologic battery.

Data Analysis
Data analysis consisted of generating descriptive statistics for all relevant variables in the data set. Independent t tests were used to detect differences between the patients who underwent TAPVC and age and gender-match reference data in 4 key areas: (1) cardiovascular function at rest, (2) cardiovascular function during exercise, (3) pulmonary function at rest, and (4) pulmonary function during exercise. Single- and multiple-covariate linear regression models were fitted and tested for 3 exercise-related end points, VO₂peak, VAT, and peak work capacity (PWC). Any single covariate with a P value less than .15 was considered a candidate for inclusion in a multiple-covariate equation. Because of the exploratory nature of the study, and the general lack of exercise-related information on school-age survivors of TAPVC, alpha was not adjusted for multiple comparisons, thereby keeping the criterion for statistical significance at = 0.05 level for all analyses.

	Results

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Patient demographics and anatomy of the pulmonary venous drainage are summarized in Table 1. All patients were clinically healthy with none taking routine cardiac medications.

Demographic and echocardiographic data at the time of testing are summarized in Table E1. No patient had greater than mild tricuspid regurgitation on resting echocardiography. There was evidence of mild flow acceleration at the pulmonary venous anastomosis in 1 patient whose right ventricular pressure estimate was 28 mm Hg.

Aerobic capacity, as measured by percentage of predicted VO₂peak, for the group was significantly lower than normal values for age and gender (P = .01). However, only 3 patients (13%) had significant impairment of aerobic capacity below the 95% confidence limit for age and gender. Raw VAT and percentage of predicted values, reported in 25 patients (93%), was significantly lower than the normal value for age and gender (P = .01). Mean raw VAT for 3 of the 5 patients who did not achieve peak aerobic capacity was 19.5 ± 6.8 mL/kg/min (90% ± 16% of predicted).

Resting Pulmonary Function
Indices of resting lung mechanics are summarized in Table 3. FVC was significantly (P = .01) below the mean predicted value for age and height in all but 5 patients (18%). Similarly, significant differences were observed in FEV₁ (P = .01) and FEF_25-75 (P = .01) in 4 patients (15%) and 5 patients (18%), respectively, when compared with normal values for age and height. When FEV₁ was expressed as a percentage of the FVC (FEV₁/FVC), this ratio was within the expected value for all but 9 patients (33%).

Neurologic Function
The results from the neurologic examinations are presented in Table E2. Neurologic function in 10 of the 27 subjects (37%) was rated as abnormal or suspect on the overall neurologic assessment. Forty-four percent of the subjects were found to have deficits in 1 or more of the 4 domains (attention, hyperactivity, fine motor, gross motor) assessed during this study. Neuromuscular assessment was rated as abnormal or suspect in 7 of the subjects (26%).

Fourteen different cardiovascular and pulmonary risk factors (Tables E1 and 2-4) were also tested for association with long-term exercise performance. O₂P at peak exercise was associated with higher values for VO₂peak (P = .03) and PWC (P = .02). There was no association between any candidate of exercise performance and the chronotropic response. Those patients with impaired FEV₁ and FEV₁/FVC were more likely to have impairment in VO₂peak (P = .04 and P = .02, respectively), although those patients who achieved higher VE during exercise were more likely to achieve greater VO₂peak (P = .03). Although DS/TV at peak exercise was above the mean for age and gender, it was not associated with lower VO₂peak (P = .63).

Six different neurologic risk factors (Table E2) were tested for inclusion in a multicovariate statistical model to predict long-term exercise performance. Whereas there was a tendency toward lower PWC (P = .11) in those subjects who scored lower in the composite score of neuromuscular function (gross motor and fine motor), none of the assessments for neurologic function significantly affected overall exercise performance as measured by VO₂peak and PWC. However, lower composite score in neuromuscular function was significantly associated with lower VAT (P = .03).

Determinants of Aerobic Exercise Performance
To test for synergistic effects, covariates with P less than .15 were entered into multicovariate analyses to arrive at the best fitting model for each of the 3 primary outcomes of exercise performance (Table E3). According to multicovariate analysis using the subjects’ demographics, perioperative data, and pulmonary variables, the strongest predictors of peak exercise performance, as measured by VO₂peak, were FEV₁ and O₂P (P = .02). The strongest predictors of submaximal exercise performance, as measured by VAT, were diastolic blood pressure and neuromuscular function (P = .07). Last, the strongest predictors of musculoskeletal performance, as measured by PWC, were gender and O₂P (P = .01).

