The In uence of Early Thoracic Fusion on the Pulmonary Function of Patients with Idiopathic Scoliosis in the Early Period of the Second Growth Peak with Different Risser Signs


 Background: Previous reports confirmed early spinal fusion may compromise pulmonary function and thoracic development in skeletal immature patients with scoliosis. However, the different effects in patients with various Risser signs remain unknown. This study aimed to compare the influence of early thoracic fusion on pulmonary function and thoracic growth in patients with idiopathic scoliosis (IS) with closed triangular cartilage (TRC) and different Risser signs. Methods: Thirty-six patients with IS and a closed TRC were retrospectively selected and divided into the low Risser (LR, Risser sign ≤2, 22 patients) and high Risser (HR, 2<Risser sign≤4, 14 patients) groups. Patient age, Risser sign, main Cobb angle, thoracic kyphosis, and fusion levels were recorded. Perioperative and follow-up pulmonary function and thoracic diameters were compared between both groups. Results: There were no differences in patients’ general characteristics between two groups. The preoperative FEV1 and FVC were 2.06±0.43 L and 2.50±0.49 L, respectively, in the LR group, and 2.31±0.49 L (p=0.067) and 2.74±0.56 L (p=0.122), respectively, in the HR group. While these values significantly increased postoperatively, to 2.62±0.46 L (p<0.000) and 3.09±0.69 L (p<0.000), in the LR group, they remained unchanged in the HR group [2.53±0.56 L (p=0.093) and 2.70±0.98 L (p=0.386), respectively]. The FEV1/FVC in both groups was >80% before and after surgery. The T1-T12 and anteroposterior thoracic diameter significantly increased after surgery in both groups, while the maximum inner chest diameter only increased in the LR group at the final follow-up. However, there were no significant differences in respiratory function and thoracic data between both groups. Conclusion: For patients with IS, early fusion didn’t deteriorate pulmonary function or thoracic development in TRC-closed patients whose Risser sign was ≤2 compared with those with a Risser sign >2.

signi cantly increased postoperatively, to 2.62±0.46 L (p<0.000) and 3.09±0.69 L (p<0.000), in the LR group, they remained unchanged in the HR group [2.53±0.56 L (p=0.093) and 2.70±0.98 L (p=0.386), respectively]. The FEV1/FVC in both groups was >80% before and after surgery. The T1-T12 and anteroposterior thoracic diameter signi cantly increased after surgery in both groups, while the maximum inner chest diameter only increased in the LR group at the nal follow-up. However, there were no signi cant differences in respiratory function and thoracic data between both groups.
Conclusion: For patients with IS, early fusion didn't deteriorate pulmonary function or thoracic development in TRC-closed patients whose Risser sign was ≤2 compared with those with a Risser sign >2.

Background
Scoliosis is de ned as the lateral curvature of the spine ≥ 10° in the coronal plane. It is a threedimensional spinal deformity that usually presents as distortion of the body, thorax, and ribs, thus restricting pulmonary system development [1].
As the most common type of structural scoliosis, the incidence of idiopathic scoliosis (IS) is approximately 1.5% among all teens, while infants with infantile scoliosis represent nearly 4% of patients with IS [2]. Children with progressive curves at a young age are at risk of severe pulmonary issues, attributable to spinal deformity and surgical management [3]. Thus, IS treatment in growing children is challenging since potential harm caused by scoliosis correlates closely with skeletal maturity.
Previous studies found that early spinal fusion may impair pulmonary function and inhibit thoracic growth in skeletally immature patients with scoliosis; however, these studies mainly focused on early onset scoliosis (EOS), particularly congenital scoliosis (CS) [4][5][6][7][8], wherein pre-existing factors, including rib malformations, respiratory muscular disorders, or syndrome-related complications in CS and other forms of EOS may play a role in respiratory function. Meanwhile, as remaining growth is a determining factor for the worsening of IS, evaluating the growth potential of young patients before therapeutic selection is vital. This is usually conducted based on Risser signs and the condition of the triangular cartilage (TRC) [9,10].
To our knowledge, the effects of early thoracic fusion in patients with IS with different skeletal maturities remain unclear, especially after TRC closure, which occurs in the early period of the second growth peak.
This study aimed to analyse and compare the long-term effects of early thoracic fusion on pulmonary function and thoracic growth in patients with IS with a closed TRC and different Risser signs, to provide potential references for interventions in young patients with IS.

