Keywords pectus excavatum - Nuss procedure - thoracic cage - cirtometry - 6-minute walk test
Introduction
Pectus excavatum (PE), also known as funnel chest, is the most common congenital deformity
of the anterior thoracic wall, and is caused by the overgrowth of the costal cartilage.
PE is predominantly observed at birth but might also become apparent at puberty.[1 ] As the child reaches puberty, symptoms of cardiopulmonary compression may be present,
including palpitation, chest discomfort, and exercise intolerance. Thus, recently,
PE has been considered not only as a cosmetic issue but also as a physiological concern,
especially in adult patients.[2 ]
[3 ]
[4 ] In 1998, Nuss et al documented a minimally invasive surgery for the correction of
PE, with good clinical results. This procedure involves placing one or more prebent
stainless steel bars underneath the concave part of the chest wall, without resection
of the cartilage, so as to push the anterior chest wall outward and, thus, remodel
the deformity.[5 ]
The effects of the Nuss correction on cardiopulmonary function have been discussed
in previous studies.[6 ]
[7 ]
[8 ]
[9 ] However, the effects of the procedure on the dynamics of the thoracic cage, which
is associated with exercise capacity, are unclear. Thoracic cirtometry, also known
as thoracoabdominal perimeter measurement, is a relatively simple and inexpensive
method to provide reliable and repeatable measures of the range of movement of the
chest wall from end-point inspiration to end-point expiration.[10 ]
[11 ] Additionally, the 6-minute walk test (6MWT), a practical physiological test, provides
an assessment of cardiopulmonary function after thoracic surgery that is reproducible,
standardized, and reliable.[12 ]
[13 ] Our aim in this study was to use cirtometry to quantify the changes in the dynamics
of the thoracic cage after Nuss correction for PE and to evaluate the association
between changes in thoracic cage dynamics and exercise capacity, measured using the
6MWT.
Materials and Methods
Participants
A prospective observational study was conducted, comprising adult patients diagnosed
with PE who were scheduled for a Nuss procedure for the correction of PE at the Taipei
Chi-Tzu Hospital in New Taipei city, Taiwan, between September 2016 and August 2017.
Preoperative assessments included a complete history, physical examination, chest
radiography, electrocardiography, pulmonary function test, echocardiography, and computed
tomography (CT) of the chest. Age, height, body weight, body mass index (BMI), the
Haller index (ratio of the transverse thoracic dimension to the sternovertebral dimension
at the most depressed point detected on CT of the chest as previously described[14 ]), sternovertebral distance (SVD) on lateral chest radiographs,[15 ] and postoperative data were recorded.
Indications for surgical repair followed the criteria described by Nuss and Kelly.[2 ] The surgical technique, a bilateral thoracoscopy-assisted Nuss procedure, was performed
as previously described.[16 ] All patients underwent portable chest radiography and were intensively monitored
for 24 hours postoperatively. Postoperative pain was controlled using fentanyl, administered
via patient-controlled epidural analgesia. Nonsteroidal antiinflammatory drugs were
also provided for pain relief. Patients were discharged from the hospital once the
pain was controlled using only oral analgesics. All patients were followed up at 1,
3, and 6 months after surgery and annually thereafter. All patients were discouraged
from performing deep breathing exercise after the surgery and resumed normal exercise
3 months after surgery.
This study was approved by our ethics committee and Institutional Review Board (IRB:
TTCH-IRB no.: 05-X17-070), and all patients provided informed consent. Patients were
excluded from the analysis if they had major complications (e.g., hemothorax, pleural
effusion, or bar flipping requiring surgical revision) or were lost to follow-up.
Cirtometry and Exercise Capacity
Detailed instructions regarding the outcome measures were provided to each participant,
including a demonstration prior to measurement.
Different cirtometry methods have been described in the literature; in this study,
we used the standardized protocol reported by Caldeira et al.[11 ] Measurements were performed by an experienced senior physician (Y.L.C.). All baseline
measurements were obtained with the patient standing upright, with arms extended alongside
the trunk and the chest uncovered. Using a conventional measuring tape (cm), the circumference
of the chest wall was measured at the axillary level (AL) and xiphoid level (XL),
using the axillary fold and xyphoid process as anatomical landmarks, respectively
([Fig. 1A ], [B ]). During the measurement, considerable care was taken to pull the tape snuggly,
but not too tightly, so as to not alter the soft tissue contours. Three measurements
were obtained at each level for both inspiration and expiration. At each level, the
measurements were performed on maximal inspiration and maximal expiration during separate
breaths, with a 1-minute interval between each measurement. Patients were asked to
maintain maximal inspiration/expiration status for more than 2 seconds to allow the
measurements to be completed. The mean values of the three measurements were recorded
by a third observer to ensure blinding. The assessor was also blinded when analyzing
the results. All patients were evaluated at four specific time points: preoperatively
and at 1, 3, and 6 months after surgery.
