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(Chest. 2003;124:2215-2219.)
© 2003 American College of Chest Physicians

Longitudinal Determinants of Peak Aerobic Performance in Children With Cystic Fibrosis*

Peter H. C. Klijn, PhD; Janjaap van der Net, PhD; Jan L. Kimpen, MD, PhD; Paul J. M. Helders, PhD and Cornelis K. van der Ent, MD, PhD

* From the Departments of Pediatric Physical Therapy (Drs. Klijn, van der Net, Kimpen, and Helders), and Pediatric Pulmonology (Dr. van der Ent), Wilhelmina Children’s Hospital, University Medical Center Utrecht, The Netherlands.

Correspondence to: Janjaap van der Net, PhD, Department of Pediatric Physical Therapy, Wilhelmina Children’s Hospital, University Medical Center, Suite KB02.056.0, PO Box 85090, 3508 AB Utrecht, the Netherlands; e-mail: J.vandernet{at}wkz.azu.nl


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Several cross-sectional studies in patients with cystic fibrosis (CF) have shown that nutritional status and lung function are important determinants of peak aerobic capacity (peak oxygen uptake [O2peak]). In order to account for individual changes, the aim of this study was to determine the longitudinal relationship of changes in nutritional status, lung function, and O2peak in children with CF.

Design and methods: Fat-free mass (FFM), lung function, and O2peak were assessed in 65 children with CF at baseline (mean ± SD age, 10.5 ± 2.9 years; mean FEV1, 92.6 ± 20.5%) and again 2 years later. FFM was calculated using skinfold thickness, and O2peak was measured using an incremental treadmill test for children < 12 years old or an incremental cycle ergometry test for children >= 12 years old. Lung function was measured before the exercise test.

Results: Over the 2-year study period, an increase was found for absolute values of FFM (6.1 kg, p < 0.001), FEV1 (229 mL, p < 0.001), and O2peak (240 mL, p < 0.001), while a decrease was found for predicted values of FEV1 (– 8.9%, p < 0.001) and O2peak (– 4.4%, p < 0.05). {Delta}O2peak over the 2-year period best correlated with {Delta}FEV1 (r = 0.619, p < 0.001) and to a lesser degree with {Delta}FFM (r = 0.506, p < 0.001). Multiple regression analysis demonstrated that {Delta}FEV1 and {Delta}FFM explained 47% of the variation of the {Delta}O2peak over the 2-year period.

Conclusions: Our results show that longitudinal changes in O2peak are associated with changes in lung function and to a lesser extent with changes in nutritional status in children with CF. Special consideration should be given to exercise training and nutritional intervention, which might improve long-term clinical outcome in children with CF.

Key Words: aerobic exercise • cystic fibrosis • nutritional status • pediatrics • pulmonary function


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Cystic fibrosis (CF) is characterized by deterioration of nutritional status and irreversible loss of lung function. Favorable prognosis and survival in this patient group have been associated with higher aerobic fitness and better nutritional status, while mortality of most patients is determined by the rate of deterioration of respiratory function.1 2 Several cross-sectional studies3 4 5 6 have shown that aerobic performance in patients with CF is associated with nutritional status. In these studies, patients with a diminished body weight have a lower aerobic capacity compared to age-matched healthy control subjects. Furthermore, CF has adverse effects on fat mass (FM) and fat-free mass (FFM). Nutritional deficiencies may lead to decreased fat stores and, as a result of protein malnutrition, may even lead to muscle wasting.4 7 Muscle mass, which is the largest constituent of FFM, is found to be a critical determinant of peak aerobic performance.8 9

Another major determinant of aerobic capacity is the ability of the lung to exchange gas.10 Cross-sectional sectional data in patients with CF show that poor lung function is associated with reduced aerobic performance.11 12

