Abstract
Background and Aims:
We performed thoracoscopic costal cartilage excision (TCCE) combined with the Nuss procedure to correct asymmetrical pectus excavatum (PE). We reviewed the efficacy of combined TCCE and Nuss procedure for asymmetric PE.
Patients and Methods:
Overall, 8 patients with asymmetrical PE underwent TCCE with the Nuss procedure. The Haller index, asymmetry index, and angle of sternal rotation were calculated using preoperative computed tomography. The procedure was performed using bilateral 2.5-cm incisions at the same level of the deepest chest wall depression. The most depressed three to four costal cartilages were partially resected through a right mini-thoracotomy. Subsequently, one or two titanium bars were implanted and secured with stabilizers. The cosmetic outcome was evaluated on the following four ratings: excellent, good, fair, and failure ( = recurrence).
Results:
The median age at surgery was 14.5 years (8–20 years). The number of bars was one in 3 cases and two in 5 cases. The preoperative Haller index, asymmetry index, and angle of sternal rotation were 4.3 (3.5–5.9), 1.15 (1.04–1.26), and 21.5° (15°–31°), respectively; 2 patients had scoliosis before the Nuss procedure. Complications included surgical site infection and hemothorax. Median follow-up time was 25.5 months (3–63). Bars were removed in 3 patients, 3 years postoperatively. Cosmetic results were excellent, 4; good, 2; fair, 1; failure, 1. Both patients with scoliosis had poor outcomes (fair, 1; failure, 1).
Conclusions:
Combined TCCE with Nuss procedure is considered safe and effective for patients with asymmetrical PE. Careful long-term follow-up is required, especially in cases with scoliosis.
Introduction
Pectus excavatum (PE) is the most common chest wall deformity. It affects ∼1 to 8 per 1,000 live births. 1 Several techniques have been used to correct this deformity. The Ravitch repair (described in 1949) was one of the most common procedures, involving complete cartilage excision and sternal osteotomy. 2 In 1998, a novel minimally invasive technique that uses small incisions on the lateral region of the chest wall was introduced by Nuss et al. 3 To date, the Nuss procedure has been widely applied as a minimally invasive operation for PE. However, a meta-analysis between the Nuss and Ravitch procedures showed no differences with respect to overall complications, length of hospital stay, and patient satisfaction. 4 A study comparing different age groups of the Nuss procedure suggests that it is highly recommended for pediatric patients; longer operation time and higher incidence of complications require careful adult patient selection. 5
Adult patients often present with asymmetrical PE, which is associated with various degrees of sternal torsion. Lollert et al. reported that 32/69 patients with PE (median age: 15 years; range: 5–35) had asymmetrical deformity; as the age of patients progressed, angle of sternal rotation increased. 6 Yoshida et al. also reported that half of patients over the age of 13 years showed moderate or severe asymmetry. 7 Although the Nuss procedure is a widely known standard treatment option for PE, surgical procedures for asymmetrical PE remain controversial. It has been reported that sternochondroplasty (SCP), which includes subperichondrial resection of the cartilage, anterior sternal osteotomy, and metal plate placement to support the sternum, yielded better results than the Nuss procedure in patients with asymmetrical PE. 8 Conversely, a report has mentioned that the Nuss procedure could be performed for asymmetrical PE, by changing the shape of the bar. 9
Since the Nuss procedure can be performed with minimal skin incisions and short operation time, our first-line treatment for PE is the Nuss procedure for adolescents and young adults. Therefore, we added thoracoscopic costal cartilage excision (TCCE) to the Nuss procedure to extend its indications for asymmetric cases. Herein, we report the results of our procedure.
Patients and Methods
Patients with asymmetric PE who underwent TCCE and Nuss procedure over the last 5 years were retrospectively reviewed. The PE repair was indicated for patients who were physically or psychologically symptomatic. Preoperative CT scans were obtained, and the Haller index was calculated as the inner transverse thoracic diameter divided by the anteroposterior distance between the anterior thoracic wall and the spine at the narrowest point. 10 In addition, the most prominent twist was selected in the CT scan slice, and the angle of sternal rotation against the horizontal line was measured. The asymmetry index was calculated in the same slice (Fig. 1). The asymmetric index, which was slightly modified from the original one, was calculated determining the largest anteroposterior diameter of the left and right hemithorax, dividing the left measurement by the right 11 ; TCCE was indicated for patients with a rotation angle ≧15°. We assessed the deformity using these indices, surgical outcomes, and complications related to the operation. The cosmetic outcome was objectively evaluated by the surgeons at the last hospital visit, according to the previously reported rating scale 12 as follows:

The sternal rotation angle against the horizontal line (a) was measured on the most prominent twist in the CT scans. In the same slice, asymmetric index (c/b) was measured.
excellent: normal chest morphology
good: slight residual depression or curvature of the lower sternum; hypertrophic or keloid scar
fair: residual depression, with nevertheless more than 50% improvement, compared to the initial presentation
failure: complete recurrence.
