Scoliosis and Pectus Excavatum in Adolescents: Does the Nuss Procedure Affect the Scoliotic Curvature?

Abstract

Background:

Pectus excavatum (PE) is known to be associated with adolescent idiopathic scoliosis (AIS). The correction of severe PE requires a mini-invasive procedure (MIRPE), with a metal bar positioned and left in the chest for 3 years. Adolescence seems to be the more appropriate time not only for MIRPE but also for AIS peak progression. This study was designed to answer the question whether, in adolescents, MIRPE could affect mild/moderate AIS.

Methods:

We carried out a meta-analysis focused on defining the natural progression of untreated AIS. Inclusion criteria were as follows: AIS patients -age 10–18 years old -Cobb angle <40°-none treated as orthotics/electrostimulation/surgery. The expected outcome was the percentage of patients who improved, worsened, or hold steady of their condition at follow-up. Between 2008 and 2014, we followed up a cohort of 67 adolescents with severe PE treated with MIRPE, assessing whether AIS underwent a modification in the period between bar insertion and removal.

Results:

Meta-analysis included 9 studies with 1641 AIS patients. Although heterogeneous (I² = 99.5%, P < .0001), the overall percentage of progression for untreated AIS was 42.5% (CI 18.2%–72.2%). In our follow-up group who underwent MIRPE, 34 out of 67 patients had concurrent AIS with a Cobb angle >10° (range 10°–45°). We demonstrated that MIRPE had a favorable effect on AIS, with a mean improvement of 1.5° (CI 0.64–2.44; P = .0011).

Conclusion:

In our PE patients with AIS, MIRPE had a beneficial effect also on the spine. From our preliminary results, it seems that MIRPE should be offered during puberty as a timely option for treating PE and stabilizing mild/moderate scoliosis progression, when concurrent.

Background

Pectus Excavatum (PE) is the most common anterior chest wall deformity with an estimated occurrence of 1 in 1000 live births being males affected three to five times more often than females.¹ In most patients, the presence of PE is already visible during the first year of life and typically progresses with pubertal growth spurt.² Although in most cases it is asymptomatic, PE can lead to cardiopulmonary dysfunctions: exercise intolerance and dyspnea on exertion are the most frequent symptoms noted in PE patients.³ PE is typically associated with mild connective tissue disorders,⁴ mitral valve prolapse, dysrhythmias, abnormal posture with dorsal lordosis, thoracic kyphosis, and/or adolescent idiopathic scoliosis (AIS), which occur in about 15% to 20%.^5,6

Surgical correction leads to both cosmetic and functional improvements in case of severe PE, whereas for mild deformities it has mainly a positive impact on cosmesis and sociopsychological trait.⁷ In 1998, Nuss described an innovative mini-invasive procedure (MIRPE) based on the concept of internal bracing: a curved metal bar is inserted through two lateral chest incisions under thoracoscopic view, avoiding cartilage resection. This approach was designed to improve both functional and cosmetic outcomes in comparison with the previous repairing techniques. The bar is then removed after about 3 years.⁸ Although initially the preferred age for such correction was deemed to be infancy when the chest is more moldable, subsequently MIRPE has been proposed during adolescence when patients, which are closer to skeletal maturity, are more committed to surgical correction.^9,10

Scoliosis is a three-dimensional deviation of the spinal axis, defined by a coronal curvature exceeding 10° on an anteroposterior X-ray image.¹¹ Its prevalence is 1%–2% in school children, which rises above 8% in young adults, with a 6:1 female/male ratio.¹²

AIS etiopathogenesis continues to be poorly understood: its diagnosis remains that of exclusion and other likely causes of scoliosis, including spinal infections and neoplasms and neuromuscular and syndromic conditions, as well as congenital anomalies of the vertebral column or the neural axis, should be excluded. In case of minor AIS, usually a conservative management is offered, in which the primary aim is to stop curvature progression. According to the Society on Scoliosis Orthopaedic and Rehabilitation Treatment (SOSORT) guidelines for scoliosis treatment, in case of mild AIS with demonstrated progression of deformity or elevated risk of worsening, orthosis is recommended to treat patients with curves above 15° Cobb angle. Conversely, surgical correction and stabilization of the affected segment of the spine is considered for AIS exceeding 45°.¹¹ To date, some reports have shown a relationship between PE and AIS in teenagers and adults,^13–15 although none reports the effect on the spine of a surgical procedure used to correct an anterior chest wall deformity such as PE.

