Abstract
Purpose
Some teenagers with adolescent idiopathic scoliosis (AIS) display compromised lung function. However, the evidence regarding the relations between pulmonary impairments and various spinal deformity parameters in these patients remains unclear, which affects clinical management. This systematic review and meta-analysis aimed to summarize the associations between various lung function parameters and radiographic features in teenagers with AIS.
Methods
A search of PubMed, Embase, PEDro, SPORTDiscus, CINAHL, Cochrane Library, and PsycINFO (from inception to March 14, 2022) without language restriction. Original studies reporting the associations between lung function and spinal deformity in patients with AIS were selected. Independent reviewers extracted data and evaluated the methodological quality of the included studies according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Pearson correlation and 95% confidence intervals were calculated using random-effects meta-analysis.
Results
Twenty-seven studies involving 3162 participants were included. Limited-quality evidence supported that several spinal parameters were significantly related to lung function parameters (e.g., absolute value and percent of the predicted forced vital capacity (FVC; %FVC), forced expiratory volume in one second (FEV1; %FEV1), and total lung capacity (TLC; %TLC)) in AIS patients. Specifically, meta-analyses showed that main thoracic Cobb angles in the coronal plane were significantly and negatively related to FVC (r = − 0.245), %FVC (r = − 0.302), FEV1 (r = − 0.232), %FEV1 (r = − 0.348), FEV1/FVC ratio (r = − 0.166), TLC (r = − 0.302), %TLC (r = − 0.183), and percent predicted vital capacity (r = − 0.272) (p < 0.001). Similarly, thoracic apical vertebral rotation was negatively associated with %FVC (r = − 0.215) and %TLC (r = − 0.126) (p < 0.05). Conversely, thoracic kyphosis angles were positively related to %FVC (r = 0.180) and %FEV1 (r = 0.193) (p < 0.05).
Conclusion
Larger thoracic Cobb angles, greater apical vertebral rotation angle, or hypokyphosis were significantly associated with greater pulmonary impairments in patients with AIS, although the evidence was limited. From a clinical perspective, the results highlight the importance of minimizing the three-dimensional spinal deformity in preserving lung function in these patients. More research is warranted to confirm these results.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Adolescent idiopathic scoliosis (AIS) is a common three-dimensional spinal deformity affecting teenagers [1]. Females are 1.4–7.2 times more likely to have AIS than males [2]. While the etiology and risk factors for the development or progression of scoliosis remain inconclusive [3], AIS and/or related treatment may cause back pain, insomnia [4], psychological distress, poor body image [5], and suboptimal quality of life [4].
Patients with AIS are not uncommon to demonstrate compromised pulmonary function [6]. Multiple studies have substantiated the presence of suboptimal pulmonary function (e.g., decreased vital capacity) in these patients [7,8,9]. While up to two-thirds of AIS patients with large scoliotic curves demonstrate restrictive respiratory abnormalities [10], recent research suggests that suboptimal ventilatory function may occur in patients with mild or moderate AIS [7, 11]. Despite the controversy [12, 13], the suboptimal pulmonary function in these patients may be related to the distortion/restriction of the spine and/or thoracic cage [14], locations of the deformity, reduced chest wall mobility [15], and/or obstructive lung disorders secondary to intrathoracic airway compression [16]. Further, patients’ pulmonary function can be compromised by the curve progression [9], and/or bracing [8, 9, 16, 17]. Conversely, these changes may be reversed by aerobic exercises.
Although a recent systematic review with meta-regression analysis revealed that the pulmonary function in patients with idiopathic scoliosis was inversely related to the curve severity [18], this review was limited by the summary of associations between coronal Cobb angles and various pulmonary parameters among patients of different types of idiopathic scoliosis. Because AIS is a three-dimensional spinal deformity, examining these associations based on coronal Cobb angles alone is incomprehensive [19]. Additionally, findings from a mixed cohort of patients with various idiopathic scoliosis cannot be generalized to patients with AIS. The current systematic review and meta-analysis addressed these limitations and summarized the evidence regarding the associations between various pulmonary functions and spinal parameters in patients with AIS, which may help clinicians identify patients at risk of having pulmonary impairment. Therefore, this review aimed to summarize the evidence regarding the: (1) associations between various pulmonary parameters and the severity of scoliosis in AIS patients; and (2) temporal relations between changes in the spinal curve due to progression/conservative treatments and the corresponding changes in pulmonary function.
Methods
This review protocol was registered with PROSPERO (CRD42016043599) and followed the Preferred Reporting Items of Systematic Reviews and Meta-analysis guidelines [20].
Search strategy
Seven databases: PubMed, Embase, PEDro, SPORTDiscus, CINAHL, Cochrane Library, and PsycINFO were searched for potential articles from inception to March 14, 2022. There were no restrictions on languages, but only English, Chinese, and Italian publications were screened. Search terms included keywords related to pulmonary function, spinal deformity, and AIS. Specifically, the Boolean search strings included (“cardiac*” OR “pulmonary” OR “lung” OR “thoracic” OR “cardiopulmonary”) AND (“test*” OR “exam*”) AND (“adolescent*” OR “teen*” OR “puberty” OR “youth”) AND (“AIS” OR “adolescent idiopathic scoliosis”). The detailed search strategy is included in Supplementary Material eTable 1.