This study was reviewed and approved by the institutional review board of our institute (16373-4).
TCCE surgical procedure
Details of TCCE procedure are as follows: The patient was placed in the supine position. The procedure was performed through bilateral 2.5–3-cm incisions at the same level of the deepest chest wall depression. Through a right mini-thoracotomy using the same lateral skin incision, the most depressed three to four costal cartilages were partially excised in a wedge shape, to avoid damage to the internal thoracic artery and intercostal vessels under thoracoscopic vision, using electrocautery forceps for osteotomy (Fig. 2). Pneumothorax (4–6 mmHg) was obtained using the LAP Protector (Hakko Co., Ltd. Medical Device Division, Tokyo) and EZ Access (Hakko Co., Ltd.) devices. After cartilage excision, the sternum was raised with the introducer. It was confirmed that sufficient excision was obtained when symmetry was obtained. Once sufficient excision was achieved, meticulous hemostasis was performed. An introducer was entered into the right thoracic cavity through the top of the right chest wall at the level, and retrosternal tunneling was performed by keeping the introducer in contact with the sternum and sternocostal cartilages. The introducer was passed in the left thoracic cavity (confirmed by left thoracoscopy) and exited the left thoracic wall, at the top of left chest wall. A guide was passed through, followed by the bent titanium bars; one or two bars were implanted and secured with stabilizers. A right-sided chest drainage tube was placed after careful hemostasis. The bars stayed in place for 3 years.

The most depressed three to four costal cartilages were partially resected under thoracoscopic vision.
Statistical analyses
The numerical values were shown as medians with their interquartile ranges. Correlation between the angle of sternal rotation and asymmetry index/Haller index was analyzed by a linear regression analysis. Statistical analyses were performed using JMP® Pro 14.0.0 (SAS Institute, Cary, NC); P < .05 was considered statistically significant.
Results
A total of 8 patients with asymmetric PE underwent TCCE and the Nuss procedure. Preoperative data of the 8 patients are shown in Table 1. The median age at surgery was 14.5 years (13–16.5 years). The sex ratio (male/female) was 3/5. The preoperative Haller and asymmetric indices and angle of sternal rotation were 4.3 (3.7–5.2), 1.15 (1.05–1.22), and 21.5° (15.5–29.5°), respectively. The angle of sternal rotation correlated well with the asymmetry index (R 2 = 0.6823, P = .015), but not with the Haller index (Fig. 3); 2 patients had scoliosis, and 1 of them underwent surgery for scoliosis before the Nuss procedure.

The angle of sternal rotation correlated well with the asymmetric index (R 2 = 0.6823, P = .015), but not with the Haller index.
Preoperative Patients' Data
Surgical outcomes are shown in Table 2.
Operative Outcomes
The most depressed three to four costal cartilages were partially excised. The number of bars was one in 3 cases and two in 5 cases. The median operative time and blood loss were 173.5 minutes (147–197 minutes) and 17.5 mL (0–50 mL), respectively. The median postoperative hospital stay was 8.0 days (8.0–12.8 days). In 3 cases, the bar was removed 3 years postoperatively (cases 1–3). No deaths were reported. Complications included surgical site infection in one case (treated conservatively) and hemothorax in one case. In the patient with hemothorax, thoracoscopic hemostasis was performed the next day. Oozing from the stump of the chondrocyte was observed, and hemostasis was performed under electrocautery. Postoperative course of the second operation was smooth. Median follow-up time was 25.5 months (9.3–45.8 months). Cosmetic results were excellent, 4; good, 2; fair, 1; and failure, 1. Both patients with scoliosis had poorer outcomes (case 2: failed, case 8: fair). In these 2 cases, thorax deformity progressed with scoliosis, even after the Nuss procedure. In 1 case (case 2) where the bar was removed, the deformity returned to the asymmetric PE (preoperative state).