Fig. 1 Illustration of measurements on chest circumferences (cirtometry). (A) Level on axillary
fold (AL) and (B) level on xyphoid process (XL).
The 6MWT was used to evaluate functional exercise capacity before and after surgical
correction. The 6MWT was performed as per the guidelines of the American Thoracic
Society.[13 ] The BMI was obtained at the time of the 6MWT, and pain score was measured using
a 10-cm visual analog scale (VAS) measured at the end of the 6MWT. Finally, the correlation
between the 6MWT data (time, BMI, and VAS) and cirtometry was analyzed.
Statistical Analysis
For continuous variables, descriptive data are expressed as means ± standard deviation
(SD) and the Student's t -test used to compare postoperative and preoperative values. For categorical variables,
the chi-square or Fisher's exact test was used to compare postoperative and preoperative
values, as appropriate for the data type. Pearson's correlation coefficient was calculated
to evaluate the relationship between cirtometry and 6MWT data (time, BMI, and VAS).
A p -value of less than 0.01 was considered significant. Statistical analyses were performed
using SPSS software (version 24; SPSS; Chicago, Illinois, United States).
Results
Clinical Characteristics and Surgical Outcomes
Initially, 55 patients were enrolled into the study, with 9 patients excluded from
the analysis due to pleural effusion (n = 2), flipping of the inserted metal bar (n = 1), and incomplete data or loss to follow-up (n = 6). Therefore, the data from 46 patients (43 men and 3 women), with a mean age
of 26.2 years (range, 18–55 years), were included in the analysis. An overview of
their demographic features and postoperative results is provided in [Table 1 ] and [Fig. 2 ]. The mean SVD after postoperative follow-up with mean of 16.7 months (12–24 months)
showed significant improving compared with that before surgery (9.6 ± 1.4 vs. 7.2 ± 1.3
cm, p < 0.01).
Fig. 2 Lateral chest plain films of a 21-year-old man before and 12 months after Nuss procedure.
Three bars were placed into the thoracic cage. Sternovertebral distance was measured
as demonstrated using yellow lines. The correction of chest wall deformity was evident.
Table 1
Demographic variables and postoperative characteristics of 46 adults with PE corrected
by Nuss procedure
Characteristics
All patients
Age, y, mean ± SD
26.2 ± 8.6
Gender (M:F)
43:3
Body height, cm, mean ± SD
174.3 ± 6.6
Body weight, kg, mean ± SD
58.5 ± 7.7
Body mass index, kg/m2 , mean ± SD
19.2 ± 1.9
Haller index, mean ± SD
4.2 ± 0.9
Preoperative SVD[a ], cm, mean ± SD
7.2 ± 1.3
Bar number placed, No. (%)
Single
6 (13.0)
Double
37 (80.4)
Three
3 (6.5)
Operation time, min, mean ± SD
81.8 ± 19.7
Estimated blood loss, mL, mean ± SD
14.3 ± 2.6
Blood transfusion, No. (%)
0 (0)
Mortality, No. (%)
0 (0)
Length of stay, d, mean ± SD
6.7 ± 2.4
Postoperative SVD[b ], cm, mean ± SD
9.6 ± 1.4
Abbreviations: PE, pectus excavatum; SD, standard deviation; SVD, sternovertebral
distance.
a Sternovertebral distance, measured on lateral chest radiograph on deep breath.
b After postoperative follow-up with mean of 16.7 months (12–24 months).
Circumferential Measurements by Cirtometry
Chest wall circumference measures at the AL and XL, before and after the Nuss procedure,
are summarized in [Fig. 3A ], [B ]. The maximal inspiration circumference increased after surgery (p < 0.01) from baseline values prior to surgery, at both the AL and XL, respectively,
as follows: prior to surgery (84.5 ± 4.9 and 80.1 ± 4.8 cm) and postsurgery at 1 month
(86.6 ± 5.0 and 81.6 ± 4.7 cm), 3 months (88.5 ± 5.1 and 83.7 ± 5.1 cm), and 6 months
(88.9 ± 4.7 and 84.3 ± 4.8 cm). At both the AL and XL, measures at 3 and 6 months
after surgery were not significantly different (p > 0.01). A similar pattern of increase in the chest wall circumference was identified
for maximal expiration at both the AL and XL (p < 0.01), respectively, as follows: prior to surgery (79.9 ± 5.2 and 74.2 ± 5.0 cm)
and postsurgery at 1 month (81.9 ± 5.6 and 76.7 ± 5.5 cm), 3 months (83.3 ± 5.0 and
78.2 ± 5.1 cm), and 6 months (83.5 ± 5.0 and 78.3 ± 5.1 cm). At both the AL and XL,
measures at 3 and 6 months after surgery were not significantly different (p > 0.01).
