Scoliosis is a 3-dimensional deformity of the spine. Thoracic scoliosis can cause structural distortion of the rib cage and influence the functioning of the cardiovascular and respiratory systems1,2. Pulmonary function testing (PFT) is the most commonly used method to measure the involvement of the respiratory system in patients with scoliosis. There has been evidence for an association between the thoracic curve and pulmonary function impairment. Newton et al.3 studied 631 patients with adolescent idiopathic scoliosis (AIS) and discovered that pulmonary function fell below threshold values once the magnitude of the main thoracic curve exceeded 70°. Johnston et al.4 found that 19% of 858 patients with AIS had restricted ventilation, especially those with a thoracic curve of >70°, a proximal thoracic curve of >30°, or structural or T5-T12 kyphosis of <10°.
Cardiopulmonary exercise testing (CPET) is a comprehensive and objective evaluation of exercise capacity5. In this testing in which exercise is increased progressively in increments, parameters of metabolic gas exchange and cardiovascular and ventilatory responses to exercise have been measured for differential diagnoses of unexplained dyspnea and exercise intolerance as well as to assess disease severity, preoperative condition, and rehabilitation6. In some scoliotic patients, ventilatory and pulmonary gas exchange impairments are inconspicuous in conventional static PFT7, but they can be revealed by CPET as the demands on pulmonary and cardiovascular function are substantially greater in intensified exercise8,9.
To date, only a few reports have dealt with the cardiopulmonary response to maximal exercise in scoliotic patients. Czaprowski et al.10 studied 70 girls with AIS and discovered lower maximum oxygen intake and output in patients with moderate scoliosis (25° to 40°). Barrios et al.11 discovered respiratory inefficiency and reduced exercise tolerance in 37 girls with AIS (20° to 45°). These results confirmed reduced exercise tolerance in patients with moderate scoliosis in comparison with normal controls.
To our knowledge, there has been no published prospective study on the correlation between radiographic parameters and the extent of the restriction in exercise capacity. The purpose of this study was to investigate whether exercise tolerance is influenced by the magnitude of thoracic curvature and kyphosis in patients with idiopathic scoliosis and to evaluate the correlation between radiographic measurements and measurements involving spirometry and cardiopulmonary function.
Materials and Methods
This prospective study was approved by the institutional review board of the Peking Union Medical College Hospital, and all of the patients (or their parents if they were <18 years old) provided informed consent. A total of 40 patients were included from January 2014 to February 2016. Patients were eligible for inclusion if they had a diagnosis of idiopathic scoliosis and had not yet received surgical intervention. Exclusion criteria were the presence of congenital heart disease or other pulmonary disease, such as asthma or bronchiectasis.
The study included 33 female subjects with a mean age of 15.5 years and 7 male subjects with a mean age of 15.9 years. All patients underwent full radiographic assessment of deformity, static PFT, ultrasonic echocardiography, and CPET using a bicycle ergometer. Echocardiography showed no cardiac abnormality or pulmonary hypertension in any subject.
Two specialists, who were not blinded to the results of the physiologic tests, independently measured the magnitude of the thoracic scoliosis and thoracic kyphosis (T5-T12) on a full-length radiograph according to the Cobb method12 and reached a consensus. The radiograph was made with the patient in a standing position; if the patient was undergoing bracing treatment, the brace was removed. The radiographic assessments were made <2 weeks before the CPET. The anthropometric and radiographic data of the patients are presented in Table I.
Specialized physicians evaluated the patients’ medical history, current medications, related symptoms, and daily physical activity before the test. The CPET involved a ramp protocol specially designed for the testing on a motor-driven bicycle ergometer (MasterScreen; Ergoline). The ergometer was calibrated at set intervals. The test protocol was established according to the ATS/ACCP (American Thoracic Society/American College of Chest Physicians) Statement on Cardiopulmonary Exercise Testing5. It started with a 3-minute warm-up at a labor of 0 W and continued in increments of 10, 15, and 20 W/min. The speed was maintained at 55 to 60 rpm during the test. The labor was reduced when the patient reached the scheduled heart rate or reported intolerable discomfort.