Figure 4 shows the pre- and postoperative chest wall in case 4. A symmetric rib cage was obtained postoperatively.

The pre- and postoperative chest wall in case 4. A symmetric chest cage was obtained postoperatively.
Discussion
Correction of the asymmetric type of PE with the Nuss procedure is challenging, since the standard Nuss procedure alone cannot always correct the asymmetry. While the Nuss procedure can correct the depressed deformity by bar placement, asymmetrical protrusions may occur due to the remaining sternal torsion. In our experience, there are several patients in whom exaggerated growth of the costal cartilage in the hemithorax later developed into asymmetrical pectus carinatum.
In addition, asymmetric PE had poorer preoperative lung volumes and poorer postoperative pulmonary function, with significantly lower peak expiratory flow, compared to the symmetric type cases. 13 Therefore, correction of asymmetry may be important for pulmonary function, as well as from an esthetic point of view. In patients with asymmetric PE, lung function should carefully be followed up until bar removal.
In this study, the angle of sternal rotation and asymmetry index were used as preoperative asymmetry indices. Since our data showed that these two indices were well correlated, both seemed to be useful for evaluating the asymmetric deformity. Conversely, the Haller index was not correlated with the angle of sternal rotation. Since asymmetry is not always related to the degree of the depression, it is essential to combine the Nuss procedure with a technique that can mainly correct the asymmetry.
Dzielicki et al. reported the results of 461 patients who underwent the Nuss procedure. They concluded that better clinical results are achievable in patients under 12 years of age with a symmetric deformity and that, in older patients (over 15 years of age) with an asymmetric deformity, additional procedures (including transverse sternotomy and limited costal cartilage excision) are required to achieve a comprehensive correction of the deformity. 14 Kabbaja et al. reported that an angle of sternal rotation >35° is a contraindication to thoracoscopic PE repair and that SCP is recommended instead. 15 Coelho et al. also reported that SCP is preferred over the Nuss procedure for asymmetric deformity. 8 According to these previous reports, the Nuss procedure alone is not recommended for patients with severe asymmetric deformities.
Conversely, Park et al. reported that the Nuss procedure, a morphology-tailored technique, performed on a large sample (n = 1170) was effective for asymmetrical PE using asymmetric bars. 9 As all pectus repairs were performed by a single surgeon, extensive experiences seemed to be required to obtain a satisfactory outcome of the morphology-tailored technique.
Park et al. reported that overgrowth of cartilage is not the main factor responsible for asymmetric PE, and it could instead be related to abnormal rib growth. 16 Therefore, the purpose of TCCE is not to shorten the costal cartilage, but to make it easier to correct sternum twist by removing the costal cartilage in a wedge shape. Since our procedure uses a symmetric bar, as in the standard Nuss procedure, it seems to be possible to perform surgery without extensive experience on asymmetric cases; TCCE combined with the Nuss procedure may potentially become a standard treatment option for asymmetric cases.
Our procedure has several limitations. Although the asymmetrical deformities were well corrected in 6 patients without scoliosis, esthetic results were not satisfactory (fair, 1; failure, 1) in 2 patients with scoliosis. In the failed case, since reoperation was not desired, an injection of adipose tissue into the recess was performed. Nagasao et al. reported that performance of the Nuss procedure for asymmetric PE exerts dynamic influence on the spine, and response patterns of the spine are predictable from morphological relationships between the asymmetric patterns of the anterior thoracic wall and spine. 17 We should be cautious when we perform the Nuss procedure on patients with scoliosis. Kabbaja et al. reported that an angle of sternal rotation >35° is a contraindication to thoracoscopic PE. 13 As the maximum rotation angle in our series was 31°, it is unknown whether our procedure is effective for asymmetric cases in which the rotation angle is >35°.
A major limitation of this study is that the follow-up period was not long enough to evaluate the long-term outcomes. The bars were removed in 3 cases. However, the long-term results after bar removal in 2 patients without scoliosis were good. This fact suggests that the long-term results of TCCE combined with the Nuss procedure are expected to be as good as those of the standard Nuss procedure.
In conclusion, TCCE in combination with the Nuss procedure may yield better results than the standard Nuss procedure in patients with asymmetric PE. Careful long-term follow-up is required, especially for cases with scoliosis.
Footnotes
Acknowledgment
The authors thank Editage for English language editing.
Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
