Introduction

Spirometry examination is a commonly used test to measure the volumes and flows as indicators of the respiratory function and is used to diagnose lung diseases and monitor lung status [1]. Assessing the pulmonary status of patients with idiopathic scoliosis is a part of the preparation for surgical correction of spine deformity.
Lung restriction is a common respiratory pattern observed in adolescents with idiopathic scoliosis. The origin of decreased lung volumes in idiopathic scoliosis is multifactorial. Several parameters have been identified as related to respiratory impairment, including: the Cobb angle [2-6], the loss of thoracic kyphosis [2], the number of vertebrae involved in the curve [2,4,7], spinal rotation, the location of the curve [8] and chest mobility [9].
Airway obstruction is rarely observed in patients with idiopathic scoliosis [10]. However, McPhail et al. [11] concluded that the prevalence of obstructive disease was 39% of patients scheduled for surgical spine correction of thoracic scoliosis. Mechanical airway obstruction reduced expiratory flows and increased airway resistance may occur as a consequence of thorax deformity. It is supposed that chest rotation can produce displacement or rotation of the intrathoracic and/or mainstem bronchi or compression of a mainstem bronchus against vertebra and mediastinal structures [12,13]. A reversibility test can help to determine whether the airway obstruction is caused by an undiagnosed lung disorder.
The aim of the study was to analyse the preoperative results of a spirometry examination in adolescent girls with severe idiopathic scoliosis.

Materials and methods

Study population
Ninety-two consecutive adolescent girls, aged 14.0 ±1.9 years, range 10-18, who were admitted for surgical treatment of idiopathic scoliosis, were enrolled. All patients met the inclusion criteria: no congenital, neuromuscular or syndromic spine deformity, no previous spine surgery and no pulmonary disorders diagnosed.

Radiological evaluation
Thoracic and lumbar/thoracolumbar Cobb angles were measured on anteroposterior standing radiographs [14]. The Lenke curve type was applied [15]. The Risser sign was used to assess the patients’ bone maturity [16].

Corrected body height calculation
The corrected body height was calculated as a sum of the measured body height and the loss of body height due to spine deformity. Body height was measured in a standing position on a stadiometer by the first author. The measurement was performed prior to the spirometry examination in the morning hours.
Stokes’ formula was used to calculate the loss of body height. In the case of a single curve (Lenke 1 or Lenke 5), the following formula was used: 1.55 – 0.0471Cobb + 0.009Cobb2, while for the double curves (Lenke 2 or Lenke 3), the following formula was applied: 1.0 + 0.066Cobb + 0.0084Cobb2 [17].

Calculation of the predicted pulmonary
parameter values
The predicted values of the FVC, FEV1 and FEV1/FVC, the lower limit of normal (LLN), the upper limit of normal (ULN), z-scores, and percentages of the predicted values of pulmonary parameters were calculated according to the Global Lung Function Initiative (GLI 2012) reference values [18]. The predicted values of pulmonary parameters were calculated independently for the measured and corrected body height.

Pulmonary testing
A spirometry examination was performed in a sitting position using the LungTest LT 250 spirometer (MES, Kraków, Poland). All examinations were done by the first author who is certified for spirometry examination. Prior to pulmonary testing, the technique of the spirometry examination was explained to the patient. A nose clip was used to prevent partial air exhalation through the nose [19]. To prevent air from escaping, the patient was asked to tighten the seal around the mouthpiece and place the tongue below the mouthpiece to avoid blocking airflow. All patients performed a minimum of 3 maneuvers and up to a maximum of 8 maneuvers of maximal inhalation followed by maximal exhalation until plateau was reached. Enthusiastic coaching was provided to encourage the patient to make a maximum effort. Phrases such as “blowing 100 candles on a cake” were helpful to forcefully exhale until plateau was reached [19, 20]. If needed, after rest time, the patient repeated the examination until acceptable repeatability was achieved, defined as follows: the difference between the largest and the next largest FVC is ≤0.150 L, and the difference between the largest and next largest FEV1 is ≤0.150 L [18]. The best single value of FVC and FEV1 was used for analysis [4, 19, 21-26]. In the case spirometry results indicated an obstruction pattern (FEV1/FVC < LLN), a reversibility test of airway obstruction was performed [1].

Intraclass Correlation Coeficient (ICC)
To determine repeatability (intraobserver agreement), 32 subjects underwent spirometry examinations twice within a one to three-day interval. The absolute value of FEV1 and FVC were analyzed. The Intraclass Correlation Coefficient (ICC), The Confidence Interval (C.I.) and the Standard Error of Measurement (SEM) were calculated.