	Discussion

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Similarly, data from this study suggest mild impairment in submaximal exercise performance, as measured by VAT. Although less impaired than VO₂peak, the mild impairment in submaximal exercise performance may be more discouraging than that observed in VO₂peak. The VAT is often considered a more reliable marker of aerobic fitness because of its ability to be sustained over a longer period of time and its sensitivity to aerobic deconditioning and sedentary lifestyle.⁶

Our data indicate that PWC and work efficiency is within normal range for age and gender despite limited aerobic parameters of performance and is superior to that reported in other cardiac lesions requiring early repair.^8,15 This is not surprising given that lesions requiring early surgical repair, such as tetralogy of Fallot and atrial switch physiology, often have residual hemodynamic abnormalities.

The incidence of mild chronotropic impairment seen in this study is inconsistent with the findings of previous studies. An early report by Byrum and colleagues¹⁶ found normal sinus node function in 7 late survivors, whereas a more recent study by Paridon and colleagues² found mild chronotropic incompetence in 5 of 6 children at late follow-up. Reasons for these discrepancies are unclear and probably multifactorial. However, it is not uncommon for children with cardiac lesions requiring extensive atrial surgery to exhibit some level of sinus node dysfunction. Often a blunted chronotropic response has been implicated in the reduction in aerobic capacity.

The results of this study indicate that decreased aerobic capacity is not directly related to the heart rate response. The poor correlation between peak heart rate and VO₂peak (r = 0.07, P = .76) in this study suggests that, at least over the range of chronotropic responses observed in these patients, VO₂peak depends more on other factors than on the heart rate response alone. Some of these other factors may include widening of the arteriovenous oxygen difference or changes in stroke volume. Although the level of regular physical activity was not assessed in these patients before the study, no patients had medically prescribed exercise restrictions. Nevertheless, physical inactivity leading to aerobic deconditioning may be a reasonable speculation based on our data.

Resting Pulmonary Function
Indices of resting lung mechanics in patients evaluated in this study were mildly decreased when compared with normative data in healthy populations. The proportionate decreases in FVC and FEV₁ reflect a pattern of restrictive airway physiology. This was suggested by the normal FEV₁/FVC ratio observed in this group. However, proportionally greater reductions in mean expiratory flows (FEF_25-75) were observed, suggesting small airway dysfunction commonly seen in obstructive airway physiology. Of the measurements of resting lung mechanics, FEV₁ and FEV₁/FVC (Figure E1) were independently related to VO₂peak. Therefore, data from this study suggest an obstructive component of airway physiology such that when coupled to an underlying mild restrictive process, a more profound impact on aerobic capacity is observed.

View larger version (7K): [in this window] [in a new window]   Figure E1. Relationship of FEV1/FVC to peak oxygen consumption. FEV1, Forced expiratory volume in 1 second; FVC, forced vital capacity; VO2, minute oxygen consumption.

In a single study performed at the same institution, Mahle and colleagues¹⁸ examined pulmonary and cardiovascular function at rest and during exercise in a subset (n = 22) of children (mean age = 11 years) surgically repaired for D-transposition of the great arteries during infancy. All patients in their study underwent a single surgical repair using similar perioperative techniques (eg, cardiopulmonary bypass, deep hypothermic circulatory arrest). Identical protocols for the measurements of pulmonary mechanics at rest and cardiovascular performance during exercise were used. Although the surgical intervention used to palliate D-transposition of the great arteries is arguably more complex than that of TAPVC, Mahle and colleagues reported mean values for pulmonary function at rest and cardiovascular performance during exercise were 100% and 113% of predicted for age and gender, respectively. Therefore, data from the current study implicate in utero developmental changes unique to TAPVC physiology as more likely rationale for the persistent abnormalities in pulmonary function and exercise performance rather than the effect of thoracic surgery.

Exercise Pulmonary Function
Data from this study indicate that the dynamic responses of the pulmonary system to exercise in these children surgically repaired for TAPVC during infancy are different than those of children of similar age and gender. Table 4 illustrates the increase in VE and the relative contribution of its components ("f" and TV) in response to progressive exercise. Similarly, the increase in TV/FVC and VE/VO₂ illustrates the relative increase in depth of breathing and increasing ventilation in relation to VO₂, respectively.