Eligibility criteria
Articles were included had they reported an association between pulmonary function and the severity of spinal curve in patients with AIS aged between 10 and 18 years [21]. Longitudinal, cross-sectional, and case–control studies were eligible. Randomized controlled trials were included if they reported the targeted associations in AIS patients preoperatively, or before and/or after conservative treatments. Studies were excluded had they examined patients with scoliosis other than AIS, cognitive impairment, Marfan syndrome, or pectus deformity.
Screening
Three independent reviewers (MK, JY, and RC) paired up to screen titles and abstracts of all identified citations for eligibility. Studies deemed to be eligible by either reviewer were included for full-text screening. Reviewers repeated the same procedure for full-text screening. If disagreements in inclusion could not be resolved by discussion, a senior reviewer (AW) arbitrated the disagreement. The reference lists of all included articles were screened and forward citation tracing was conducted on Scopus to identify additional articles. The corresponding authors of all included studies were contacted by emails to identify omitted studies, or to seek raw data for our meta-analyses.
Data extraction
Two reviewers (MK and RC) independently extracted data from each included paper. Any disagreements were resolved with the third reviewer (AW). The collected data included: (1) study characteristics (e.g., year of publication, study design); (2) participants’ characteristics (e.g., age and gender); (3) absolute values and/or percentage predicted values of pulmonary parameters; (4) spinal/thoracic deformity parameters; and (5) statistical analyses of the associations between (3) and (4). If the included studies conducted subgroup analyses, relevant data were extracted. Missing data was marked as “not reported.” A list of definitions of pulmonary and spinal parameters is shown in eTable 2. This includes common terminology such as Lenke and King's classifications of scoliotic curve [23], angle of trunk rotation [22], surface spinal penetration index [24] and endothoracic hump ratio [25].
Risk of bias assessments
Two independent reviewers (RC and AW) assessed the methodological quality of prospective studies using the Quality in Prognostic Studies (QUIPS) [26], cross-sectional studies using Appraisal tool for Cross-Sectional Studies (AXIS) [27], and case–control studies using Newcastle–Ottawa Scale (NOS) [28]. Studies that retrospectively analyzed data or collected data at a single time point were assessed using AXIS. Any disagreements in the assessment results were resolved by consensus.
Data syntheses
Meta-analyses
The primary measure was the associations (e.g., Spearman’s/Pearson coefficients) between various spinal parameters and pulmonary functions in patients with AIS. The correlation coefficients were interpreted as weak, moderate, and strong if their values were 0.3, 0.5, and 0.7, respectively [29]. If three or more clinically homogenous studies investigated the same association, data were pooled for meta-analysis using random-effects model using the Comprehensive Meta-analysis version 3.0 software (Biostat, NJ, USA). Separate meta-analyses were conducted for studies involving multiple regression models. The significance level was set at 0.05. Statistical heterogeneity of the included studies in meta-analyses was graded as low, moderate, and high if the I2 statistics were ≤ 25%, between 26 and 74%, and ≥ 75%, respectively [30]. If meta-analyses were not conducted, the correlations were summarized narratively.
Subgroup analyses
Subgroup analyses were planned to examine the cross-sectional/longitudinal associations between spinal parameters and pulmonary functions based on: (1) genders; (2) severity of the pulmonary impairment; (3) severity of scoliosis; (3) thoracic or lumbar scoliosis; and (4) before and after conservative treatments or curve progression.
Levels of evidence
Levels of evidence were rated as strong, moderate, limited, and very limited based on established criteria (eTable 3) [31, 32].
Results
Database searches yielded 3723 non-duplicated titles and abstracts for screening. Twenty-one out of 278 full-text articles were included. Further, manual searches of reference lists and forward citation of the included articles yielded six additional included articles (Fig. 1).
Study characteristics
Table 1 summarizes characteristics of the 22 included cross-sectional studies [8, 9, 11, 16, 17, 33,34,35,36,37,38,39,40,41,42,43,44,49] and five case–control studies [7, 50,51,52,53] that involved 3,162 participants. All included studies used spirometry and some also used plethysmography [9, 16, 33, 41, 49, 53] to evaluate lung function. The reported pulmonary function parameters included the absolute values of forced vital capacity (FVC), forced expiratory volume in the first second (FEV1), FEV1/FVC ratio, forced expiratory flow at 25% and 75% of FVC (FEF25–75%), FEF25%, FEF50%, peak expiratory flow (PEF), vital capacity (VC), residual volume (RV), total lung capacity (TLC), RV/TLC ratio, functional residual capacity, etc. Some studies reported these parameters as the percentage of predicted values (e.g., %FVC, %FEV1, and %TLC). The predicted values were determined according to age-, gender-, and height-matched normative data [54]. Some included studies used equations to estimate patients’ “actual height” from the arm span [7, 8, 16, 17, 35,36,37, 39, 47, 48, 53] or Cobb angles [11, 42, 45] to predict participants’ pulmonary functions. Pulmonary functions were considered normal if their measured values exceeded 80% of the predicted values [9, 49].