Statistical analysis
The Shapiro-Wilk test was used to analyze data distribution. Mean, standard deviation and range were calculated. The significance of differences between pulmonary parameters: predicted values, LLN, ULN, the z-score, and the percentage of predicted FVC, FEV1, and FEV1/FVC, was determined by Student t-test. The Spearman correlation coefficient was used to calculate the correlation between the parameters: Cobb angle versus absolute values, pulmonary parameters, and loss of body height versus pulmonary parameters. Spirometry examination repeatability was determined for FVC and FEV1 using the Intraclass correlation (ICC), the Confidence Interval (CI), the Standard Error of Measurement (SEM). Analysis was performed with Statistica Software (TIBCO Software Inc., Palo Alto, the USA) and IBM SPSS Statistics 18 (Chicago, Illinois, the USA). The significance level was set at p = 0.05.
Results

Radiological analysis
The thoracic and lumbar/thoracolumbar Cobb angle values are presented in Table 1. The median of the Risser sign was 3.
The Lenke 1 group consisted of 40 patients, the Lenke 2 group of 10 patients, the Lenke 3 group of 31 patients, and the Lenke 5 group of 11 patients.

Corrected body height calculation
The mean body height loss was 5.4 cm ±2.9 (2.0-13.2). The corrected body height was significantly higher than the measured body height (166.3 cm vs. 160.5 cm, p < 0.01).

Predicted values of the pulmonary parameters
The predicted values, upper limit of normal (ULN) and lower limit of normal (LLN) for FVC and FEV1 were significantly higher when calculated based on the corrected body height versus the measured body height. The FEV1/FVC values, on the other hand, were significantly lower when calculated according to the corrected body height, Table 2.

Pulmonary parameters obtained
during the spirometry examination
The absolute values of FVC, FEV1, and FEV1\FVC, as well as z-score values and the percentage of predicted values of pulmonary parameters are presented in Table 3.
When measured body height was used, z-score values of the FVC and FEV1 were within normal range (-1.64 ÷ 1.64), however when corrected body height was used,
z-score values decreased and revealed to be below normal, the expected range for both parameters (FVC -1.76 vs. -1.25; FEV1 -1.86 vs. -1.41). Also, the percentages of the predicted value of the FVC and FEV1 decreased when the corrected body height was used instead of the measured one (FVC 79.54% vs. 85.47%; FEV1 78.35% vs. 83.73%). In contrast, the FEV1\FVC z-score value revealed within the expected range, for both the measured and corrected body height. An increase of the parameter’s value was observed when corrected body height was used (-0.35 vs. -0.40). When percentages of the predicted value of FEV1\FVC were obtained for the corrected body height, values were higher comparing to the ones obtained based on the measured body height (96.87% vs. 96.52%), as presented in Table 3.
When the measured body height was used, in 56.5% of patients, pulmonary parameters revealed to be within the normal range; in 32.6% of patients, values of the pulmonary parameters suggested restriction, and in 10.9%, results pointed to the obstruction pattern. However, when pulmonary reference values were recalculated using the corrected body height, the number of patients presenting pulmonary parameter values within the normal range decreased to 48.9%, the number of patients with a possible restriction pattern increased to 42.4%. The number of patients presenting an airway obstruction pattern decreased to 8.7% when values were calculated based on the corrected body height, Fig. 1.
Also, in patients with a possible restriction pattern, using the corrected body height instead of the measured body height impacts severity classification. When the pulmonary parameters were calculated according to the corrected body height, the mild restrictive pattern decreased from 53.3% to 41.0%, while the moderate increased from 20.0% to 25.6%, and severely moderate restriction increased from 20.0% to 28.2%, as shown in Fig. 2.
Out of 92, 10 patients revealed an airway obstruction pattern when calculated for the measured body height:
5 patients presented mild, 2 patients moderate and 3 patients moderately severe airway obstruction. When using the corrected body height, 8 patients presented an airway obstruction pattern: 2 patients mild, 2 patients moderate, 3 patients moderately severe, and 1 patient severe airway obstruction. An example of a patient is presented in Appendix 1.
A significant negative correlation between the absolute FVC and the FEV1 values versus the thoracic Cobb angle (r = -0.2673, p = 0.016; r = -0.3087, p = 0.005,
respectively) was observed. No such correlation was revealed for the lumbar spine (FVC r = -0.3560, p = 0.490; FEV1 r = -0.3701, p = 0.400). Also, with increasing body height loss, the absolute values of both pulmonary parameters (FVC and FEV1) decreased, as presented in Figures 3 and 4.
The Intraclass Correlation Coefficient
The repeatability of pulmonary parameter measurements FEV1 and FVC was excellent. Values of ICC, CI and SEM are presented in Table 4.
Discussion