Fig. 3 Changes in chest wall circumference at the (A) axillary and (B) xyphoid levels at
four time points: preoperatively and at 1, 3, and 6 months after surgery on maximal
inspiration (right) and maximal expiration (left). The minimum, first quartile (Q1),
median, third quartile (Q3), and maximum values are presented in box-and-whisker plots;
actual measurements are marked on the plots and annotated under the figures. *p < 0.01, **p ≥ 0.01. mon, month; preop, before surgery; postop, after surgery.
Exercise/Fitness Capacity
The BMI was assessed at each follow-up visit after surgery, calculated after removing
the weight of the inserted bar(s) (0.4 kg/bar), with no difference between the pre-
and postoperative BMI values (p > 0.01).
The results of the 6MWT are shown in [Fig. 4 ]. Compared with that before surgery (545.8 ± 65.0 m), the maximum walking distance
improved at 3 months (627.8 ± 61.5 m, p < 0.001) and 6 months after surgery (658.5 ± 52.8 m, p < 0.001), but was not significantly different at 1 month after surgery (535.7 ± 94.9
m, p = 0.396). Furthermore, the maximum walking distance was significantly different between
1 and 3 months after surgery (p < 0.001), and between 3 and 6 months after surgery (p < 0.001).
Fig. 4 A box-and-whisker plot of the walking distance, measured using the 6-minute walk
test (6MWT), before surgery and at 1, 3, and 6 months after surgery. The minimum,
first quartile (Q1), median, third quartile (Q3), and maximum values are marked on
the plots and annotated under the figures. *p < 0.01, **p ≥ 0.01. mon, month; preop, before surgery; postop, after surgery.
Correlation between the Chest Wall Circumference and the 6MWT
Significant correlations between the improvement in chest wall circumference on maximal
inspiration and the 6MWT result were identified at the AL and XL (Pearson's correlation
coefficient, 0.8424 and 0.7951, respectively). These positive correlations support
an association between increased exercise capacity and an increased expansion of the
anterior chest wall after Nuss correction in adults with PE.
Discussion
The present study demonstrated that improved dynamics of the thoracic cage were achieved
after Nuss repair for PE in adults. Generally, patients with PE undergo surgical correction
to improve cosmetic, psychosocial, and/or physiological concerns.[2 ]
[3 ]
[4 ] The Nuss repair is a minimally invasive technique for PE correction.[5 ] After its introduction in 1998, Nuss correction became widely accepted and popular,
as it required minimal resection while providing good cosmetic and functional results.[2 ]
[7 ]
[8 ]
[9 ] Originally, the Nuss procedure was developed primarily for the correction of PE
in prepubertal children, with an optimal age for correction of 12 to 16 years.[5 ]
[17 ] However, recent studies have also demonstrated satisfactory outcomes of this procedure
for correction of PE in adults, regardless of age.[4 ]
[16 ]
[17 ]
[18 ]
Morphological changes in the thoracic cage, after the Nuss procedure, have been previously
evaluated using chest imaging (CT or radiography)[18 ]
[19 ]
[20 ]
[21 ] and optoelectronic plethysmography.[22 ]
[23 ] These studies demonstrated an increase in the volume of the thoracic cage or static
lung volume after surgical correction. In the present study, we also evaluated radiological
changes of chest wall after surgical repair using SVD measured by lateral chest radiographs.
The results showed a significant increase after Nuss procedure.
However, the effect of the correction on the dynamics of the thoracic cage during
inspiration and expiration had not been well characterized to date. In 1972, Moll
and Wright demonstrated the reliability of measuring chest expansion using a measuring
tape (cm) in an objective clinical study.[24 ] Since its introduction, this technique has been described as cirtometry or thoracoabdominal
measurement by some academics, and has been used to quantify the mobility of the chest
wall.[10 ]
[11 ] The information of key studies concerning cirtometry is summarized in [Table 2 ]. Cirtometry plays an important role in the assessment of patients with a variety
of disease conditions, such as ankylosing spondylitis, asthma, and chronic obstructive
pulmonary disease, as well as to investigate the effects of physical treatments designed
to improve respiratory function.[25 ]
[26 ]
[27 ]
[28 ] The intra- and interrater reliabilities and reproducibility of thoracoabdominal
measurements in patients with various diseases have been reported to be fair to good,
with greater variability for interrater measurements.[10 ] Based on this evidence, all cirtometry measurements in the present study were obtained
by one experienced rater, with the rater blinded to clinical and 6MWT data.
