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Medicine & Science in Sports & Exercise:
doi: 10.1249/MSS.0b013e31827b0b20
Clinical Sciences

Enhanced Physiology for Submaximal Exercise in Children after the Fontan Procedure

BANKS, LAURA; MCCRINDLE, BRIAN W.; RUSSELL, JENNIFER L.; LONGMUIR, PATRICIA E.

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Author Information

Division of Cardiology, Labatt Family Heart Centre, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, CANADA

Address for correspondence: Patricia E. Longmuir, Ph.D., Healthy Active Living and Obesity Research Group, Children’s Hospital of Eastern Ontario Research Institute, 401 Smyth Dr., RI#1-214, Ottawa, Ontario, Canada K1H 8L1; E-mail: plongmuir@cheo.on.ca.

Submitted for publication May 2012.

Accepted for publication October 2012.

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Abstract

Purpose: After the Fontan procedure, children exhibit reduced peak exercise capacity, yet their submaximal exercise response remains unclear. This study sought to determine the relationship between submaximal and peak exercise capacity and physical activity in Fontan patients.

Methods: This cross-sectional study recruited 50 Fontan patients (59% males) with a median age of 9 yr (range = 6–12 yr). The median age at Fontan procedure was 2.9 yr (range = 1.6–9.1 yr). Study assessments included medical history, exercise testing, and accelerometry.

Results: Significantly lower submaximal oxygen consumption (V˙O2) and HR in response to a standardized workload than published values for healthy children (mean ± SD) of −1.72 ± 5.24 (P < 0.001) and −1.45 ± 1.98 (P < 0.001), respectively, suggest enhanced submaximal work efficiency in this group of patients after Fontan. Higher submaximal V˙O2 z-score was associated with higher submaximal HR z-score (P = 0.02) and lower body mass index z-score (P = 0.01). Higher V˙O2peak was associated with higher submaximal V˙O2 z-score (P < 0.01), male sex (P = 0.03), higher RER (P = 0.02), lower submaximal HR z-score (P < 0.01), and higher chronotropic responsiveness (P < 0.0001). Exercise test duration z-score was associated with lower submaximal HR z-score (P = 0.02) and higher chronotropic responsiveness (P = 0.02).

Conclusions: Fontan patients exhibited a lower submaximal V˙O2 and HR responsiveness at a given workload than healthy controls did during standardized exercise testing. Thus, they may be better adapted to perform submaximal exercise. Although peak exercise capacity is limited, Fontan patients are able to perform submaximal physical activities at the same level as their healthy peers.

The functional status of the pediatric Fontan cohort has become increasingly important given the improved long-term survival rates into adulthood. Peak exercise capacity (i.e., V˙O2peak) is a criterion measure of cardiorespiratory fitness and functional status (31). It can be defined as the highest oxygen consumption obtained during incremental exercise despite increase in workload. Submaximal exercise is commonly used to predict peak or maximal exercise capacity, whereby the cardiorespiratory response (i.e., HR and oxygen consumption) to one or more submaximal work rates is measured (31). A lower submaximal V˙O2peak and HR for a given workload is indicative of greater physical fitness (31). Both submaximal and peak exercise capacity are objectively measured through cardiopulmonary exercise testing.

After the Fontan procedure, children with functional single ventricle morphology demonstrate lower physical activity levels and lower peak exercise capacity attributed to a combination of cardiopulmonary, muscular, and psychosocial limitations (13,17,30,33). Although exercise capacity is near-normal among most children with congenital heart disease (10,22,29), it is typically two-thirds of the expected normative V˙O2 in children after Fontan surgery (17,23). Less is known about submaximal exercise capacity in the presence of congenital heart disease. Anaerobic threshold may be reduced after the Fontan procedure (33). However, Paridon et al. (23) have reported that submaximal exercise capacity may be better preserved than peak exercise capacity. If that were true, children after the Fontan may be better able to perform submaximal exercise than would be expected by their V˙O2peak results. Specifically, the combined objective assessments of submaximal V˙O2, V˙O2peak, and physical activity levels may better characterize functional status and assist health care providers in setting appropriate expectations and guidelines regarding physical activity participation.

The primary objective of this study was to determine the submaximal exercise capacity for children after the Fontan procedure, in reference to published normative exercise testing data for children with innocent heart murmurs (6). A secondary objective was to determine the relationships between submaximal and peak exercise capacity, HR responsiveness, and objectively measured physical activity levels. We hypothesized that children after Fontan procedure would have reduced submaximal and peak exercise capacity, related to HR responsiveness, but independent of physical activity levels.