Spinal parameters were measured by X-rays or computed tomography scans. Five studies used biplanar X-rays with three-dimensional reconstruction of the spine and/or rib cage [17, 33, 43, 49, 55]. The reported spinal parameters included proximal thoracic Cobb angles [9, 35, 43, 55] main thoracic Cobb angles on anteroposterior radiographs in a standing [7, 8, 16, 17, 29,30,35, 34,35,36,37,38,43, 41,42,43,44,49, 53, 55] or supine bending position [39], thoracic kyphosis angles [9, 35, 41, 43, 45], and apical vertebral rotation angles [17, 39, 43, 49, 50, 55] (Table 1). Most included studies used univariate analyses to determine the associations of interest. Nine studies used multiple regression to evaluate such associations [9, 16, 38, 39, 37,38,39,44, 51] (Table 1).
Risk of bias assessments
All 22 included cross-sectional studies did not justify their sample sizes, nor report the response rate or non-responders’ characteristics [8, 9, 11, 16, 17, 29,30,35, 33,34,35,36,37,38,39,40,41,42,43,44,49, 55] (eTable 4). Five cross-sectional studies [17, 37, 38, 40, 55] did not describe participants’ demographics (e.g., gender distribution) [17, 38, 40], while seven studies [11, 34, 37, 39, 46, 48, 49] did not discuss their limitations. Nine included studies did not mention the ethical approval or the informed consent process [9, 11, 34, 33,34,39, 43, 44, 46]. Similarly, all included case–control studies [7, 46,47,48,53] did not describe the non-response rate, while four of them [7, 47,48,53] did not describe the recruitment process of controls (eTable 5).
Associations between spinal parameters and lung function
Univariate correlations between 43 spinal parameters and 32 pulmonary function parameters were reported (Table 2 and eTable 6). Twenty-seven meta-analyses were conducted to reveal 22 significant correlations. Of them, 20 showed significant but weak correlations. Further, 11 included studies used multivariate analyses to identify independent spinal parameters that predicted pulmonary function [9, 11, 16, 38, 39, 41,42,43,44, 51, 53]. Given the numerous investigated correlations, only significant correlations with at least limited-quality evidence were reported and discussed in this review.
No included studies investigated the gender-related correlations between spinal parameters and lung function. No included studies reported the temporal relations between changes in spinal structure and the corresponding changes in pulmonary function in conservatively treated patients with AIS. Although Lin et al. [35] reported that lung function parameters did not significantly differ between AIS patients with and without a history of brace usage, some studies [44, 51] found that compared to “non-brace” patients, those with bracing had poorer lung function. Furthermore, some studies compared patients’ lung function based on different Lenke classification types [47, 48], a Cobb angle cutoff [52], a kyphosis angle cutoff [17, 37], and BMI [38, 42]. Two included studies compared spinal parameters based on the severity of lung impairment [41, 49].
Significant negative univariate correlations
Meta-analyses showed that proximal thoracic Cobb angles were negatively related to %FVC (r = − 0.194; 95% confidence interval [95% Cl]: − 0.253 to − 0.134) and %FEV1 (r = − 0.234; 95% Cl: − 0.291 to − 0.175) (Supplementary Material eFigure 1), while main thoracic Cobb angles were negatively associated with %FVC (r = − 0.302), FVC (r = − 0.245), %FEV1 (r = − 0.348), FEV1 (r = − 0.232), FEV1/FVC ratio (r = − 0.166), %TLC (r = − 0.183), TLC (r = − 0.302), and %VC (r = − 0.272) (Fig. 2). Similarly, significant negative correlations were noted between the number of involved thoracic vertebrae and %FVC (r = − 0.262; 95% Cl: − 0.524 to − 0.215) and %FEV1 (r = − 0.255; 95% Cl: − 0.346 to − 0.159), between main thoracic apical vertebral rotation and %FVC (r = − 0.215; 95% Cl: − 0.314 to − 0.112) and %TLC (r = − 0.126; 95% Cl: − 0.240 to − 0.009), between maximum rib hump and FVC (r = − 0.225; 95% Cl: − 0.367 to − 0.072), as well as between lumbar lordosis and %FVC (r = − 0.099; 95% Cl: − 0.165 to − 0.032) and %FEV1 (r = − 0.116; 95% Cl: − 0.182 to − 0.049) (Table 2; eFigures 2–5).
Significant positive univariate correlations
Thoracic kyphosis angles were positively related to %FVC (r = 0.180; 95% Cl, 0.151 to 0.432) and %FEV1(r = 0.193; 95% Cl: 0.007 to 0.365) (Table 2; eFigure 6). Other meta-analyses revealed that higher rib cage thickness (r = 0.377; 95% Cl: 0.155 to 0.562), width (r = 0.635; 95% Cl: 0.486 to 0.748), and volume (r = 0.784; 95% Cl: 0.716 to 0.838) were significantly associated with higher FVC (Table 2; eFigures 7–9).