It has been suggested that children have breathing patterns similar to that in adults, as measured by the relative contributions of "f" and TV to VE during progressive exercise. In 177 boys and girls (mean age = 11 years), Armstrong and colleagues¹⁹ showed as exercise increased to maximal levels, there was a greater reliance on "f" to create VE as indicated by the increase in f/TV ratio (41%-47%), whereas the TV/FVC ratio remained relatively stable (38%-41%) throughout progressive exercise. Data from the current study are consistent with such a pattern. However, the extent to which the TV could increase was limited, as noted by the lower average value for TV across exercise intensities. Therefore, the greater than normal increase in "f" to meet the ventilatory requirement for exercise likely contributed to the high DS/TV seen at peak exercise as a consequence of greater ventilation of anatomic dead space rather than any intrinsic lung parenchymal disease.

The analysis of the slopes of VE versus VCO₂ enabled an assessment of the breathing patterns related to the efficiency of the ventilatory response to metabolic demands. Data from this study indicate 72% of the patients had abnormal ventilatory responses to progressive exercise when compared with normal values for age and gender. Although these results are superior to data reported in other congenital cardiac lesions, residual hemodynamic abnormalities often seen in such defects as tetralogy of Fallot and Fontan physiology preclude reliable comparison.^17,20

Regardless of the cause of the pulmonary impairment, exercise performance in children surgically repaired for congenital heart disease is seldom limited by their pulmonary system.²¹ This is because the impaired function of the cardiovascular system usually limits oxygen delivery before the pulmonary reserve is exhausted. The adequate BR at peak exercise (19% ± 11%) in this study suggests the limitation in exercise performance was not primarily a factor of their underlying pulmonary abnormalities.

Neurologic Function
Neurologic status and exercise performance have been assessed in a variety of congenital heart anomalies requiring early surgical repair. However, the relationship of one to the other has not been explored. To the extent that neurologic function was assessed, the results of this study are inconclusive. Although these results indicate that a subgroup of children surgically repaired for TAPVC during infancy exhibit a pattern of neurologic dysfunction characterized by deficits in attention, hyperactivity, and neuromuscular function, these abnormalities do not clearly affect late cardiopulmonary exercise performance. This is encouraging given the persistent neurodevelopmental abnormalities seen in other congenital heart defects requiring early surgical repair.^22,23

Limitations
The main limitation of this study was the cross-sectional design. Therefore, inferences about the long-term impact of surgical repair for TAPVC during infancy are limited. This study was also limited by its small sample size. On the basis of the similarities between those who returned for testing and those who were eligible but did not return, there does not seem to be an obvious selection bias. However, other factors not accounted for between those subjects who returned for testing and those who optioned not to return, such as parental status, race and ethnicity, and geographic demographics, could contribute to the results of this study. In addition, the relative small size of the sample precluded more sophisticated statistical modeling and analysis. Finally, the noninvasive assessment of exercise performance may have precluded the identification of all cardiovascular, pulmonary, and hemodynamic abnormalities otherwise identified with more invasive methods.

	Conclusions

Top Abstract Introduction Materials and Methods Results Discussion Conclusions References

 
Although the subjects were clinically asymptomatic at rest, residual abnormalities of the cardiovascular and pulmonary system during exercise persist at late follow-up in children surgically repaired for TAPVC during infancy. Specifically, obstructive airway physiology is evident on long-term follow-up. Whether this attribute is unique to abnormal development of the pulmonary veins or is evidence of subclinical pulmonary disease has yet to be fully clarified. As in other congenital heart defects requiring early surgical repair, deficits in neurologic function persist at late follow-up after repair for TAPVC during infancy. However, the impact on long-term functional outcome, as measured by the indices of exercise performance, has yet to be fully clarified. Although the mild abnormalities in cardiovascular, pulmonary, and neurologic function seem to be well tolerated, careful continued observation is required as these patients enter adulthood.

	Footnotes

 
Supported in part by a grant from the National Institutes of Health General Clinical Research Center (Grant No. M01-RR-00240).

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Michael G. McBride Paul M. Kirshbom J. William Gaynor Thomas L. Spray Permission Requests Citing Articles Citing Articles via Google Scholar Google Scholar Articles by McBride, M. G. Articles by Paridon, S. M. Search for Related Content PubMed PubMed Citation Articles by McBride, M. G. Articles by Paridon, S. M.