While as per SOSORT guidelines, bracing is indicated for those patients affected by AIS above 15° to prevent progression, it appears pivotal to clarify whether a surgical approach such as MIRPE could have a positive impact on the spine or, conversely, a timely priority should be given to AIS treatment.

To better understand such associated condition, we developed a simplified, but effective mathematical model, which hypothesizes how forces are working in the chest following Nuss bar positioning (Supplementary Data; Supplementary Data are available online at www.liebertpub.com/lap). Then we carried out a systematic review with meta-analysis to understand the natural progression of untreated AIS.

Eventually, we present a cohort of patients affected by PE operated at our institution in which we analyzed the presence of concurrent AIS before surgery and in whom we analyzed whether this condition improved, deteriorated, or remained unchanged following the bar removal, 3 years after its placement.

Methods

Systematic review and meta-analysis

To evaluate the natural history of patients with untreated AIS, we carried out a systematic review and a random effects meta-analysis. We used a random effects model to perform the analysis to take into account the heterogeneity of previous studies. Computerized literature searches were conducted in database, including the PubMed, Cochrane Library, and Scopus databases. Only articles published in English were considered. The key word “untreated scoliosis” was used for each database while the other key word “pectusexcavatum & scoliosis” was used only for the PubMed database. The titles and abstracts of studies that were identified in the computerized searches were examined to exclude any articles that were clearly irrelevant. The full text of the remaining articles was retrieved, and each article was read to determine whether it contained information on the actual topic. Studies meeting the inclusion criteria were examined and carefully cross-checked to establish that no overlapping data were presented, thereby to ensure the integrity of the meta-analysis results.

Inclusion criteria for this meta-analysis were the following: AIS patients (1) aged 10–18 years old, (2) with a Cobb angle less than 40°, and (3) none of whom has been treated specifically as orthotics or with electrical stimulation or by surgery.

The expected outcome that we retrieved was the percentage of patients with untreated AIS who experienced an improvement, worsening, or hold steady of their condition at follow-up. When appropriate, confidence intervals (CI) were calculated using exact likelihood. Level of significance was set to two-sided 5%.

Patients

From April 2008 to December 2014, 67 patients affected by severe PE which underwent MIRPE at our Pediatric Surgery Department at Meyer Children's Hospital in Florence were followed up. All patients had a perioperative MRI scan, a two projection chest X-rays both at time of surgery and at 3 years follow-up following Nuss bar removal. Postoperative chest X-rays were taken at the usual 3 months follow-up outpatient check following Nuss bar removal. It is worth to mention that the enrolled patients, who were also affected by AIS, did not follow any rehabilitation program or bracing therapy. Cobb angles were assessed by three independent radiologists by specific software (Adobe Photoshop CC, Adobe^®). A descriptive statistical analysis was performed to summarize the variables of interest. Results for quantitative variables are expressed as mean ± SD. We used a paired sample t-test, with a P value set at .05 for significance, to make a comparison among Cobb angles.

Results

Preliminary searches identified 567 potentially relevant articles from the electronic database (PubMed: n = 331; Cochrane Library: n = 8; and Scopus: n = 228). After exclusion of 194 studies containing overlapping data or appearing in more than one database, 373 articles remained. After screening the titles and abstracts, 311 studies without specific information in AIS natural history were further excluded, as well as 27 studies that do not meet the inclusion criteria. Eight studies were excluded because of congenital scoliosis and 4 others because of concurrent disease (beta-thalassemia, neurofibromatosis, Marfan syndrome, and poliomyelitis). Of the remaining 23 studies, 11 studies were excluded because of data loss, 2 studies because of a long-term follow-up, and 1 of them because it was a trial protocol. Eventually only 9 reports met all the inclusion criteria (Fig. 1): three of these were conducted in Germany,^19–21 while the remaining studies were conducted in the United States,²² Canada,²³ England,²⁴ France,²⁵ Ireland,²⁶ and Denmark.²⁷ A total of 1641 AIS patients were assessed in the meta-analysis. Table 1 highlights the key aspects from each report. Although heterogeneous (I² = 99.5%, P value < .0001), the overall percentage of progression for untreated AIS was 42.5% (95% CI 18.2%; 72.2%) (Fig. 2).