Reported multivariate analyses
Three meta-analyses showed significant correlations between main thoracic Cobb angles and %FVC (r = − 0.309), as well as between main thoracic kyphosis angles and FEV1 (r = 0.318) or %FVC (r = 0.226) after adjusting for confounders (Fig. 3). These results were similar to the corresponding meta-analyses of univariate analysis (Fig. 2; eFigure 6).
Discussion
This is the first systematic review and meta-analysis to summarize the associations between various spinal parameters and pulmonary function parameters in patients with AIS. Limited-quality evidence supports that increased thoracic Cobb angles, number of involved thoracic vertebrae, apical vertebral rotation, rib hump, and lumbar lordotic angles are related to decreased %FVC, whereas increased thoracic kyphosis angles are associated with larger %FVC and %FEV1. Rib cage parameters are positively correlated with FVC.
Scoliosis involves three-dimensional spinal deformity and thoracic cage distortion that may affect each other and worsen lung function [56]. Notably, thoracic cage deformity may alter spinal curvature, and causes rotation and shortening of the thoracic spine, leading to compromised chest wall compliance [57], decreased lung volume under the rib hump, and lung impingement on the concave side. The compressed lung tissues may reduce lung compliance, causing restrictive lung diseases [58]. Similarly, the rotational vertebral deformity may cause thoracic asymmetry [11], which increases the chest wall stiffness [59], reduces the efficiency of respiratory muscles and the diaphragm [8]. The vertebral rotation and rib hump can also cause imbalance in bilateral paraspinal and respiratory muscles [60], limiting the elevation of ribs and reducing lateral and anteroposterior movements of the thoracic cage [11]. These altered chest wall and respiratory muscle mechanics may decrease TLC [61], and increase the risk of hypercapnia, hypoxemia, and alveolar hypoventilation, causing irreversible lung atrophy [57].
While it is well known that patients with thoracic Cobb angles > 50° display clinically significant pulmonary impairments [62], our findings suggest that pulmonary impairment exists even in patients with mild-to-moderate idiopathic scoliosis [53]. However, some patients with severe spinal curvature may not show pulmonary decline if they have good apical vertebral rotational flexibility [39]. Notably, AIS patients with a flexible spine (rotational flexibility > 55%) have normal lung function [56]. Therefore, thoracic curve flexibility should be considered in evaluating the associations.
The decreased %FVC and %VC but a normal FEV1/FVC ratio among patients with AIS in the included studies indicate that they show restrictive lung characteristics [7, 55]. However, there are conflicting findings regarding the relation between spinal deformity and obstructive lung disease in patients with AIS. While one included study reported no significant relation between main thoracic Cobb angles and FEV1/FVC ratio [34], another included study found that 68 out of 176 AIS patients with thoracic Cobb angle > 40° had obstructive lung diseases although no significant correlation between Cobb angles and FEV1/FVC ratio was noted [16]. The latter study also showed that 73% of these 68 patients had irreversible obstructive lung disease that could not be improved by bronchodilator [16]. Although multiple factors (e.g., lower airway malacia, asthma) may lead to obstructive lung characteristics [16], rib cage deformity-related intrathoracic airway compression or respiratory muscle weakness may contribute to such findings [8]. Given the high prevalence of irreversible obstructive lung diseases in patients with moderate to severe AIS, endoscopy or chest imaging may be indicated for this airway obstruction [16].
The consistent findings of significant but weak correlations between various structural characteristics and pulmonary function may be ascribed to no adjustment for confounders (e.g., BMI and duration of bracing). Abnormal mechanical loading of respiratory muscles and altered muscle length-tension relationship can affect respiratory muscle contraction and lung function [7, 63], especially in patients with mild AIS [60]. Higher BMI is associated with better %FVC in teenagers with Cobb angle > 40° [38, 42]. Research found that the association between BMI and %FVC was stronger than those between thoracic Cobb angles or kyphosis angles and %FVC [38]. Heavier teens tend to have greater thoracic kyphosis, which yields better %FVC than hypokyphotic peers [38]. Additionally, one study found that brace wearing temporarily compromised %FEV1 in AIS patients after accounting for thoracic kyphosis [51], although it was unclear whether participants took off the brace during spirometry. Compared to AIS patients without bracing, patients with a thoracic curve and bracing displayed significantly poorer %FVC and %FEV1 [44, 51]. However, the pulmonary function/compliance restores to previous conditions once the brace is removed [64]. Likewise, the negative association between lumbar lordosis and %FVC or %FEV1 might have disappeared if confounders were considered.
This review had some limitations. Because many included studies performed pulmonary function tests on AIS patients preoperatively, their findings may represent patients with more severe curves. Further, most included studies did not define the vertebral levels for classifying the proximal and main thoracic curves, which might introduce discrepancies in our pooled results.
Implications
Most included studies measured anteroposterior and lateral spinal features on radiographs. Future studies should adopt low-dose biplanar X-ray imaging for three-dimensional thoracic cage and spinal structure reconstruction [19], which could capture the three-dimensional impacts of spinal/thoracic deformities on patients with AIS. This allows comprehensive evaluation of the relations between spinal deformities and lung function, which may guide clinical management and research.
