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Optoelectronic plethysmography demonstrates abrogation of regional chest wall motion dysfunction in patients with pectus excavatum after Nuss repair

      Abstract

      Purpose

      We previously demonstrated that patients with pectus excavatum (PE) have significantly decreased chest wall motion at the pectus defect compared with the rest of the chest vs unaffected individuals and use abdominal respiratory contributions to compensate for decreased upper chest wall motion. We hypothesize that PE repair will reverse chest wall motion dysfunction.

      Methods

      A prospective, institutional review board–approved study compared patients with PE before and after Nuss repair. Informed consent was obtained before motion analysis. Sixty-four patients with uncorrected PE ages 10 to 21 years underwent optoelectronic plethysmography analysis. Repeat analysis was performed in 42 patients 6 months postoperative (PO).

      Results

      Volume of the chest wall and its subdivisions were calculated. Total chest wall volume at rest was significantly increased after repair and in each thoracic compartment. PO patients developed increased midline marker excursion at the pectus defect and significantly decreased excursion at the level of the umbilicus.

      Conclusions

      Optoelectronic plethysmography kinematic analysis demonstrates that chest wall remodeling during Nuss repair results in increased thoracic volume. Chest wall motion dysfunction at the pectus defect is reversed after Nuss repair. Abdominal respiratory contributions are also markedly decreased. These findings may help to explain why patients with PE report an improvement in endurance after the Nuss procedure.

      Key words

      Pectus excavatum (PE) accounts for 87% of chest wall deformities [
      • Goretsky M.J.
      • Kelly R.E.
      • Croitoru D.P.
      • et al.
      Chest wall anomalies: pectus excavatum and pectus carinatum.
      ]. More than a cosmetic defect, this chest malformation is known to be associated with symptoms of shortness of breath, lack of endurance, and exercise intolerance related to the degree of cardiac and pulmonary compression [
      • Kelly R.E.
      • Cash T.F.
      • Shamberger R.C.
      • et al.
      Surgical repair of pectus excavatum markedly improves body image and perceived ability for physical activity: multicenter study.
      ]. Patients with PE have been shown to compensate for decreased upper chest wall expansion by increasing the diaphragmatic component of their respiration [
      • Goretsky M.J.
      • Kelly R.E.
      • Croitoru D.P.
      • et al.
      Chest wall anomalies: pectus excavatum and pectus carinatum.
      ]. In severe cases, apparent paradoxical respiration at the pectus defect can be observed.
      A multicenter study of PE initiated by our institution has demonstrated that surgical repair of PE significantly improves the perceived limitations on physical activity experienced by affected individuals. Efforts to elucidate the cause of exercise intolerance have largely included studies of pulmonary function, namely, spirometry. We have previously described that patients with uncorrected PE have decreased formal pulmonary function test (PFT) values relative to unaffected individuals, with forced vital capacity and forced expiratory volume in 1 second, percent predicted values being 13% lower than population means [
      • Lawson M.L.
      • Mellins R.B.
      • Tabangin M.
      • et al.
      Impact of pectus excavatum on pulmonary function before and after repair with the Nuss procedure.
      ]. However, only small increases in formal PFT values have been demonstrated after Nuss repair [
      • Lawson M.L.
      • Mellins R.B.
      • Tabangin M.
      • et al.
      Impact of pectus excavatum on pulmonary function before and after repair with the Nuss procedure.
      ,
      • Xiao-ping J.
      • Ting-ze H.
      • Wen-ving L.
      • et al.
      Pulmonary function for pectus excavatum at long-term follow-up.
      ]. The lack of correlation between formal PFT results and perceived increases in exercise tolerance reported by the postoperative patients with PE indicates the need for novel objective modalities of cardiopulmonary function be applied to this patient population.
      Noninvasive optoelectronic plethysmography (OEP) is an optical reflectance system that measures chest wall volume changes. This motion analysis technology measures absolute volume of the chest wall and variations of its subcompartments: the pulmonary rib cage, abdominal rib cage, and abdomen segments [
      • Aliverti A.
      • Dellacà R.
      • Pelosi P.
      • et al.
      Compartmental analysis of breathing in the supine and prone positions by optoelectronic plethysmography.
      ]. We have previously applied OEP to patients with PE and demonstrated significantly decreased chest wall motion at the area of the pectus defect during respiration compared with unaffected individuals. Patients with PE concurrently exhibit a significant increase in abdominal contributions to respiration, which likely is an attempt at compensation for the dysfunction of the upper chest wall motion [

      Redlinger RE Jr, Kelly RE, Nuss D, et al. Regional chest wall motion dysfunction in pectus excavatum patients demonstrated via opto-electronic plethysmography (OEP). J Pediatr Surg (in press).