FIG. 1.

Detailed flowchart of the systematic review on “untreated AIS.” AIS, adolescent idiopathic scoliosis.

FIG. 2.

Meta-analysis of nine studies of “untreated AIS.” Outcome is the percentage of patients with untreated AIS who experienced progression. Summary percentage calculated with random effects method. AIS, adolescent idiopathic scoliosis.

Table 1.

Characteristics of Included Studies

Study details	Untreated AIS patients age	Initial Cobb angle		Outcome
Authors, year assessed in each study, n°		(Year)	(Degrees)	Measure
Lonstein and Carlson²²	727	9–15 and more	<29°	Cobb angle ★
Scott and Piggott²⁴	30	17 (in average)	5°−45°	Cobb angle ★
Weiss et al.²¹	43	12–14 and more	5°−30°	Cobb angle ★
Duval-Beaupère²⁵	262	NR	<30°	Cobb angle
Hopf et al.¹⁹	135	NR	5°−30°	Cobb angle
Hansen²⁷	76	10–17	5°−31°	Cobb angle ★
Goldberg et al.²⁶	153	15 (at least)	NR	Cobb angle
Weiss et al.²⁰	179	15 (at least)	33°(in average)	Cobb angle
Coillard et al.²³	36	8–15	15°−30°	Cobb angle ★

★ = calculated on standing anteroposterior or posteroanterior radiographs.

NR, not reported.

Sixty-seven patients affected by severe PE who underwent MIRPE at our Department were followed up. This sample consisted of 56 males (84%) and 11 females (16%), with a mean age at the time of surgery of 16.5 years (range, 12–26 years; SD, 3.2) (Fig. 3a, b). The deformity was deemed severe for 54 patients (81%) and asymmetrical for 39 of them (58%). Haller index ranged from 2.6 to 13 (mean, 5.2; SD, 2.1), while asymmetry index ranged from a minimum of 85 to a maximum of 114.3 (mean, 98.7; SD, 5.8). MIRPE was performed by placing a single bar in 60 patients (89.6%) and two bars in the remaining seven cases. AIS ranged from 10° (which represents the diagnostic cutoff) up to 45° and it was concurrent in 34 patients (51%; 95% CI 32.4%–67.6%) out of the 67 PE treated by MIRPE.

FIG. 3.

Age distribution (a) for the patients who underwent MIRPE (b) for the selected patients which had concurrent AIS. MIRPE, mini-invasive procedure; AIS, adolescent idiopathic scoliosis.

In this group, three of them had a Cobb angle greater than 25°, indicating a moderate degree of AIS.

Considering all the treated patients, the arithmetic mean of Cobb angle values before MIRPE was 10.9°, decreasing to 9.4° (−1.5°) following bar removal (95% CI 0.64–2.44; P value .0011). Among the treated patients, 29 experienced a significant regression of the degree of scoliosis, 17 of which were AIS reverted from mild (Fig. 4). Interestingly enough, among those patients in which Cobb angle was initially below 10° (AIS diagnostic cutoff), 26 out of 33 (79%) displayed an overall improvement. In contrast, the percentage of clinical progression of AIS for our cohort was 4.5% (i.e., 5 out of 67 patients) (95% CI 0.9%–12.5%).

FIG. 4.

Effect of the Nuss procedure on the spinal curvature of pectus excavatum patients. The empty dots represent the measurement of initial Cobb angle while the horizontal dashes represent the Cobb angle measured at 3 years follow-up following Nuss bar removal.

Discussion

In the present study, we demonstrated that patients affected by concurrent scoliosis and PE operated by MIRPE underwent an overall improvement of their scoliotic curvature, over a 3-year follow-up period, following Nuss bar removal.