Thirteen parameters belonging to 4 categories were recorded5. Parameters related to metabolic gas exchange were the oxygen intake (VO2), anaerobic threshold (AT), and respiratory exchange ratio (RER). Parameters related to pulmonary gas exchange were oxygen saturation (SpO2) and the dead space/tidal volume ratio (Vd/Vt). Parameters related to ventilation were the respiratory rate (RR), ventilation capacity (VE, the ventilation volume per minute), tidal volume (Vt), and breath reserve (BR). Parameters related to the circulatory system were oxygen pulse (O2/pulse, the oxygen absorption per heartbeat), heart rate (HR), heart rate reserve (HRR), and change in systolic blood pressure (ΔSBP).
Ventilatory parameters were recorded through a respiratory valve and mouthpiece incorporating a gas analyzer, and cardiovascular parameters were monitored during the CPET by continuous electrocardiography. Blood pressure was recorded by an electrical blood pressure monitor at rest, during warm-up, immediately after maximal exercise, and 1 and 3 minutes after the start of the recovery period that followed the exercise. A category-ratio scale (Borg CR10 scale) was used to evaluate patients’ perceived exertion after the test13.
Descriptive statistics are reported as the mean and standard deviation. The 2-tailed Spearman correlation coefficient (r) was used to test bivariate relationships. The 2-tailed Student t test was used to test differences between 2 groups. A p value of 0.05 was considered significant. All analyses were performed using SPSS statistical software (version 20.0; IBM).
Thirty-three of the patients with idiopathic scoliosis who completed maximal exercise testing had primary thoracic curvature and 5 had primary lumbar curvature. Neither the oxygen intake as a percentage of the predicted value nor the oxygen intake/kg differed significantly between patients presenting with primary thoracic and primary lumbar curves (Table II). The distributions of coronal thoracic scoliosis and thoracic kyphosis are presented in Figures 1 and 2.
Of the 40 patients, 38 completed the test by exercising until exhaustion and were considered to have reached maximal physical capacity. The reasons for ceasing exercise were lower-limb weakness in 35 patients and thirst in 3. Two of the 38 patients also reported shortness of breath on exertion. The remaining 2 patients did not complete the maximal test protocol and underwent submaximal exercise. One of them coughed seriously as a result of airway secretions, and the other declined to progress to a level of maximal exertion. The PFT and CPET parameters are summarized in Table III.
In female patients, no association was found between coronal thoracic curvature and PFT results, whereas in CPET, those with a thoracic curve of ≥60° had lower blood oxygen saturation at maximal exercise (p = 0.032). Female patients with a thoracic curve of ≥50° had a higher respiratory rate (p = 0.041) and ventilation volume per minute (p = 0.046) and lower breathing reserve at maximal exercise (p = 0.038). These results indicated that exercise tolerance was not associated with coronal thoracic curvature. However, there was a possible relation between the magnitude of thoracic curvature and pulmonary function. CPET revealed potential alteration in the ventilatory pattern and pulmonary gas exchange. The test results according to curve magnitude in female patients are summarized in Table IV.
There were significant positive correlations between kyphosis at T5-12 and the PFT results, as shown by the forced expiration volume in 1 second (r = 0.456, p = 0.01), forced vital capacity (r = 0.366, p = 0.043), vital capacity (r = 0.525, p = 0.006), and total lung capacity (r = 0.388, p = 0.031). In the CPET, thoracic kyphosis was correlated with the tidal volume (r = 0.401, p = 0.025). The outcomes suggested no correlation between kyphosis and exercise tolerance, yet an obvious correlation between kyphosis and pulmonary function (Table V). Parameters related to the cardiovascular system and metabolic gas exchange were correlated with neither thoracic curvature nor kyphosis (Tables IV and V).