While patients with mild AIS may not show respiratory dysfunction at rest, they may display reduced functional capacity [65], or maximum oxygen uptake during exercise tolerance tests [50]. Spirometry may not detect subtle deterioration or dyspnea on exertion, which may indicate scoliosis-related respiratory decline. Clinicians should conduct progressive exercise tests on patients with suspected respiratory impairments to detect early respiratory dysfunction. If the curve progresses, regular progressive exercise tests are recommended [57].
Scoliosis can directly (spinal deformity) or indirectly (respiratory muscle weakness/ inefficiency) affect respiratory function. Although patients with mild-to-moderate scoliosis may not experience dramatic pulmonary impairments during daily activities, it is important to use bracing or physiotherapy scoliosis-specific exercises to prevent or delay curve progression in these patients [64]. However, bracing should be worn for at least 16 h per day to prevent curve progression [57, 66]. Therefore, aerobic training should be prescribed to patients with bracing to optimize their lung functions.
Since pulmonary deficits in AIS patients may worsen with curve progression, patients indicated for surgical correction may experience pulmonary impairment secondary to severe scoliosis [67]. While AIS patients with moderate lung volume are less likely to require postoperative ventilatory support [37], those with moderate or severe defects (< 60% of predicted VC) may indicate high-risk surgical fusion. The latter should undergo full spirometry before surgery. VC can be used as a screening indicator for all patients before spinal surgery [37] because such surgery may adversely affect pulmonary function/compliance [68].
Because there was no included prospective study, the causal relations between changes in spinal/thoracic deformity and changes in lung function remain unclear. Future prospective studies should investigate such relations after adjusting for confounders. Further, as prior research involving AIS patients aged > 18 years revealed that patients had worsening pulmonary function (e.g., FVC) as they aged [67, 69], future prospective research with long-term follow-ups should determine whether AIS patients with near-normal, mild, or moderate lung dysfunction would experience declined lung function and body’s functionality in later life [70].
Conclusions
This systematic review highlights that larger proximal and main thoracic Cobb angles, smaller kyphosis angles, greater lumbar lordotic angles, a longer thoracic curve, a larger rib hump, increased apical vertebral rotation angles and smaller rib cages are associated with poorer pulmonary functions. Other factors can also affect the lung function in these patients. Nevertheless, the clinical impact of scoliosis on lung function is mainly subclinical except for those with severe structural deformity. We definitely need more research to strengthen the quality of evidence. Future prospective studies should evaluate the temporal relations between changes in spinal/thoracic parameters and changes in pulmonary function in order to inform the clinical management of AIS patients with potential respiratory decline.
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Soucacos PN, Zacharis K, Soultanis K, Gelalis J, Xenakis T, Beris AE (2000) Risk factors for idiopathic scoliosis: review of a 6-year prospective study. Orthopedics 23:833–838
Konieczny MR, Senyurt H, Krauspe R (2013) Epidemiology of adolescent idiopathic scoliosis. J Child Orthop 7:3–9. https://doi.org/10.1007/s11832-012-0457-4
Wajchenberg M, Astur N, Kanas M, Martins DE (2016) Adolescent idiopathic scoliosis: current concepts on neurological and muscular etiologies. Scoli Spinal Disord 11:1–5
Wong AY, Samartzis D, Cheung PW, Cheung JPY (2019) How common is back pain and what biopsychosocial factors are associated with back pain in patients with adolescent idiopathic scoliosis? Clin Orthop Relat Res 477:676
Misterska E, Glowacki M, Latuszewska J, Adamczyk K (2013) Perception of stress level, trunk appearance, body function and mental health in females with adolescent idiopathic scoliosis treated conservatively: a longitudinal analysis. Qual Life Res 22:1633–1645. https://doi.org/10.1007/s11136-012-0316-2
Sperandio EF, Alexandre AS, Liu CY, Poletto PR, Gotfryd AO, Vidotto MC, Dourado VZ (2014) Functional aerobic exercise capacity limitation in adolescent idiopathic scoliosis. Spine J 14:2366–2372
Abdelaal AAM, Abd El Kafy EMAES, Elayat MSEM, Sabbahi M, Badghish MSS (2018) Changes in pulmonary function and functional capacity in adolescents with mild idiopathic scoliosis: observational cohort study. J Int Med Res 46:381–391