The first report regarding concomitant PE and scoliosis dates back two decades ago and shows that of a 600 patient series with anterior chest wall deformities, roughly a quarter had a mild scoliosis with an average Cobb angle of 15°. Moreover, 8% of these patients with scoliosis required therapeutic intervention of bracing and/or spinal fusion.²⁸ Subsequent studies reported similar results regarding AIS prevalence in PE patients.^13,14

Among patients who underwent surgical repair of severe PE at our Department, about half of them were diagnosed as AIS with a Cobb angle greater than 10° (range, 10–45°). In addition, 1 of 10 scoliotic patients displayed a moderate degree AIS (Cobb angle greater than 25°).

Wang et al.¹⁵ noticed that 80% of the scoliotic PE patients had the spinal column bent to the right as in leftward concavity, thus hypothesizing a significant role of mechanical factors in concurrent chest wall deformities. In our study, about 60% of our scoliotic patients had a leftward concave spine, while the other 40% had a rightward concave spine. There was no significant difference among the two types of scoliosis.

Few reports are available on estimating the biomechanical effect of bar placement in PE and only one in PE associated with scoliosis. Chang et al. designed a three-dimensional finite element analysis model (FEM) to analyze the distribution of stress and strain induced in the chest wall of PE patients who underwent MIRPE. The simulation results indicated that a high bilateral stress distribution was also found posteriorly in proximity to the vertebral spine from the third to the seventh ribs.²⁹

Nagasao et al. enrolled 25 patients with only asymmetric PE and mild to moderate spine deformity (with a Cobb angle comprised in between 17° and 30°) who underwent the Nuss procedure and used CT scan data to produce FEMs and to simulate each patient's thorax. The underlying hypothesis was that by correcting an asymmetric PE, the spine received a force directed from the side of the anterior wall with concavity to the contralateral side.³⁰ Results from this study allowed to establish that the spinal curvature modifies in response to the placement of the Nuss bar. This transformation allows to bend the spine from the side of major concavity to the side with minor concavity and this improvement is primarily dependent on the preoperative morphologic relationship between the anterior chest wall and the spine.

In addition to that, we tried to evaluate a medium-term effect of bar placement on spine curvature of a PE population, including both symmetric and asymmetric cases, which underwent Nuss procedure at our Pediatric Surgical Center exploiting perioperative and post removal radiological data.

Eventually, we demonstrated in our series that 3 years following Nuss bar placement, the spinal curvature of scoliotic patients undergoes an overall improvement.

The primary aim of conservative management for mild/moderate scoliosis is to stop curvature progression in AIS patients. Guidelines for conservative treatment are based on current information regarding the risk for significant curvature progression in a given period of time obtained by a known formula.³¹ In particular, a positive family history, laxity of skin and joints (connective tissue defect), flattening of the physiological thoracic kyphosis (that impedes an efficient bracing), angle of trunk rotation exceeding 10°, and growth spurt have been suggested as possible determinants of a higher risk of scoliosis progression.

Bunnell reported that the risk of progression at the beginning of puberty is 20% in 10° scoliosis, 60% in 20° scoliosis, and as much as 90% in 30° scoliosis. At the age of peak height growth, the risk of progression is 10%, 30%, and 60%, respectively, whereas in later stages falls down to 2% in 10° scoliosis, 20% and 30%.³²

As reported in our study, most of the treated patients were adolescents with a presumable medium-high risk of progression (Fig. 4).

According to the SOSORT guidelines for conservative management of scoliosis, bracing is recommended for those patients whose progression risk is 60% or above.³¹

We speculated whether the correction of PE, which ideally occurs during adolescence, when the chest is still malleable, hinders an orthotic treatment for the spine.¹⁰ Although this aspect remains beyond the aim of our study, it appears that the positioning of Nuss bar for patients who present concurrent PE and AIS can be considered as continuation of bracing therapy aimed to achieve a more balanced distribution of forces on the spine thus reducing the scoliosis degree.

In conclusion, from our results, we confirmed a relationship between PE and AIS and we demonstrate that MIRPE had a positive effect both on the correction of the anterior chest wall defect and on the spine curvature. Although still to be validated, it seems that MIRPE should be offered during puberty as a timely option for treating PE and reverting mild/moderate scoliosis progression, when concomitant.

Footnotes

Disclosure Statement

No competing financial interests exist.

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