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METHODS

This study was approved by The Hospital for Sick Children Research Ethics Board, and participants and their parents (or legal guardian) gave written informed assent and/or consent. It was conducted as part of a larger clinical trial, examining the effects of a home-based physical activity intervention on increasing physical activity and gross motor skills and developing positive attitudes toward activity in children after the Fontan procedure, which has been described previously (13).

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Study Participants

Briefly, all eligible Fontan patients from The Hospital for Sick Children were invited to participate in this study. As a result, 50 participants were recruited who could complete the exercise testing protocol and met the following inclusion/exclusion criteria: >1 yr post-Fontan procedure, 6–12 yr old, and no other physical activity contraindications. Cardiac history was abstracted from medical records.

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Cardiopulmonary Exercise Testing

Children fasted for 2 h before the cardiopulmonary exercise test. To promote exercise equipment familiarization, children performed 2 × 2-min warm-up stages (6% grade at 1.0 km·h−1 and 8% grade at 2.0 km·h−1), which preceded the standardized Bruce protocol treadmill test (General Electric T-2000 treadmill). Body mass (kg) and height (m) were measured before the exercise test, and body mass index (BMI) was calculated (a ratio of mass to height [kg·m−2]) and normalized for age and sex (4). Standard 12-lead ECG (CASE 8000; GE Medical Systems, Milwaukee, WI), blood pressure, and breath-by-breath analysis of metabolic variables, including oxygen consumption (V˙O2) and RER were monitored during each stage using a metabolic cart (MAX-2 metabolic cart; Physio-Dyne, Quogue, NY). Each graded exercise test progressed until either voluntary or symptom-limited exhaustion. Submaximal V˙O2 data were derived during the last 60 s of each completed stage of the Bruce protocol. Partially completed stages of the Bruce protocol were excluded from submaximal V˙O2 data. V˙O2peak was defined as the highest V˙O2 achieved, and the corresponding HR value was recorded. Chronotropic responsiveness was calculated from recorded HR data using a previously reported equation (1,9), modified to better predict peak HR response in children (16):

Equation (Uncited)
Equation (Uncited)
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Total exercise test duration was also recorded at the end of the test. Inclusion of cardiopulmonary exercise testing data within this analysis required that participants were able to complete at least one stage of the Bruce protocol graded exercise test while breathing into the cardiopulmonary gas collection tube.

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Accelerometry use.

Children were provided with an omnidirectional accelerometer (Mini Mitter Respironics, Actical 2.1; 15-s epoch data storage), which was worn above the iliac crest at the midaxillary line for five schooldays (i.e., weekday) and two non–school days (i.e., weekend). A physical activity log was provided to record the reason and periods for which the accelerometer was removed. Accelerometry data were considered valid and included in analyses if the monitor collected at least 8 h of valid accelerometer measurements per day on at least three weekdays and one weekend day. Accelerometer malfunction removed the baseline data for one participant. Data were obtained and included in the analysis for all other participants because they achieved at least 4 d of monitoring.

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Data analysis.

A cut point for the definition of moderate-to-vigorous physical activity from accelerometry was set at 1600 counts per minute (24). Total time spent performing daily and weekly physical activity was calculated. All cardiopulmonary test z-scores and sample t-tests were computed to compare Fontan and healthy participants, including submaximal V˙O2, HR, and total exercise test duration. Z-scores were calculated, within age and sex strata, using data from normal children with innocent heart murmurs (6). Exercise data from each completed submaximal stage of the Bruce protocol were included in the analysis. Summary data are reported by stage with the mean ± SD or median (range), where appropriate. Linear regression models using a maximum likelihood algorithm for variable selection were used to determine predictors of submaximal exercise capacity, peak exercise capacity, exercise test duration, and physical activity. Linear regression data are reported with a parameter estimate and SE. Regression modeling with repeated-measure analysis was also conducted to determine the influence of participant dropout at any given stage. Statistical significance was P < 0.05. All analyses were performed by the primary author using SAS software (version 9.2; SAS Institute, Cary, NC).