Patients who performed regular aerobic exercise had better performance in the CPET, as demonstrated by peak oxygen intake normalized by body weight (p < 0.001), peak oxygen intake normalized by the predicted value (p = 0.003), maximum heart rate (p = 0.020), and heart rate reserve at maximal exercise (p = 0.014). However, there was no difference in PFT results or in the parameters related to ventilation and pulmonary gas exchange (Table VI).
Scoliosis can have negative impacts on the respiratory and cardiovascular systems over time14. Progression of untreated severe thoracic scoliosis causes increasing mortality, which is related to pulmonary hypertension and right-sided heart failure15,16. Patients with idiopathic scoliosis may not show respiratory discomfort during ordinary activities, and conventional static spirometry may be unable to discover pulmonary dysfunction in asymptomatic patients. These potential impairments could be revealed by CPET11. Reduction in exercise capacity and abnormal ventilatory patterns have been found in patients even with asymptomatic mild to moderate scoliosis10,11.
Overall exercise tolerance did not appear to be correlated with the magnitude of the thoracic curve, as shown by the crucial parameter, oxygen intake17, either expressed as the percentage of the predicted value (VO2%pred) or normalized by body weight (VO2/kg). However, lower blood oxygen saturation at maximal exercise was demonstrated in patients with thoracic scoliosis of ≥60°, and lower tidal volume and breathing reserve were demonstrated in patients with thoracic scoliosis of ≥50°. It was also revealed that thoracic hypokyphosis or lordosis was correlated with the decline of pulmonary function. These results suggested possible deleterious effects on ventilation and gas exchange during maximal exercise in patients with larger thoracic curves.
This is in accordance with some previous research, which revealed that scoliotic deformity had a negative impact on the respiratory system4,9,18-20. In healthy subjects, ventilation and gas exchange are usually ample to provide oxygen delivery up to maximal exercise, and it is the limitations of the cardiovascular system that play a major role in exercise intolerance21. In the present study, 35 (92%) of 38 patients reported only leg weakness at peak exertion, indicating that they had not yet reached the level at which the circulatory system limits a further increase. However, for patients with ventilatory dysfunction, it is not the case. In strenuous exercise, ventilation parameters change in a certain pattern22. Tidal volume increases as the ventilation volume increases. The absolute value of tidal volume in patients with scoliosis is less than normal at any given ventilation volume per minute. Therefore, the body has to utilize a greater proportion of the ventilation capacity in tidal breathing to compensate. When tidal volume reaches the maximal point, the body promotes further increases in ventilation by a faster respiration rate. This increase in the respiration rate happens earlier in scoliotic patients, as the redundant tidal volume is limited18. Moreover, ventilation capacity is closer to the maximum ventilatory volume, as shown by reduction of the breathing reserve, in scoliotic patients. When the body approaches the anaerobic threshold, lactic acid starts to accumulate, resulting in a sympathetic reaction and causing vasoconstriction and body fatigue23. With continued increase in the amount of exercise, ventilation or pulmonary gas exchange cannot meet the body’s need, as demonstrated by a significant decline of blood oxygen saturation during exercise.
Previous research has revealed that scoliosis results in restrictions on the size and the shape of the chest and limits movement of the rib cage through distortion of the spine, diminution of normal thoracic kyphosis, and deformity of the ribs20,24-26. In addition, Mohammadi et al.19, Kearon et al.25, and Martínez-Llorens et al.27 discovered a relationship between the resulting ventilatory disorders in scoliotic patients and weakness of respiratory muscles. The restricted breath movements result in hypoventilation of the pulmonary alveoli. Static PFTs revealed that the severity of thoracic scoliosis may negatively affect total lung volume and forced vital capacity4,20,28. There is also evidence of a lower ratio of forced expiratory volume in 1 second to forced vital capacity in patients with scoliosis, indicating the existence of obstructive ventilation dysfunction29,30. These ventilatory disorders lead to hypoxia, as demonstrated by oxygen desaturation in arterial blood31,32. Inefficient gas exchange secondary to ventilatory dead space increase and ventilation perfusion maldistribution was also reported33.