A spirometry examination performed before the surgical treatment of idiopathic scoliosis can detect pulmonary impairment even if it is not clinically evident [10]. Body height is one of the variables considered when calculating the predicted values, LLN and ULN of pulmonary parameters according to GLI 2012 reference values [18]. In patients with severe idiopathic scoliosis, the measured body height is decreased as a consequence of spine deformation. The loss of body height was calculated based on the Stokes formula, which analysed Cobb angles, the spinal length, and the spinal height on 387 standard standing radiographs of patients with juvenile or adolescent scoliosis (182 single curves, 205 double curves) aged 9-20 years old. For patients with a single curve and a double curve, separate formulas were proposed to calculate body height loss [17]. Tyrakowski et al. [27] concluded that none of the four compared methods- Bjure, Kono, Ylikowski, Stokes- could be recommended as most valid. However, according to Gardner et al. [28], who compared 5 methods- Bjure, Kono, Ylikowski, Stokes, and Hwang, Stokes’s formula is one of the two most valid methods of calculating the loss of height. A significant difference was found between the measured versus the corrected body height (p < 0.01), the results are in line with our earlier findings [23-25]. Also, the use of corrected body height instead of the measured one may affect the interpretation of spirometry results, as well as change the classification of pulmonary impairment severity [23,25]. Both the z-score value and the percentage of the predicted FEV1 and FVC value revealed significantly lower results when calculated based on the corrected body height comparing to the meaured body height
(p < 0.01). Furthermore, in our study, in 30 out of 92 patients (32.6%), spirometry results suggested a restrictive pattern when the measured body height was used, while this number increased to 39 patients (42.4%), if the corrected body height was taken for reference value calculations. Although a spirometry examination alone is not the gold standard to diagnose restriction that is often observed in patients with idiopathic scoliosis, our study helped to assess the pulmonary status of patients and determine if further pulmonary investigation is needed, or identify the patients who may require more intensive rehabilitation before or after surgery.
On the other hand, spirometry is recommended as
a tool for assessing the pattern of airway obstruction [29]. Out of 92 patients, 10 patients (10.9%) were diagnosed with airway obstruction when the measured body height was used versus 8 patients (8.7%) when the corrected body height was used. Farell and Garridos’ [30] preoperatively analysed the morphology of large airways in patients with right thoracic idiopathic scoliosis and demonstrated that right-sided airways become narrowed as a result of loss of thoracic kyphosis. Furthermore, the authors concluded that FEV1/FVC correlates negatively with airway narrowing, suggesting that obstruction contributes to lung function impairment in patients with thoracic scoliosis and hypokyphosis. Borowitz et al. [13] reported the flattening of the initial portion of the expiratory loop, suggesting the obstruction of a large airway, which improved after the surgical correction of scoliosis. According to Boyer et al. [31] lower airway obstruction may develop as spine deformity increases and is often reversible with a bronchodilator. The airway reversibility test may help to assess whether aiway obstruction may be a consequence of spinal deformity. It may also help to assess if a patient needs further investigation of the cause of the airway obstruction. However, in the presented case of a 16-year-old girl, the test results were negative suggesting that airway obstruction might be secondary to spine deformity [32].
Weinstein et al. [33] suggested that pulmonary impairment may occur in patients with idiopathic scoliosis presenting a thoracic Cobb angle of more than 100-120°. However, studies showed that pulmonary impairment may be observed in patients with smaller curves. Johnston et al. [6] concluded that in untreated adult patients with idiopathic scoliosis, a thoracic curve magnitude greater than 40° correlated negatively with the FVC value (p < 0.008). Also, our study revealed a negative correlation between thoracic curve magnitude and pulmonary parameters (FVC, FEV1). These observations are consistent with other authors [4-7]. Moreover, our study showed a negative correlation between the loss of body height versus the FVC or FEV1 absolute value (r = -0.2441, p = 0.019; r = -0.2489,
p = 0.017, respectively).
As previous studies showed, preschool children can perform reproducible and technically acceptable spirometry maneuvers [34-36]. However, prior to the spirometry examination, it is of critical importance to explain the procedure using age appriopriate language and describe the technique step by step so that the patient understands and cooperates [19]. However, no difference was described in FEV1 and FVC values in children with and without a nose clip [37]. Spirometry can be conducted in both a sitting and a standing position. Due to safety reasons and to avoid falling down as a syncope result, we decided to use a straightened-up sitting position, both feet on the ground [19]. Patients who perform spirometry examinations may need several attempts to learn the proper technique and achieve acceptable repeatability. Collaboration and commitment of both the patient and the technician are needed to achieve credible spirometry results.

Conclusion

Pulmonary impairment can occur in adolescent patients with severe thoracic idiopathic scoliosis. In patients with pulmonary impairment, more cases present a restrictive pattern, however, airway obstruction is also observed. The correction for body height loss may affect the predicted values of pulmonary parameters and the interpretation of spirometry examination results.

Appendix 1
Due to obstruction pattern, the patient performed airway obstruction reversibility test. The FEV1 and FVC improvement after bronchodilator did not reach the threshold of 200 ml or 12% change. Furthermore, the FEV1/FVC value remains abnormal suggesting that the bronchodilatation test is negative with irreversible airway obstruction [31].
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