      ,
      • Cala S.J.
      • Kenyon C.M.
      • Ferrigno G.
      • et al.
      Chest wall and lung volume estimation by optical reflectance motion analysis.
      ]. The aim of this study was to demonstrate improvement in chest wall motion and thoracic volumes after the minimally invasive Nuss repair through the use of OEP motion analysis.

      1. Methods

      1.1 Subjects

      A prospective, institutional review board–approved study compared patients before and after Nuss repair. Sixty-four patients with uncorrected PE underwent OEP analysis, 42 of which underwent a repeat analysis 6 months postoperatively. Fifty-five unaffected control patients (C) also underwent analysis. All subjects were between the ages of 10 and 21 years. Patients with any major medical condition impairing participation, including neurologic and cardiopulmonary diseases, were excluded. In addition, those with any prior chest or upper abdominal surgery; diaphragmatic surgery, injury, or paralysis; or pregnancy were also excluded from the study. Informed consent to include demographic, preoperative information, and OEP kinematic data for our OEP database was obtained. The informed consent follows the human experimental guidelines of the US Department of Health and Human Services and has the approval of Eastern Virginia Medical School's Institutional Review Board (08-05-EX-0101).

      1.2 Optoelectronic plethysmography

      Each consenting subject was studied using OEP. Seventy-nine hemispherical and 10 spherical reflective markers were attached to the patient's thorax using bioadhesive hypoallergic tape. Forty-two anterior, 37 posterior, and 10 lateral markers were arranged circumferentially, along anatomical thoracic landmarks: clavicle, manubriosternal angle, nipple line, xiphoid, lower costal margin, umbilicus, and anterior superior iliac spine [

      Fermi E, Aliverti A. Optoelectronic plethysmography compendium marker setup revision 3, BTS S.p.A.

      ,
      • Dellaca
      • Aliverti A.
      • Pelosi P.
      • et al.
      Estimation of end-expiratory lung volume variations by optoelectronic plethysmography.
      ] (Fig. 1). Vertically, the markers were arranged along the anterior axillary lines, mid clavicular lines, and the midline [

      Fermi E, Aliverti A. Optoelectronic plethysmography compendium marker setup revision 3, BTS S.p.A.

      ]. Eight infrared cameras, operating at 120 Hz, tracked the displacement of the markers during deep breathing exercises. Standing at rest, subjects performed the following respiratory maneuvers in sequence: (1) 3 normal quiet breaths; (2) 3 breaths with slow maximal inhalation, held for 1 second, followed by slow maximal exhalation; and (3) 3 breaths with slow maximal inhalation, followed by forceful maximal exhalation. All scans were performed in the motion analysis laboratory within the Pectus Clinic at the Children's Hospital of the King's Daughters in Norfolk, VA.
      Figure thumbnail gr1
      Fig. 1Each consenting subject had 89 hemispherical reflective markers (42 anterior and 47 posterior) attached to anatomical thoracic landmarks.

      1.3 Data analysis and statistics

      Proprietary software from BTS Bioengineering executes real-time pattern recognition algorithms and computes the 3-dimensional coordinates of the reflective markers. Once the coordinates of the points belonging to the chest wall surface have been acquired, a special geometric modeling of the chest wall is applied to describe the surface of the whole chest wall and its compartments. Chest wall volumes were determined via breath-by-breath variations in end-expiratory and end-inspiratory lung volumes. The compartmental contributions were analyzed among controls and preoperative patients with PE to determine relative expansion of the thoracic rib cage, abdominal rib cage, and abdomen. It is important to note that chest wall volume variations are not necessarily equal to lung volume variations; however, OEP has been shown to correlate well with end-expiratory lung volume obtained from Pulmonary Function Tests [
      • Aliverti A.
      • Dellacà R.
      • Pelosi P.
      • et al.
      Compartmental analysis of breathing in the supine and prone positions by optoelectronic plethysmography.
      ,
      • Dellaca
      • Aliverti A.
      • Pelosi P.
      • et al.
      Estimation of end-expiratory lung volume variations by optoelectronic plethysmography.
      ]. Statistical analysis was performed using independent-sample t test and χ2 test.