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RESULTS

The characteristics of our study participants are similar to that of the larger cohort from which the participants were derived (13). A total of 50 participants (59% males) were recruited at a median age of 9 yr (range = 6–12 yr). The median height percentile was 22% (range = <0.01% to 93%). The median age at Fontan procedure was 2.9 yr (range = 1.6–9.1 yr), with a median follow-up interval from Fontan procedure of 6.2 yr (range = 1.4–9.6 yr). The median resting oxygen saturation was 98% (range = 92%–100%). The underlying cardiac anatomy included hypoplastic left heart syndrome (32%), double-inlet left ventricle (22%), tricuspid atresia (19%), double-outlet right ventricle (20%), and pulmonary atresia (6%). The type of Fontan connection included an extracardiac conduit or tunnel (88%), intracardiac lateral tunnel (10%), or Bjork procedure (2%). Complications after Fontan procedure included arrhythmia (42%), thrombosis (34%), and stroke (8%). A small percentage of participants had a patent fenestration (12%, 6/50). Current medication treatment included at least one of the following: acetylsalicylic acid (48%), angiotensin-converting enzyme inhibitors (42%), cardiac glycosides (10%), warfarin (10%), and/or β-blockers (8%), with the exception of 22% of participants who were not prescribed any of the aforementioned medications. A pacemaker had been placed in 4% of participants. Participants had a BMI z-score of 0.12 ± 1.03 (P = 0.11).

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Cardiopulmonary exercise testing.

Cardiopulmonary responses to the graded exercise test are summarized by stage in Table 1. All participants completed at least one stage of the Bruce treadmill protocol. V˙O2peak exercise test duration was reduced with a z-score (mean ± SD) of −2.10 ± 1.05 (P < 0.001). Chronotropic responsiveness to peak exercise was 57% ± 22%. Submaximal oxygen consumption (V˙O2) and HR response z-scores were reduced: mean ± SD of −1.72 ± 5.24 (P < 0.001) and −1.45 ± 1.98 (P < 0.001), respectively. These significantly lower z-scores for submaximal exercise response indicate that during each submaximal stage of the Bruce protocol (protocol stages 1, 2, and 3), study participants required significantly less effort (i.e., lower HR and lower energy consumption) than published values for healthy children (6). Participants had a V˙O2peak of 28.0 ± 5.3 mL·kg−1·min−1 with a corresponding peak HR (HRpeak) of 152 ± 27 bpm. The factors associated with submaximal and peak exercise capacity, exercise duration, and physical activity are shown in Table 2. Briefly, in a linear regression model (using a maximum likelihood algorithm), higher submaximal V˙O2 z-score was associated with higher HR z-score and lower body mass index z-score. Higher V˙O2peak was associated with higher submaximal V˙O2 z-score, male sex, lower submaximal HR z-score, higher chronotropic responsiveness, and higher RER. Exercise test duration z-score was associated with submaximal HR z-score and chronotropic responsiveness. In a regression model (adjusted for repeated measures on each patient), accounting for differences in dropout at each of the stages, our primary outcome of lower relative oxygen uptake z-score relative to published norms was conserved overall and for each stage individually.

Table 1
Table 1
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Table 2
Table 2
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Objectively measured physical activity levels.

Participants’ performed 363 ± 137 min·wk−1 of moderate-to-vigorous physical activity (13). Moderate-to-vigorous physical activity was not associated with submaximal V˙O2 z-score, V˙O2peak, or exercise test duration z-score. Factors influencing participants’ physical activity levels have been previously described (13).

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DISCUSSION

Previous studies have consistently identified a reduction in peak exercise performance in children after the Fontan procedure (8,17,21,23,33,34). Few studies have examined the physiological response to submaximal exercise, which, in contrast to peak exercise capacity, may actually fall in a healthy range (23). In fact, our study participants exhibited lower submaximal V˙O2 and HR response at a given workload during standardized graded exercise testing than published data for healthy controls. This suggests that they may be better adapted to perform submaximal exercise, despite a reduction in peak exercise capacity (V˙O2peak). These findings were related to HR responsiveness, and independent of objectively measured physical activity levels and participant dropout at any given stage. Future research is required to elucidate the mechanism responsible for the preservation or enhancement of submaximal exercise performance. One hypothetical mechanism to explain these findings would be more efficient oxygen extraction by the working muscles in response to decreased oxygen saturation levels before the final Fontan repair. Greater peripheral exercise system effectiveness may be capable of compensating for the central limitations of cardiac output at submaximal levels of exercise. Future research may also investigate the translation of these findings into healthy cohorts. Greater peripheral exercise system effectiveness may possibly be translated to healthy children through activities that focus on high-intensity interval training of the peripheral muscles.

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Submaximal and peak exercise performance in children after the Fontan procedure.