Kim YJ, Lenke LG, Bridwell KH, Cheh G, Whorton J, Sides B (2007) Prospective pulmonary function comparison following posterior segmental spinal instrumentation and fusion of adolescent idiopathic scoliosis: Is there a relationship between major thoracic curve correction and pulmonary function test improvement? Spine 32:2685–2693. https://doi.org/10.1097/BRS.0b013e31815a7b17
Newton PO, Faro FD, Gollogly S, Betz RR, Lenke LG, Lowe TG (2005) Results of preoperative pulmonary function testing of adolescents with idiopathic scoliosis: a study of six hundred and thirty-one patients. JBJS 87:1937–1946
Banjar HH (2003) Pediatric scoliosis and the lung. Saudi Med J 24:957–963
Takahashi S, Suzuki N, Asazuma T, Kono K, Ono T, Toyama Y (2007) Factors of thoracic cage deformity that affect pulmonary function in adolescent idiopathic thoracic scoliosis. Spine 32:106–112
Wood KB, Schendel MJ, Dekutoski MB, Boachie-Adjei O, Heithoff KH (1996) Thoracic volume changes in scoliosis surgery. Spine 21:718–723
Kearon C, Killian J (1993) Fadors determining pulmonary fundion in adolescent idiopathic thoracic scoliosis. Am Rev Respir Dis 148:288–294
Wozniczka JK, Ledonio CG, Polly DW, Rosenstein BE, Nuckley DJ (2017) Adolescent idiopathic scoliosis thoracic volume modeling: the effect of surgical correction. J Pediatr Orthop 37:e512–e518
Leong J, Lu W, Luk K, Karlberg E (1999) Kinematics of the chest cage and spine during breathing in healthy individuals and in patients with adolescent idiopathic scoliosis. Spine 24:1310
McPhail GL, Ehsan Z, Howells SA, Boesch RP, Fenchel MC, Szczesniak R, Jain V, Agabegi S, Sturm P, Wall E (2015) Obstructive lung disease in children with idiopathic scoliosis. J Pediatr 166:1018–1021
Ilharreborde B, Dubousset J, Skalli W, Mazda K (2013) Spinal penetration index assessment in adolescent idiopathic scoliosis using EOS low-dose biplanar stereoradiography. Eur Spine J 22:2438–2444. https://doi.org/10.1007/s00586-013-2892-4
Kempen DHR, Heemskerk JL, Kaçmaz G, Altena MC, Reesink HJ, Vanhommerig JW, Willigenburg NW (2022) Pulmonary function in children and adolescents with untreated idiopathic scoliosis: a systematic review with meta-regression analysis. Spine J. https://doi.org/10.1016/j.spinee.2021.12.011
Melhem E, Assi A, El Rachkidi R, Ghanem I (2016) EOS® biplanar X-ray imaging: concept, developments, benefits, and limitations. J Child Orthop 10:1–14
Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341
Altaf F, Gibson A, Dannawi Z, Noordeen H (2013) Adolescent idiopathic scoliosis. Bmj 346
Ovadia D (2013) Classification of adolescent idiopathic scoliosis (AIS). J Child Orthop 7:25–28. https://doi.org/10.1007/s11832-012-0459-2
Bunnell WP (1984) An objective criterion for scoliosis screening. J Bone Joint Surg 66:1381–1387. https://doi.org/10.2106/00004623-198466090-00010
Dubousset J, Wicart P, Pomero V, Barois A, Estournet B (2003) Spinal penetration index: new three-dimensional quantified reference for lordoscoliosis and other spinal deformities. J Orthop Sci 8:41–49. https://doi.org/10.1007/s007760300007
Ito K, Kawakami N, Miyasaka K, Tsuji T, Ohara T, Nohara A (2012) Scoliosis associated with airflow obstruction due to endothoracic vertebral hump. Spine (Phila Pa 1976) 37:2094–2098. https://doi.org/10.1097/BRS.0b013e31825d2ea3
Hayden JA, van der Windt DA, Cartwright JL, Côté P, Bombardier C (2013) Assessing bias in studies of prognostic factors. Ann Intern Med 158:280–286
Downes MJ, Brennan ML, Williams HC, Dean RS (2016) Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open 6:e011458
Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses.
Portney LG (2015) Foundations of clinical research : applications to practice. Philadelphia, PA : F.A. Davis Company, Philadelphia, PA
Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ (Clinical Research Ed) 327:557–560. https://doi.org/10.1136/bmj.327.7414.557
Wong AYL, Chan LLY, Lo CWT, Chan WWY, Lam KCK, Bao JCH, Ferreira ML, Armijo-Olivo S (2021) Prevalence/incidence of low back pain and associated risk factors among nursing and medical students: a systematic review and meta-analysis. PM & R 13:1266–1280. https://doi.org/10.1002/pmrj.12560
Lau KKL, Samartzis D, To NSC, Harada GK, An HS, Wong AYL (2021) Demographic, surgical, and radiographic risk factors for symptomatic adjacent segment disease after lumbar fusion: a systematic review and meta-analysis. J Bone Joint Surg 103:1438–1450. https://doi.org/10.2106/JBJS.20.00408
Bouloussa H, Pietton R, Vergari C, Haen TX, Skalli W, Vialle R (2019) Biplanar stereoradiography predicts pulmonary function tests in adolescent idiopathic scoliosis: a cross-sectional study. Eur Spine J 28:1962–1969. https://doi.org/10.1007/s00586-019-05940-3