      2. Results

      Sixty-four patients with PE underwent OEP analysis (PE, 64). Of these patients, 42 underwent repeat analysis 6 months after minimally invasive PE repair (PO, 42). Twenty-two patients had multiple pectus bars used to repair their defect. Patient demographics are reported in Table 1. The volume of the thorax at rest was determined in PE and PO. The total chest wall volume at rest was significantly increased in the postoperative patients (PE, 13.48 L; PO, 14.87 L) (Table 2). Subcompartment analysis also demonstrated significant improvements in all compartments: pulmonary rib cage (PE, 7.35 L; PO, 8.26 L), abdominal rib cage (PE, 2.16 L; PO, 2.35 L), and abdomen (PE, 3.91 L; PO, 4.21 L). Respiratory volume changes of the thorax and chest wall compartments were measured over the course of maximal respiration. These values are recorded in Table 3. Changes in the total chest wall volume during maximal respiration were similar between PE and control subjects (PE, 2.91; PO, 2.87). The correlation between compartmental volume changes after PE repair, body mass index (BMI), and height was performed. Although not statistically significant, a moderate correlation with the abdominal compartment volume change and height was found (Table 4).
      Table 1Patient demographics
      Variable, mean (%)PE (n = 64)PO (n = 42)
      Age (y)15.515.7
      SexMale56 (88%)36 (86%)
      Female8 (12%)6 (14%)
      Height (cm)173174.1
      Weight (kg)58.061.0
      BMI19.320.0
      Multiple pectus bars22 (52%)
      Table 2Thoracic compartment volumes
      Volume (L), meanPE (n = 64)PO (n = 42)P
      Chest wall13.4814.87<.01
      Pulmonary rib cage7.358.26<.01
      Abdominal rib cage2.162.35<.01
      Abdomen3.914.21<.01
      The volume of the thorax at rest in preoperative and postoperative patients was calculated using OEP analysis.
      Table 3Respiratory volume changes
      Volume (L), meanPE (n = 64)PO (n = 42)P
      Chest wall2.912.87.59
      Pulmonary rib cage1.441.40.95
      Abdominal rib cage0.770.71.32
      Abdomen0.840.91<.01
      The change in thoracic volume and chest wall compartments was calculated over the course of maximal respiration.
      Table 4Pearson correlation
      CorrelationBMIPHeightP
      Chest wall−0.210.190.233.15
      Pulmonary rib cage−0.161.320.181.26
      Abdominal rib cage−0.140.390.223.16
      Abdomen−0.203.210.564.09
      The compartment volume change in preoperative and postoperative patients with PE at rest vs BMI and height.
      Optoelectronic plethysmography analysis allows for measurement of specific areas of the chest wall during respiration. To compare chest wall motion over the area of the pectus defect, mean marker point excursion at the midline was compared with more lateral aspects of the chest wall at multiple horizontal anatomical levels of the thorax and abdomen. PO patients demonstrated significantly increased midline marker excursion at the level of the pectus defect. PO patients had 107% more midline marker excursion at the angle of Louis, a 112% increase at the level of the nipple line, a 57% increase at the xiphoid process, and a 57% increase at the costal margin compared with patients with PE (Fig. 2). Impressively, PO midline marker excursion of the umbilicus was decreased by 507% compared with that of the preoperative patients. Similarly significant increases in chest wall motion at the area of the pectus defect, with concurrent decrease in anterior motion at the umbilicus, were seen when PO patients were compared with control patients (Fig. 3).
      Figure thumbnail gr2
      Fig. 2Relative chest wall excursion—PE vs PO. Mean marker excursion between the 2 groups at the midline was compared with corresponding lateral aspects of the chest wall at multiple horizontal anatomical levels of the thorax and abdomen.
      Figure thumbnail gr3
      Fig. 3Relative chest wall excursion—C vs PO. Mean marker excursion between the 2 groups at the midline was compared with corresponding lateral aspects of the chest wall at multiple horizontal anatomical levels of the thorax and abdomen.