Table 2
Summary of key studies concerning cirtometry on clinical disorders
Study
Objective
Results and conclusions
Debouche et al (2016)[10 ]
1. Assessing the reliability and reproducibility of chest wall expansion measurement
in young healthy adults
2. Examine the correlation between upper and lower chest expansion measurements and
lung function
1. Good intra- and interrater reliabilities and reproducibility were found in either
upper or lower chest wall expansion measurement
2. Both upper and lower chest wall measurements were correlated with pulmonary function,
but upper measurements may be more useful
Caldeira et al (2007)[11 ]
1. To examine the intra- and interrater reliabilities
2. Correlation between cirtometry and pulmonary volumes measured by respiratory inductive
plethysmography
1. Intrarater reliability was satisfactory, but significant differences were noted
in all sets of interrater measurements
2. Cirtometry does not accurately reflects lung volumes
Moll and Wright (1972)[24 ]
1. To determine the normal range of cheat wall movement
2. To evaluate the effect of different diseases on chest expansion, including ankylosing
spondylitis, chronic chest disease, and obesity
1. A wide scatter of normal values was observed at all decades and showed wide variation
with age and sex
2. Circumferential measurement alone would be adequate for usual purposes
Grubisić et al (2014)[25 ]
To determine the relationship between the bone mineral density, spinal mobility, and
chest expansion index in patients with ankylosing spondylitis
Thoracic and lumbar spine mobility and chest expansion index decreased in patients
with lower bone mineral density in lumbar and hip region
Johansson et al (2012)[26 ]
Comparing chest mobility, respiratory movement, and pain sensitivity in SHR patients
with patients with asthma, COPD, and alleged healthy control subjects
SHR patients demonstrated signs of dysfunctional breathing and seemed to be most similar
to patients with COPD group except for lung function
Malaguti et al (2009)[27 ]
1. Evaluating the reliability and accuracy of cirtometry
2. Investigating the relationship between chest wall mobility and inspiratory capacity
in patients with COPD
1. High reliability of intra- and interobserver measurements
2. An association between inspiratory capacity and chest measurements at the abdominal
level was found, but the results showed no correlation between chest wall mobility
and pulmonary function
Abbreviations: COPD, chronic obstructive pulmonary disease; SHR, sensory hyperreactivity.
Numerous studies have investigated changes in lung volume and pulmonary function after
the Nuss procedure, with controversial results.[8 ]
[22 ]
[29 ] However, in our clinical experience, most patients cannot complete standard pulmonary
spirometry and cardiopulmonary exercise testing (CPET) after the Nuss procedure, due
to pain that can persist up to 3 months after surgery. Thus, the use of pulmonary
spirometry and CPET data might not be suitable for repeated follow-up, especially
in the early postoperative period. For these reasons, the 6MWT, which was used in
the present study, would provide a more suitable proxy measure of the change in exercise
capacity, before and after the surgery. The maximal walking distance in 6 minutes
has been previously used as a reliable measure of the effect of new therapies or interventions
on exercise capacity.[12 ]
[13 ]
In the present study, we identified a significant improvement in the excursion of
the thoracic cage by 1 month after Nuss correction for PE in adults, with improvement
stabilizing at 3 months after surgery. The increase in thoracic volume at 3 months
postsurgery was associated with an increase in the maximal walking distance on the
6MWT. The lack of improvement in the maximal walking distance at 1 month after surgery
likely results from early postoperative pain. All observed increases in postoperative
chest wall excursion (at both the AL and XL and at the end points of both inspiration
and expiration) were correlated with the increase in the maximum walking distance
(all Pearson's correlation coefficients > 0.7). Therefore, the increase in chest wall
circumference reflects the increase in functional exercise capacity, with both cirtometry
and the 6MWT providing simple and reliable ways for surgeons to monitor the clinical
and functional outcomes of patients undergoing a Nuss procedure.
The limitations of the present study should be acknowledged. Foremost, the number
of patients was relatively small. Thus, further studies with larger numbers of patients
and subgroup analyses are needed to confirm our findings. Furthermore, we only selected
adults for evaluation because possible skeletal growth may occur in younger patients.
Additionally, further studies on the changes in chest wall mobility and physiological
benefits of the Nuss procedure in patients with PE are needed after the removal of
the stainless steel bar(s).
In conclusion, cirtometry is a simple, readily available, and replicable method to
evaluate changes in chest wall dynamics after Nuss correction of PE in adults. The
chest wall circumference at different levels significantly improved after surgery,
with the improvement in chest excursion stabilizing at 3 months after surgery. This
postcorrection improvement in chest wall mobility was highly correlated with exercise
capacity. Future studies should evaluate the maintenance of benefits after the removal
of the supporting bar(s).