Methods
We retrospectively collected the pre-and postoperative data of patients diagnosed with IS who underwent posterior thoracic fusion between September 2015 and September 2017 in the Department of Spinal Surgery, Peking Union Medical College Hospital (PUMCH). Medical records were reviewed for age at surgery, sex, PUMC classi cation of scoliosis, extent of thoracic fusion, and maximum follow-up years. Radiographs were also reviewed for preoperative Risser signs, main Cobb angles, and thoracic kyphosis before and after surgery and at follow-up. Patients selected in the study were grouped into the LR group (Risser ≤ 2) and the HR group (2 < Risser ≤ 4) based on their preoperative Risser signs. All patients were between 9 and 12 years old with closed TRC at the time of admission, diagnosed with IS, and underwent one-time posterior fusion surgery related to the thoracic spine. A minimum 2-year postoperative follow-up was required for each patient. All patients had a Risser sign of 5 at the nal follow-up. Patients with incomplete medical records, who were unable to complete the follow-up, had primary cardio-pulmonary disease such as congenital heart defect, diaphragmatic hernias, or had severe postoperative complications such as pulmonary infection or spinal injury were excluded. Patients with rib abnormalities, such as rib fusions or absent ribs, were also excluded.
Standard pulmonary function tests (PFTs) were recalled, and forced expiratory volume in 1 s (FEV1), forced vital capacity (FVC), and FEV1/FVC were recorded both before surgery and at follow-up. Total lung capacity (TLC) and vital capacity (VC) were recorded at follow-up. All PFTs included the predicted and measured values. The predicted value indicates the normal ventilation parameters of the population, consistent with the sex, age, body weight, and height of the patient.
Spinal height from the 1st thoracic vertebrae (T1) to the 12th thoracic vertebrae (T12) (the straight-line distance between the midpoint of the upper endplate at T1 and the midpoint of the lower endplate at T12), maximum inner chest diameter (MICD, the maximum linear distance between the medial margin of the ribs on the coronal plane), Campbell's space available for lung ratio (SAL, the ratio of the distance between the concave side and the convex side of the lateral curvature from the rst costal apex to the highest point of the diaphragm), anterior and posterior thoracic diameter (APTD, the distance between the anterior chest wall and the anterior border of the vertebral body through the highest point of the diaphragm on the sagittal plane), and thoracic sagittal longitudinal diameter (TSLD, the distance between the highest point of the diaphragm and the highest point of the chest on the sagittal plane) were measured (Fig. 1). Two experienced surgeons who were blinded to the outcomes performed all measurements. The mean values were used for the analysis.

Statistical Analysis
The data were analysed using SPSS (IBM Corp. Released 2013. IBM SPSS Statistics for Windows, version 19.0. Armonk, NY: IBM Corp.) and are expressed as the mean ± SD. For the independent samples, the Mann-Whitney U test was used to compare data between each group, while the nonparametric test of related samples (Wilcoxon) was used to compare the preoperative, postoperative, and follow-up data in each group. Differences were considered statistically signi cant at p < 0.05.

General data
Twenty-two patients met the criteria for the LR group, with a mean age of 11.3 ± 0.7 years old and followup time of 3.5 ± 1.5 years. The HR group included fourteen patients, with a mean age of 11.8 ± 0.4 years and follow-up time of 3.5 ± 1.4 years. Both groups had similar thoracic fusion proportions. The mean preoperative main Cobb angle was 46.0 ± 10.1°, with a thoracic kyphosis of 21.1 ± 13.6° in the LR group, which were similar to those of the HR group [46.9 ± 7.4° (p = 0.275) and 21.5 ± 10.3° (p = 0.670), respectively]. On nal review, the Cobb angle and thoracic kyphosis decreased to 8.1 ± 6.6° and 17.7 ± 9.7°, respectively, in the LR group, and 9.5 ± 6.6° and 18.2 ± 4.7°, respectively, in the HR group. There was no signi cant difference between both groups (Table 1).  (Fig. 3.).
At follow-up, the predicted TLC and VC were 4.79 ± 0.80 and 3.61 ± 0.53 L, respectively, in the LR group, which were signi cantly higher than the measured values [3.90 ± 0.99 (p = 0.039) and 3.