Previous studies of submaximal exercise capacity in Fontan participants have primarily relied on ventilatory anaerobic threshold and RER for defining submaximal exercise (23,33). Although anaerobic threshold may be reduced after the Fontan procedure (23,26,30,33), differentiating between submaximal and V˙O2peak can be difficult in children with congenital heart disease who have a diminished peak exercise capacity (18,30). For these reasons, we specifically analyzed submaximal exercise effort at each stage of the Bruce protocol. Paridon et al. (23) have also indicated that cardiopulmonary exercise testing in younger Fontan participants underestimates capacity because of the lack of motivation and submaximal exercise effort. In our current study, we observed variability in RER within our cohort even at higher stages of the Bruce protocol (range = 0.82–1.14). This may suggest that submaximal effort, rather than peak effort, may have been achieved in select participants. This variability in effort may indicate that some Fontan patients have a peripheral muscle limitation (i.e., muscle weakness) (3), secondary to any central cardiovascular or pulmonary function limitation. It may also reflect the effect of a sedentary lifestyle and lack of experience with performing higher intensity physical activity. Hypothetically, the increase in submaximal exercise performance could also be associated with an up-regulation of anaerobic metabolism, potentially in response to central limitations of exercise capacity, which, in conjunction with other related metabolic factors, contributed to increases in the submaximal performances observed. Future studies should evaluate this potential mechanism with blood lactate concentration measurements at each submaximal exercise stage.

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Physiological limitations to peak exercise capacity in children after the Fontan procedure.

Our findings further demonstrate that lower submaximal and V˙O2peak may, in part, be secondary to lower submaximal HR in a cohort of Fontan participants. Impaired HR responsiveness, the presence of a right-to-left intracardiac shunt, and increasing hypoxia with increasing exercise all contribute to the diminished peak exercise capacity observed in children after the Fontan procedure (17,23,33). Few studies have examined the submaximal exercise capacity of Fontan participants. Zajac et al. (33) reported reduced anaerobic threshold, V˙O2peak, and lower HR at peak exercise among a smaller cohort of children and adolescents after Fontan procedure (n = 14). Notably, Paridon et al. (23) reported that Fontan participants achieved about 65% of the predicted V˙O2peak and 78% of the predicted submaximal V˙O2 (at anaerobic threshold). The findings from Paridon et al. in conjunction with the results of this study suggest the intriguing possibility that, after the Fontan procedure, children are able to tolerate greater submaximal physical activities than assumed from peak exercise data.

Impaired HR responsiveness has also been reported in Fontan participants (7,21,26,33,34), likely resulting from surgical disturbances of conduction from the sinoatrial node to the atrial tissue (28) and/or blunted sympathetic nervous system response to exercise (19). Therefore, although Fontan participants may not be able to increase both HR and stroke volume to meet the physiological demands of increased cardiac output during peak exercise, our data suggest that these limitations appear not to influence submaximal exercise capacity. The underlying physiological mechanism to explain our novel submaximal exercise findings warrants future investigation.

The positive association between V˙O2peak and submaximal V˙O2 z-score was an unexpected finding in this study. Typically, a lower submaximal V˙O2 z-score reflects greater efficiency at a given submaximal stage of the Bruce protocol; thus, we hypothesized that a lower submaximal V˙O2 z-score would be associated with a higher relative V˙O2peak. A closer look at our study results indicates that most participants (76% at stage 1, 82% at stage 2, and 94% at stage 3) had submaximal V˙O2 z-scores below 0. The skewed distribution of the submaximal V˙O2 z-scores suggests that higher V˙O2peak values were attained by study participants whose submaximal z-scores were closer to 0 (i.e., similar to published values for healthy children). Ultimately, after the Fontan procedure, children may demonstrate superior performance on submaximal intensity physical activities. As a result, exercise interventions and physical activity participation in this cohort should focus on increasing submaximal physical activity to promote health benefits. As well, an increase in submaximal physical activities may help to overcome both central cardiopulmonary and peripheral muscle limitations in this unique cohort.

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Physical activity levels in children after the Fontan procedure.

Objectively measured physical activity levels were low in our Fontan participants (13), independent of both submaximal and peak exercise capacity. Recent data from the Canadian Health Measures Survey (5) demonstrate that children in the Fontan cohort typically performed less physical activity than healthy Canadian children did. Our findings support the growing body of evidence reporting low physical activity levels in several congenital heart disease cohorts (15,17,25). Congenital heart disease cohorts overwhelmingly failed to achieve the current physical activity recommendations of 60 min of daily moderate- to high-intensity exercise, which may contribute to increased long-term cardiovascular risk (2). A chronic physiological deconditioning feedback loop has been hypothesized, whereby physical inactivity leads to lower submaximal and peak exercise capacity, which, in turn, limits future physical activity participation (30). We have also previously demonstrated that physical activity restrictions are unclear between cardiologists and Fontan patient families, which may be a confounding factor leading to decreased physical activity participation (12). Clinically relevant physical activity consensus statements need to be developed for Fontan children with the understanding that they can be physiologically capable of participating in submaximal physical activities without restriction (12,20).