Huh S, Eun LY, Kim NK, Jung JW, Choi JY, Kim HS (2015) Cardiopulmonary function and scoliosis severity in idiopathic scoliosis children. Korean J Pediatr 58:218
Lin Y, Feng E, Shen J, Tan H, Jiao Y, Rong T, Chen L, Yuan W, Cong H, Liu S, Luo J (2022) Influences of thoracic spinal deformity on exercise performance and pulmonary function: a prospective study of 168 patients with adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 47:107–115. https://doi.org/10.1097/brs.0000000000004161
Machino M, Kawakami N, Ohara T, Saito T, Tauchi R, Imagama S (2021) Three-dimensional reconstruction image by biplanar stereoradiography reflects pulmonary functional states in adolescent idiopathic scoliosis. J Clin Neurosci 88:178–184. https://doi.org/10.1016/j.jocn.2021.03.043
Muirhead A, Conner AN (1985) The assessment of lung function in children with scoliosis. J Bone Joint Surg Br 67:699–702
Tung R, Uvodich M, Anderson JT, Carpenter K, Sherman A, Lozano R (2018) Do heavier patients with adolescent idiopathic scoliosis have more preserved thoracic kyphosis and pulmonary function? Spine Deform 6:704–706
Upadhyay SS, Mullaji AB, Luk KD, Leong JC (1995) Relation of spinal and thoracic cage deformities and their flexibilities with altered pulmonary functions in adolescent idiopathic scoliosis. Spine 20:2415–2420. https://doi.org/10.1097/00007632-199511001-00008
Villamor GA, Andras LM, Redding G, Chan P, Yang J, Skaggs DL (2019) A comparison of maximal voluntary ventilation and forced vital capacity in adolescent idiopathic scoliosis patients. Spine Deform 7:729–733. https://doi.org/10.1016/j.jspd.2019.02.007
Wang Y, Yang F, Wang D, Zhao H, Ma Z, Ma P, Hu X, Wang S, Kang X, Gao B (2019) Correlation analysis between the pulmonary function test and the radiological parameters of the main right thoracic curve in adolescent idiopathic scoliosis. J Orthop Surg Res 14:443. https://doi.org/10.1186/s13018-019-1451-z
Xu L, Sun X, Zhu Z, Qiao J, Mao S, Qiu Y (2015) Body mass index as an indicator of pulmonary dysfunction in patients with adolescent idiopathic scoliosis. J Spinal Disord Tech 28:226–231. https://doi.org/10.1097/BSD.0b013e31825d97df
Yaszay B, Bastrom TP, Bartley CE, Parent S, Newton PO (2017) The effects of the three-dimensional deformity of adolescent idiopathic scoliosis on pulmonary function. Eur Spine J 26:1658–1664
Yu B, Wang Y, Qiu G, Shen J, Zhang J, Lao L (2013) The influence of preoperative brace treatment on the pulmonary function test in female adolescent idiopathic scoliosis. J Spinal Disord Tech 26:E254–E258. https://doi.org/10.1097/BSD.0b013e318289be35
Akazawa T, Kotani T, Sakuma T, Nakayama K, Iijima Y, Torii Y, Iinuma M, Kuroya S, Asano K, Ueno J, Yoshida A, Murakami K, Minami S, Orita S, Inage K, Shiga Y, Nakamura J, Inoue G, Miyagi M, Saito W, Eguchi Y, Fujimoto K, Takahashi H, Ohtori S, Niki H (2021) Pulmonary function improves in patients with adolescent idiopathic scoliosis who undergo posterior spinal fusion regardless of thoracoplasty: a mid-term follow-up. Spine Surg Relat Res 5:22–27. https://doi.org/10.22603/SSRR.2020-0077
Daruwalla J, Tan W (1985) Spirometric pulmonary function tests before and after surgical correction of idiopathic scoliosis in adolescents. Ann Acad Med Singapore 14:475–478
Gitelman Y, Lenke LG, Bridwell KH, Auerbach JD, Sides BA (2011) Pulmonary function in adolescent idiopathic scoliosis relative to the surgical procedure: a 10-year follow-up analysis. Spine (Phila Pa 1976) 36:1665–1672. https://doi.org/10.1097/BRS.0b013e31821bcf4c
Kim YJ, Lenke LG, Bridwell KH, Kim KL, Steger-May K (2005) Pulmonary function in adolescent idiopathic scoliosis relative to the surgical procedure. J Bone Joint Surg Am 87:1534–1541. https://doi.org/10.2106/JBJS.C.00978
Pietton R, Bouloussa H, Langlais T, Taytard J, Beydon N, Skalli W, Vergari C, Vialle R (2022) Estimating pulmonary function after surgery for adolescent idiopathic scoliosis using biplanar radiographs of the chest with 3D reconstruction. Bone Joint J 104-b:112–119. https://doi.org/10.1302/0301-620x.104b1.Bjj-2021-0337.R2
Barrios C, Pérez-Encinas C, Maruenda JI, Laguía M (2005) Significant ventilatory functional restriction in adolescents with mild or moderate scoliosis during maximal exercise tolerance test. Spine 30:1610–1615. https://doi.org/10.1097/01.brs.0000169447.55556.01
Ran B, Fan Y, Yuan F, Guo K, Zhu X (2016) Pulmonary function changes and its influencing factors after preoperative brace treatment in patients with adolescent idiopathic scoliosis: a retrospective case-control study. Medicine 95:e5088. https://doi.org/10.1097/MD.0000000000005088