Values Compared between Groups
None of the PFTs signi cantly differed between both groups in the preoperative and follow-up tests. Thoracic growth and development
The preoperative APTD were 143.7 ± 18.6 and 147.7 ± 20.0 mm in the LR and HR groups, respectively, The preoperative SAL was 92.5 ± 3.1% in the LR and 92.7 ± 3.5% in the HR group, while the TSLD was 74.9 ± 14.7 mm in the LR and 77.7 ± 15.6 mm in the HR group. The SAL and TSLD were similar to postoperative and follow-up results in both groups (Table 2).

Comparison of Diameters between Groups
None of the thoracic diameters showed any signi cant difference between the groups on preoperative, postoperative, or follow-up tests.

Discussion
This study retrospectively included patients with IS and different Risser signs who underwent thoracic fusion at our hospital after TRC closure. These patients had a similar preoperative age, main Cobb angle, thoracic kyphosis, fusion segments, and follow-up period. Upon comparing the preoperative and followup pulmonary function and thoracic growth diameters in the LR and HR groups, we found that: 1. All patients demonstrated compromised preoperative FEV1 and FVC compared to the predicted values. 2.
After early thoracic fusion, although the FEV1 and FVC were still lower than the predicted values in both groups, they increased signi cantly in the LR group compared with the preoperative results. 3. The FEV1/FVC in both groups was > 80% regardless of preoperative or follow-up tests, which did not change after spinal fusion. 4. The T1-T12 height and APTD in both groups increased signi cantly after thoracic fusion. However, compared with the postoperative results, the follow-up T1-T12 height showed no increase, while the APTD increased signi cantly. 5. In the LR group, the MICD also increased at the nal follow-up. 6. All PFTs and thoracic parameters were similar between both groups on preoperative, postoperative, and follow-up measurements.
The clinical strategies for IS in very young children are extremely challenging. For mild to moderate scoliosis, conservative treatments such as physiotherapy, casting, and bracing are mostly recommended for juvenile patients, which can slow down the progression of the deformity until spine fusion can be performed [11,12]. However, spinal deformity in this group is often relentlessly progressive; thus, in addition to casting and bracing, spinal fusion with instrumentation is usually indicated for patients with progressive scoliosis > 50° [13][14][15], as well as in primary thoracic curves > 30° at the beginning of puberty if patients show progress during the rst year of pubertal growth [16]. This treatment is undertaken with the belief that a spine that is "short and straight" would be better in the long term than a spine with further curve progression that is "longer but crooked" [17,18]. Newer concepts a rm the importance of maintaining spine growth and minimize curvature simultaneously; thus, "growth-friendly" systems are promoted [19][20][21].
The in uence of early spinal fusion in young patients possibly involves three aspects: spinal deformity, thoracic growth, and pulmonary function. Previous studies have shown that deformity progression in CS may not be well-controlled by early fusion because of the high revision surgery rate, pseudarthroses, and adding-on phenomenon at the cephalad or caudal ends of the initial fusion [4,6,22]. However, in our study, both groups demonstrated similar preoperative Cobb angles and kyphosis after undergoing similar extension of thoracic fusion, and the follow-up assessment demonstrated similar signi cantly reduced main Cobb angle and kyphosis, indicating that both groups had well-controlled deformities.
In thoracic growth, IS itself can have negative effects on the growing spine as asymmetrical forces act on the growth plates of the vertebral column [12]. When managing severe and very severe scoliosis in young patients, posterior instrumented fusion is a rational choice because correction of the deformity compensates for the overall loss of spinal height [12]. In 2008, Bowen et al. found that patients with CS who had fusions before the age of 5 years demonstrated a 0.48-cm increase per year in the T1-T12 height, which was nearly half of those who did not [5]. For normal growth, the length from T1-T12 averages at 18 cm at 5 years of age, 22 cm at 10 years of age, and 26.5-28 cm in adults, based on the studies by Dimeglio et al. [23,24]. This is consistent with our results, in which the preoperative T1-T12 was approximately 23.5 ± 1.6 and 24.4 ± 1.6 cm in the LR and HR groups, respectively. At the nal followup, although lower than adult levels were reported by Dimeglio, these levels increased signi cantly to 25.8 ± 1.4 and 25.9 ± 1.4 cm, and the annual growth rate of T1-T12 were 0.64 cm and 0.41 cm for the LR and HR groups, respectively. In contrast, in both the LR and HR groups, the T1-T12 height and APTD increased signi cantly after thoracic fusion. Compared with the postoperative results, the follow-up T1-T12 height in both groups showed no increase, while APTD still increased signi cantly. This indicated that after TRC closure, patients who had thoracic fusion may remain at a steady T1-T12 height, but the anteroposterior diameter of the thoracic cage may continue to increase. More importantly, compared with the preoperative value, postoperative MICD in the LR group remained unchanged, but the follow-up MICD increased signi cantly. This revealed that patients with low Risser signs may maintain their growth potential in the thoracic width, while those with high Risser signs may not.