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The need for submaximal exercise rehabilitation in children after the Fontan procedure

Exercise training studies have shown that training programs may increase submaximal and peak exercise capacity in Fontan participants (3,27). We have previously demonstrated that a home-based physical activity intervention may be effective in improving physical activity levels and/or peak exercise capacity (11,13,14). Ultimately, the widespread implementation of submaximal exercise-based rehabilitation beginning in childhood may be both tolerable and important to prevent accelerated cardiovascular disease risk.

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Limitations.

The following limitations should be considered when interpreting these results. This study was limited to participants who survived the Fontan procedure beyond early childhood and were able to perform cardiopulmonary exercise testing. Our cohort is composed of a convenience sample because all eligible Fontan patients were contacted to participate in this study. However, study data may not be reflective of all children surviving with congenital heart disease. Participants who volunteered for the physical activity study were possibly more active than others who have undergone the Fontan procedure, although the activity levels of our study participants were similar to previous research reported for this population (17). Eight percent of study participants were taking β-blocker medication, which may blunt HR responsiveness. Therefore, it is unlikely that the reduced submaximal HRs observed were a by-product of treatment effects.

Published data on children’s exercise responses during the Bruce protocol were used for comparison with our Fontan participants, rather than simultaneously studying a healthy control cohort of children. Few large studies have published normative data on children performing a standardized exercise test (i.e., Bruce protocol). The control data used in this study were derived from a large sample of children (grouped by age and sex) and reflect children with innocent heart murmurs from whom normative values were established. Therefore, this older, referral-based cohort might be different from today’s general population of healthy Canadian children. However, these data might also be a strength in this study, given that newer published data (based on smaller samples and/or without expired gas measures) indicate that the cardiorespiratory response to exercise has declined in recent years (32). Therefore, Fontan children may have even greater submaximal exercise efficiency than we have reported. Data on maturational status were not obtained in the current study or in the study of healthy controls. Differences in maturation status of study participants and healthy controls may affect the exercise response observed. However, the current study was conducted using the specific age cut point data provided for the healthy control data. Our study was unable to compare RER, height, and mechanical efficiency (i.e., gait variability) between the Fontan cohort and healthy control group because comparison data were not published with the original research (6). The median RER in our cohort was significantly below 1.10 at all stages of the Bruce protocol (Table 1), suggesting that many study participants did not perform anaerobic exercise. The smaller stature in our Fontan cohort (median height percentile = 22%) may influence mechanical efficiency and may require a greater effort (i.e., higher submaximal HR and V˙O2) at a given stage of the Bruce protocol due primarily to decreased stride length. The Fontan cohort has a lower submaximal HR and V˙O2 at each stage despite smaller stature, which is indicative of an even greater efficiency.

Diurnal variation in exercise testing performance cannot be fully excluded. Both Fontan and healthy control (6) participant testing times were scheduled in conjunction with clinic and research visits to minimize participant inconvenience. Time of day was not significantly related to exercise performance (P < 0.83).

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CONCLUSIONS

Our study has revealed that children after the Fontan procedure exhibit lower submaximal V˙O2 and HR responses for a given workload than healthy controls during standardized graded exercise testing, demonstrating that they may be better adapted to perform submaximal physical activities. Our findings suggest that Fontan participants are physiologically able to perform submaximal physical activities, such as would be typically experienced during physical education, active peer play, and recreational sports at the same level as their healthy peers do. Targeted submaximal exercise and activity interventions may facilitate improvements in functional status in Fontan participants and prevent increased cardiovascular disease and obesity risk as these children progress into adolescence, a time when physical activity levels begin to decline. Submaximal exercise test performance may provide clinicians with an additional indicator of functional status and a viable alternative in instances where peak exercise testing is not feasible or motivation for peak performance is limited. Future studies and clinical assessments may derive greater benefit from a combined submaximal and peak exercise assessment for predicting health outcomes in congenital heart disease cohorts.

The support of participating families and contributions of Stephanie Wong, Gareth Smith, Susan Iori, Laura DeSouza, and Laura Fenwick for exercise study assessments are greatly appreciated. The Heart and Stroke Foundation of Ontario (Grant No. NA 5950) funded this research. Patricia Longmuir was supported by The Canadian Institutes of Health Research (CIHR) doctoral research award during the data collection period for this study. Laura Banks is currently funded by a CIHR doctoral research award.

The authors have no conflict of interest to declare.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

CONGENITAL HEART DISEASE; PHYSICAL ACTIVITY; BRUCE PROTOCOL; CHILDREN; FONTAN; EXERCISE CAPACITY

©2013The American College of Sports Medicine

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