From cross-sectional studies,3 4 5 6 it can be speculated that individual changes in aerobic performance are caused by changes in lung function and nutritional status. However, with cross-sectional sectional investigations individual changes cannot be detected. Longitudinal data may enable clinicians to design interventions that are relevant and effective in improving outcome in children with CF. The longitudinal relationship between aerobic performance, lung function, and nutritional status has been described for adults with CF,13 but has not been studied previously in children with CF. The aim of this study was to determine the longitudinal relationship between changes in aerobic performance, lung function, and body composition in children with CF.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
Measurement of nutritional status, lung function, and exercise performance is part of the annual medical check-up of the Cystic Fibrosis Center of the Wilhelmina Children’s Hospital and University Medical Center at Utrecht. Patients who met the following criteria were approached for the study: age between 4 years and 18 years; stable clinical condition, ie, no need for oral or IV antibiotic treatment in 3 months prior to testing; and ability to perform the tests. One hundred sixty-three children with CF were eligible for inclusion in the study. Seventy-nine children and their parents agreed to participate. Children completed the measurements of nutritional status, lung function, and exercise performance (measurement at baseline [T1]) and again 2 years later (measurement at year 2 [T2]). The treatment regimen for the study subjects was consistent with current standards of care for CF. The study was approved by the institutional review board. Assent was obtained from each participant and informed consent from their parents.

Lung Function Testing
FVC and FEV1 were obtained from maximal expiratory flow-volume curves (Masterscreen; Jaeger; Wuerzburg, Germany). Values are expressed as the percentage of predicted values.14

Assessment of Nutritional Status
Weight and height were measured with an electronic scale (Mettler; Greifensee, Switzerland) and a stadiometer (Holtain; Crymich, UK), respectively. Left-sided biceps, triceps, and subscapular and suprailiac skinfolds were measured with an accuracy of 0.1 mm using a caliper (Holtain). The mean of three readings was recorded for each site. Total body fat percentage was estimated by the use of age- and gender-dependent equations on the relation between body fat percentage and body density.15 FFM was then calculated as the difference between body weight and FM.

Exercise Testing
The standard exercise protocol for annual check-up measurements was used. Until the age of 12 years, the children performed a treadmill test according to the Bruce protocol.16 Children >= 12 years old used an electronically braked cycle ergometer (Lode Examiner; Lode; Groningen, the Netherlands). Workload increased 15 W/min. Subjects were asked to maintain a pedaling rate at 60 revolutions per minute. During the tests, patients were encouraged to perform to the best of their ability. Both tests were continued to voluntary exhaustion.

Continuous respiratory gas analysis and volume measurements were performed breath-by-breath with a triple V valveless mouthpiece and stored in a computerized exercise system (Oxycon Champion; Jaeger; Breda, the Netherlands). Measurements taken included oxygen uptake (O2), carbon dioxide production, minute ventilation, and respiratory exchange ratio. The highest O2 achieved during the last 30 s of exercise was taken as peak O2 (O2peak).17 Heart rate was monitored by three-lead ECG (Hewlett-Packard; Amstelveen, the Netherlands) and oxygen saturation by pulse oximetry (Nellcor 200 E; Nellcor; Breda, the Netherlands). Internal gas and volume calibrations were made before each test.

Efforts were considered to be at a maximum level if subjects showed clinical signs of intense effort and were unable to maintain speed,18 and if at least one of two criteria were met: (1) cardiac frequency > 180 beats/min, or (2) maximal respiratory exchange ratio (ie, carbon dioxide production/O2) > 1.0.5 10 O2peak as a percentage of predicted (O2peak%) values were obtained from an age- and gender-matched Dutch reference population, which used the same modes of exercise.19

Data Analysis
Data are presented as mean value ± SD unless otherwise indicated. Comparisons of group characteristics between T1 and T2 were made with paired t tests. Individual differences in FFM, FEV1, and O2peak were calculated between T1 and T2 (difference between measurements at baseline and year 2 [T12]). Correlation analyses (Pearson r) and stepwise linear regression were made for {Delta}FFM, {Delta}FEV1, and {Delta}O2peak for the two measurements. Differences were considered significant if p < 0.05 (two tailed). Data were analyzed using the Statistical Package for the Social Sciences (version 9.0; SPSS; Chicago, IL).