A progressive spinal deformity leads to thoracic cage distortion, and more importantly, compromise lung growth [12]. For a healthy child, the greatest increase in the number of alveoli occurs in the rst 2 years of life [25,26], and the multiplication of alveoli is typically completed by the age of 8 years [6]. Further, there are signi cant barriers to the acquisition of PFTs in young patients, including a short attention span and di culty in cooperating [27,28]. Thus, we included patients over 9 years of age to avoid the in uence of different bases of lung growth.
Previous studies have demonstrated the frustrating effects of early spinal fusion on pulmonary function, mainly in patients with EOS. Goldberg et al. reported that in 11 patients fused before 10 years of age, the FEV1 and FVC both averaged to 41% of normal values on the nal follow-up when patients reached at least 15 years of age, while these increased to 79% and 68%, respectively, in those who were fused at an older age. Furthermore, those whose scoliosis resolved or were stabilized by nonoperative means demonstrated normal levels of FEV1 and FVC (98.7% and 96.6% of normal) [7]. In another study by Karol et al., 28 patients with a mean age of 3.3 years underwent spinal fusion, after an average 11-year followup. They found that the average FVC was 57.8% and FEV1 was 54.7% of normal values. Further, in 12 of the 28 patients, the FVC was < 50% of the normal value. They concluded that fusion of the proximal aspect of the spine (T1 or T2) and more than four segments were associated with diminished pulmonary function [4]. Vitale et al. compared the difference between early thoracic fusion and thoracolumbar fusion in infantile patients with congenital scoliosis. They found that the predicted FVC averaged at 64.2% and 88.5% for patients with thoracic and lumbar fusions, respectively, while the thoracic fusion group also showed lower scores on quality of life [8].
These studies included patients with various Cobb angles and fusion segments, and the types of scoliosis as well as the associated abnormalities were also inconsistent among groups, especially in patients with CS. In our study, only patients with IS were included because either congenital or syndromerelated scoliosis may be accompanied by rib malformation or muscular diseases. The similarity of patients' basic information also con rmed the comparability between the two groups in our study. All the patients entered the second growth peak as they demonstrated a closed TRC, in which Risser signs ≤ 2 occurred in the early stage of this period, the junction of accelerating and decelerating period [12,16]. Traditionally used to estimate the future growth potential of the spine, the Risser sign grading system is based on the fact that vertebral growth is completed at approximately the same time as fusion of the completely ossi ed iliac crest apophysis to the iliac bone occurs [12,29]. Clinically, for a patient with severe scoliosis, if the Risser sign is < 2, both fusion and non-fusion surgical intervention may be considered as clinical strategies, and to our knowledge, no research has compared the postoperative pulmonary function in patients who underwent fusion surgery with different Risser signs.
In our study, the average preoperative FEV1 of the LR group was 80.5% and the FVC was 83.1% of normal values; they increased signi cantly to 84.8% (p < 0.000) and 87.3% (p < 0.000) at the nal follow-up. This study has several limitations. First, a group of non-surgery or non-fusion patients with similar basic information as the LR and HR groups would make the study better, which requires a prospective study design in the future. Second, the number of patients available for the study was limited, not only due to the inclusion criteria, but also because of patient's compliance with the postoperative follow-up. Third, we lacked postoperative evaluation results of pulmonary function in this study; Further, evaluation of the life quality score and cardiovascular system such as ejection fraction and pulmonary artery pressure should also be assessed.

Conclusions
This study demonstrated that early thoracic fusion would not deteriorate thoracic cage development and respiratory function in patients with TRC closed idiopathic scoliosis with low Risser signs (0-2) compared with high Risser signs (3-4) during long-term observation. On the contrary, compared with patients with high Risser signs, early thoracic fusion may improve pulmonary function, especially FEV1 and FVC, in patients whose Risser sign is ≤ 2, and patients with lower Risser signs may also have a higher growth potential in thoracic development.