Our finding that patients with a thoracic curve of ≥50° had higher ventilation volume per minute normalized by the predicted value (p = 0.046) appears counterintuitive. No such correlation was found between the magnitude of thoracic curvature and ventilation volume per minute in the research of Kearon et al.25, and Barrios et al.11 came to the opposite conclusion. Lack of physical activity, loss of lean muscle mass, or muscle deconditioning may be responsible. We can see from the scatterplot in Figure 3 that 2 patients with a thoracic curve of ≥70° had relatively good ventilation volume per minute as a percentage of the predicted value. The routine question regarding daily physical activity before the CPET revealed that 1 of these patients, who had a thoracic curve of 76°, was a 15-year-old student who had engaged in regular swimming, 3 to 4 km once per week for 7 years. The other patient, who had a thoracic curve of 72°, was a 35-year-old kindergarten teacher whose routine work included much manual labor. With these 2 cases excluded, no relation was found between the severity of curvature and ventilation volume per minute. Furthermore, we compared the PFT and CPET parameters of patients with and without regular exercise (Table VI). Significant differences were found in oxygen intake, maximum heart rate, and heart rate reserve at maximal exercise, which are all indices reflecting patients’ exercise tolerance. These results indicated that regular aerobic sport activity may be associated with better exercise capacity. In fact, peripheral muscle dysfunction, which leads to leg fatigue, is also 1 of the factors influencing CPET results34. A study of the effect of a physical training program by Bjure et al.35 revealed better heart rate response and increased ventilation per minute that were proportional to the improvement in oxygen intake in female patients with idiopathic scoliosis. Nevertheless, there were no changes in static pulmonary function over the same period. Similarly, Bas et al.36 reported better power output, oxygen intake, and maximum heart rate with unchanged forced vital capacity and forced expiratory volume in 1 second after 6 weeks of aerobic training in adolescent patients with moderate idiopathic scoliosis. Therefore, although physical training may not be able to change pulmonary pathology, it is still recommended in patients with idiopathic scoliosis for maintaining cardiovascular and peripheral muscle conditioning18,25,37.
Regarding parameters related to the cardiovascular system, oxygen pulse, heart rate reserve, and change in systolic blood pressure were not significantly correlated with thoracic curvature or kyphosis, suggesting that the cardiovascular system may be less affected than the respiratory system in patients with idiopathic scoliosis. Some previous research has indicated that untreated scoliosis may increase mortality due to pulmonary hypertension and right-sided heart failure15. In the present study, ultrasonic echocardiography confirmed the absence of pulmonary hypertension in all of the subjects. However, only 2 (6%) of 33 female patients in the study had a thoracic curvature of ≥70°. Further study is required to uncover the influence that scoliosis may have on the cardiovascular system.
The present study had two main limitations. The size of the sample was small, with an especially small number of male patients. Also, the precise location and magnitude of thoracic curves were not investigated in detail and may have had an impact on cardiopulmonary function.
In conclusion, overall exercise tolerance did not appear to be correlated with the magnitude of the thoracic curve and kyphosis, but some of the parameters involving ventilatory function and pulmonary gas exchange worsened as thoracic curvature increased or kyphosis decreased. Exercise capacity was better in patients who performed regular aerobic exercise, and physical activity is recommended for patients with idiopathic scoliosis.
Investigation performed at the Departments of Orthopedics and Respiratory Medicine, Peking Union Medical College Hospital, Peking Union Medical College, Chinese Academy of Medical Science, Beijing, People’s Republic of China
Disclosure: No external funding was received for this study. The Disclosure of Potential Conflicts of Interest forms are provided with the online version of the article.
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