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Eight of the 79 children were excluded from the analysis because they did not fulfill the criteria for a maximum exercise test. Six children reached the age of 12 years during the study period and therefore changed from treadmill to cycle ergometer. Several studies20 21 22 have shown higher O2peak on a treadmill compared to a cycle ergometer. Consecutive annual changes in O2peak could be the result of different exercise modes, and therefore these six children were also excluded.

Table 1 summarizes the characteristics of the study group at T1 and T2 (n = 65). The group had mild-to-moderate airflow obstruction, while their ages were normally distributed. There were no differences between the patients who collaborated in the study and the group of CF patients (n = 163) eligible for participation. Comparisons between boys and girls showed no differences in baseline characteristics or in changes of the study parameters during the study period.


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  		Table 1. Patient Characteristics at Baseline and at Repeat Testing 2 Years Later*

 
Comparisons between T1 and T2 are presented in Table 2 . Absolute values of FFM, FEV1, and O2peak increased during the 2-year period. With respect to predicted values, FEV1 as a percentage of predicted (FEV1%) and O2peak% decreased over the 2-year period. Correlations between individual changes in body composition, lung function, and aerobic performance are shown in Table 3 . The changes in O2peak correlated best with changes in FEV1 and to a lesser degree with changes in FFM. The relationship between these variables and {Delta}O2peak for T12 are demonstrated in Figure 1 .


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  		Table 2. Differences in Means for FFM, Lung Function, and Aerobic Capacity*

 

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  		Table 3. Correlation Between Changes in Body Composition, Lung Function, and Peak Aerobic Capacity Over 2-Year Period

 


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  		Figure 1. Individual {Delta}O2peak related to (top, A) {Delta}FFM (r = 0.564, p < 0.001) and (bottom, B) {Delta}FEV1 (r = 0.619, p < 0.001) over a 2-year period.

 
Changes in FEV1, FFM, height, weight, and body mass index (BMI) were entered in a step-wise regression model, with {Delta}O2peak as the dependent variable. Analysis revealed that {Delta}FEV1 (p < 0.001) explained 38% of the variation in {Delta}O2peak. {Delta}FFM (p < 0.001) was also included in the model, whereas changes in height, weight, and BMI were excluded. Together, {Delta}FEV1 and {Delta}FFM accounted for 47% of the variability in {Delta}O2peak (regression equation: {Delta}O2peak = 60.4 + 0.40·{Delta}FEV1 + 33.40·{Delta}FFM).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We longitudinally studied the effect of changes in FFM and lung function on peak aerobic capacity in children with CF. Our longitudinal data indicate that changes of peak aerobic capacity in children with CF can be ascribed, to a great extent, to changes in lung function. The additional effect of changes in FFM may explain an additional 9% of the variance of changes in O2peak.

The results of this longitudinal study are in agreement with results from cross-sectional sectional studies showing that lung function3 4 6 23 24 and nutritional status3 4 6 are important predictors of aerobic performance in patients with CF. Long-term data describing the relationship between these variables in children are not available. Moorcroft and colleagues13 reported a decline in absolute and predicted values of FEV1 in adult patients with CF over a mean period of 6.3 years; O2peak remained stable in this study, and an association between lung function and aerobic capacity was not found. In our study, the increase in absolute O2peak was mainly related to an increase in FEV1. Lung growth typically occurs in healthy subjects < 20 years old and may account for the increase in FEV1.25 In young patients with CF, the growth-related increase in absolute values of FEV1 might compensate for the disease-related loss of pulmonary function. In addition, the amount of FFM seems a potential factor in offsetting losses in pulmonary function.13 In the study of Moorcroft and coworkers,13 potential lung growth was not expected. This could explain the absence of an association between change in lung function and aerobic capacity in their study. Our patients clinically deteriorated over the 2-year period as FEV1% decreased, which is in agreement with the study results of Moorcroft and colleagues.13 However, in addition we found a concomitant decrease in age- and gender-predicted values of O2peak. Absolute values of lung function show lung growth in children with CF but may underestimate progression of lung disease.13 The clinical relevance of absolute changes in FEV1 and O2peak in young children with CF can only be judged when predicted normal values of FEV1 and O2peak are taken into account.