Saraiva BMA, Araujo GS, Sperandio EF, Gotfryd AO, Dourado VZ, Vidotto MC (2018) Impact of scoliosis severity on functional capacity in patients with adolescent idiopathic scoliosis. Pediatr Exerc Sci 30:243–250. https://doi.org/10.1123/pes.2017-0080
Szeinberg A, Canny GJ, Rashed N, Veneruso G, Levison H (1988) Forced vital capacity and maximal respiratory pressures in patients with mild and moderate scoliosis. Pediatr Pulmonol 4:8–12
Murray JF, Nadel JA (2000) Textbook of respiratory medicine. Saunders, Philadelphia
Machino M, Kawakami N, Ohara T, Saito T, Tauchi R, Imagama S (2020) Accuracy of rib cage parameters from 3-Dimensional reconstruction images obtained using simultaneous biplanar radiographic scanning technique in adolescent idiopathic scoliosis: Comparison with conventional computed tomography. J Clin Neurosci 75:94–98. https://doi.org/10.1016/j.jocn.2020.03.016
Upadhyay S, Mullaji A, Luk K, Leong J (1995) Evaluation of deformities and pulmonary function in adolescent idiopathic right thoracic scoliosis. Eur Spine J 4:274–279
Koumbourlis AC (2006) Scoliosis and the respiratory system. Paediatr Respir Rev 7:152–160
Vitale MG, Matsumoto H, Bye MR, Gomez JA, Booker WA, Hyman JE, Roye DP Jr (2008) A retrospective cohort study of pulmonary function, radiographic measures, and quality of life in children with congenital scoliosis: an evaluation of patient outcomes after early spinal fusion. Spine 33:1242–1249
Thilagaratnam S (2007) School-based screening for scoliosis: is it cost-effective? Singapore Med J 48:1012–1017
Smyth R, Chapman K, Wright T, Crawford J, Rebuck A (1984) Pulmonary function in adolescents with mild idiopathic scoliosis. Thorax 39:901–904
Cooper DM, Rojas JV, Mellins RB, Keim HA, Mansell AL (1984) Respiratory mechanics in adolescents with idiopathic scoliosis. Am Rev Respir Dis 130:16–22
Weinstein SL (2019) The natural history of adolescent idiopathic scoliosis. J Pediatr Orthop 39:S44–S46. https://doi.org/10.1097/BPO.0000000000001350
Martínez-Llorens J, Ramírez M, Colomina M, Bagó J, Molina A, Cáceres E, Gea J (2010) Muscle dysfunction and exercise limitation in adolescent idiopathic scoliosis. Eur Respir J 36:393–400
Katsaris G, Loukos A, Valavanis J, Vassiliou M, Behrakis P (1999) The immediate effect of a Boston brace on lung volumes and pulmonary compliance in mild adolescent idiopathic scoliosis. Eur Spine J 8:2–7
Duiverman M, de Boer E, van Eykern L, de Greef M, Jansen D, Wempe J, Kerstjens H, Wijkstra P (2009) Respiratory muscle activity and dyspnea during exercise in chronic obstructive pulmonary disease. Respir Physiol Neurobiol 167:195–200
Roye BD, Simhon ME, Matsumoto H, Bakarania P, Berdishevsky H, Dolan LA, Grimes K, Grivas TB, Hresko MT, Karol LA, Lonner BS, Mendelow M, Negrini S, Newton PO, Parent EC, Rigo M, Strikeleather L, Tunney J, Weinstein SL, Wood G, Vitale MG (2020) Establishing consensus on the best practice guidelines for the use of bracing in adolescent idiopathic scoliosis. Spine Deform 8:597–604. https://doi.org/10.1007/s43390-020-00060-1
Johari J, Sharifudin MA, Ab Rahman A, Omar AS, Abdullah AT, Nor S, Lam WC, Yusof MI (2016) Relationship between pulmonary function and degree of spinal deformity, location of apical vertebrae and age among adolescent idiopathic scoliosis patients. Singapore Med J 57:33–38
Upadhyay S, Ho E, Gunawardene W, Leong J, Hsu L (1993) Changes in residual volume relative to vital capacity and total lung capacity after arthrodesis of the spine in patients who have adolescent idiopathic scoliosis. J Bone Joint Surg Am 75:46–52
Pehrsson K, Bake B, Larsson S, Nachemson A (1991) Lung function in adult idiopathic scoliosis: a 20 year follow up. Thorax 46:474–478
Muniyappanavar NS, Shivakumar J, Dixit PD, Shenoy JP, Teli SS, Chandrashekar A (2013) Impact of asymptomatic idiopathic scoliosis on pulmonary function. Natl J Physiol, Pharm Pharmacol 3:153–157
Acknowledgements
The authors would like to thank Ms. Rebeca Chan, Mr. Johnny Yan, Ms. Rachel Yan, and Mr. Kenney Lau for their help in the search or assisting the data analyses.
Funding
Prof. Stefano Negrini is holding stocks of Italian Scientific Spine Institute. No funding was received for conducting this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
There were no financial or competing conflicts of interest in relation to this work.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Kan, M.M.P., Negrini, S., Di Felice, F. et al. Is impaired lung function related to spinal deformities in patients with adolescent idiopathic scoliosis? A systematic review and meta-analysis—SOSORT 2019 award paper. Eur Spine J 32, 118–139 (2023). https://doi.org/10.1007/s00586-022-07371-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00586-022-07371-z