      3. Discussion

      Although modalities including computed tomographic scan and formal PFT data effectively document the severity of a PE defect, there remains a paucity of objective data that quantifies improvement after minimally invasive PE repair. Optoelectronic plethysmography is a modality based on measuring the displacement of a finite number of points on the surface of the chest wall. It is noninvasive and does not involve connections to the patient unlike other conventional methods of measuring pulmonary function. We have previously reported the use of OEP chest wall motion analysis in patients with PE and demonstrated significant chest wall motion deficits at the area of the pectus defect during respiration compared with unaffected individuals. Patients with uncorrected PE concurrently exhibited a significant increase in abdominal contributions to respiration, which we believe is an attempt to compensate for dysfunctional upper chest wall motion [

      Redlinger RE Jr, Kelly RE, Nuss D, et al. Regional chest wall motion dysfunction in pectus excavatum patients demonstrated via opto-electronic plethysmography (OEP). J Pediatr Surg (in press).

      ,
      • Cala S.J.
      • Kenyon C.M.
      • Ferrigno G.
      • et al.
      Chest wall and lung volume estimation by optical reflectance motion analysis.
      ]. Here, we report our findings in the original cohort of patients with PE by applying OEP kinematic analysis after minimally invasive Nuss repair.
      It was felt that operative repair would alter the dysfunctional mechanical properties of the chest wall found in patients with uncorrected PE and result in quantifiable differences in chest wall volumes and chest wall motion during respiration. Static chest wall volumes were increased in patients after PE repair. Significant increases in the absolute chest wall volume and the contributions of each of the thoracic compartments were noted in postoperative patients. Similar volume calculation was performed over the course of maximal inspiration and expiration to determine volume changes during the respiratory cycle. PO patients did not demonstrate an increase in thoracic inspiratory capacity because the respiratory volume changes were quite similar. PO patients did demonstrate significantly larger volume changes in the abdomen during maximal breathing maneuvers; however, there was a moderate association between the increase in abdominal volume and the change in patient height over the study period.
      Optoelectronic plethysmography analysis allows for focal measurement of defined points on the chest wall during respiration. Marker point excursion along the anterior surface of the chest wall during respiration was measured to evaluate relative chest wall motion at the pectus defect in comparison with the rest of the chest wall. Six months after Nuss repair, patients were found to exhibit increased chest wall motion at the area of the pectus defect compared with the rest of the chest when compared with preoperative patients with PE as well as controls. Markers placed at midline anatomical positions that correlate to the area of the chest that contains the pectus defect (the angle of Louis, nipple line, xiphoid process, and costal margin) on PO patients exhibited significantly more marker excursion compared with more lateral positions of the chest at that horizontal level. Most significantly, there is a marked change in the motion of the abdomen during respiration in postoperative patients. Comparing patients with uncorrected PE and unaffected controls to PO patients demonstrates significantly decreased abdominal contributions to respiration, as seen with the 507% and 93% decreases in anterior marker excursion at the level of the umbilicus, respectively.
      Optoelectronic plethysmography motion analysis technology allows for calculation of absolute chest volumes, compartmental variations during respiration, and evaluation of respiratory kinematics. We demonstrate in this study that patients with PE who have undergone the minimally invasive Nuss repair experience significant increases in chest wall volume and chest wall motion at the area of the pectus defect during respiration compared with preoperative PE individuals. After operative remodeling of the chest wall, PO patients also exhibit a significant decrease in abdominal contributions to respiration. An unexpected finding is that PO patients actually exhibit hyperdynamic motion of the chest wall and concordantly decreased use of the abdomen during respiration as compared with control individuals. The finding of reversal of the paradoxical breathing motion of the chest wall noted in uncorrected individuals is likely affected by operative remodeling of the upper chest. Placement of the Nuss bar beneath the chest wall defect results in sternal elevation and allows for more effective use of muscles of respiration. These findings may help to explain why patients experience improved endurance with resolution of easy fatigability and shortness of breath after the Nuss procedure. Ongoing studies will continue to evaluate changes in chest wall volumes and variations in relative chest wall motion at various time points, while the Nuss bars remain in postoperative patients as well as after bar removal. We hope to determine whether the hyperdynamic motion of the upper chest wall persists while the pectus bars remain in place or if chest wall motion more closely resembles that of control patients with time.

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