FFM is a critical determinant of aerobic exercise capacity in conditions of health and disease.5 9 26 Long-term decline in nutritional status with a reduction in total body weight occurs in many patients with CF. When patients with CF reach adulthood, the main impact of weight loss is likely a decrease in FFM since there usually is a preexisting reduced FM.27 FFM increased significantly during the study period, which was to be expected due to the young age of our patients. During the normal process of growth, FFM increases but different periods of FFM deposition can be discriminated.28 Tempo and timing of progression in O2peak may depend on age- and gender-related changes in FFM. Since reference values for FFM are not available, it is not clear how large the increase in muscle mass should be, based on gender and age. In order to detect clinically relevant changes in FFM of individual patients, more research is warranted to develop age- and gender-specific values for pediatric FFM proportions.

Measuring FFM by measurement of skinfolds is based on the assumption that measuring fatness reflects lean body mass as well. Besides that, it assumes that subcutaneous distribution of fat is a constant proportion of total body fat. Both might be questioned. However, significant correlations between FFM estimated with skinfold measurements as compared to water isotope dilution techniques, which is considered to be the "gold standard," have been published.29 Furthermore, de Meer and colleagues26 showed that skinfold measurements can be used to monitor FFM irrespective of clinical severity of CF.

Results of cross-sectional sectional studies30 31 in chronic airway obstruction have shown a relationship between lung disease and nutritional status, which acts by a catabolic intermediary metabolism secondary to pulmonary infection and inflammation. In general, chronic catabolic influence of inflammatory mediators (cytokines) may induce protein breakdown and inhibit muscle development in patients with CF.32 33 To our knowledge there are no studies available in which the long-term association between lung function and body composition in children with CF have been described. The relationship between {Delta}FFM and {Delta}FEV1 over our study period (r2 = 0.25) is in agreement with the cross-sectional relationship between lung function and nutritional status found for children34 (r2 = 0.06 to 0.25) and adults13 (r2 = 0.19) with CF.

Other factors, such as habitual physical activity, muscle function, and peripheral muscle strength, are also important for maintaining exercise tolerance. A limitation of our study is that we did not assess daily physical activity. It has been shown that the amount of daily physical activity is related to a diminished nutritional status,35 and that the amount of time spent in vigorous physical activities is associated with lower aerobic fitness.36 In addition, Lands and colleagues3 found that muscle function assessed with an anaerobic exercise test was a more sensitive determinant of maximal aerobic capacity than lean body mass in adults with CF. In children with CF, peripheral muscle force is related to maximal workload, even in the absence of diminished pulmonary function and nutritional status.34

Our results suggest that deterioration in lung function in children with CF might also point to a significant decrease in peak exercise capacity. The latter is associated with quality of life37 and survival.1 Special consideration should be given to exercise training, since several studies38 39 40 have shown positive effects on lung function, O2peak, and quality of life after a period of exercise training. Since FFM has an additional effect on aerobic performance, emphasis should also be given to nutritional management.13

We conclude that longitudinal changes in lung function are associated with functional changes in the aerobic capacity of children with CF. In the long-term, FFM may be important for maintaining functional exercise capacity. We speculate that regular exercise training and nutritional intervention might effectively improve long-term clinical outcome in patients with CF.


   Footnotes
 
Abbreviations: BMI = body mass index; CF = cystic fibrosis; FEV1% = FEV1 as a percentage of predicted; FFM = fat-free mass; FM = fat mass; T1 = measurement at baseline; T2 = measurement at year 2; T12 = difference between measurements at baseline and year 2; O2 = oxygen uptake; O2peak = peak oxygen uptake; O2peak% = peak oxygen uptake as a percentage of predicted

Received for publication October 11, 2002. Accepted for publication June 26, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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