- Email: [email protected]
Cardiac Morphologic Changes After the Nuss Operation for Correction of Pectus Excavatum
GENERAL THORACIC
Cardiac Morphologic Changes After the Nuss Operation for Correction of Pectus Excavatum Jin Yong Jeong, MD, Hyung Joo Park, MD, Jongho Lee, MD, Jae Kil Park, MD, and Keon Hyeon Jo, MD Department of Thoracic and Cardiovascular Surgery, Incheon St. Mary’s Hospital, Incheon; Department of Thoracic and Cardiovacular Surgery, Seoul St. Mary’s Hospital, Seoul; Department of Thoracic and Cardiovacular Surgery, Daejeon St. Mary’s Hospital, Daejeon; and College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
Background. Pectus excavatum results in compression of the heart and may compromise cardiac function. Several studies have shown that surgical correction improves cardiac function as assessed on echocardiography. However, morphologic changes to support this have not been reported. Methods. Between July and December 2011, 109 patients underwent the Nuss operation. We measured the Haller index and other variables. To identify the location of the heart within the chest cavity, the distances from the middle of the spine to the right and left heart walls and from the anterior border of the spine to the anterior and posterior heart walls were measured. To characterize dimensional changes, the anteroposterior, transverse lateral, and right and left oblique longest lengths were measured. Results. The postoperative Haller index was significantly different from the preoperative one (2.52 ± 0.40
versus 4.50 ± 1.45; p < 0.001). The location changes in the anterior, rightward, and leftward directions were 4.97 ± 8.03 mm (p < 0.01), 1.66 ± 7.89 mm (p [ 0.027), and L2.70 ± 11.12 mm (p [ 0.01), respectively. The dimensional changes in anteroposterior and right oblique lengths were 5.42 ± 6.42 mm and 16.33 ± 7.77 mm (p < 0.01), respectively. Conclusions. The heart moved positively in the anterior and rightward directions and negatively in the leftward direction, and the anteroposterior and right oblique dimensions were increased after surgical correction. These data suggest that the heart tends to return to a normal position and shape, and that these changes may contribute to improvement in cardiac function.
P
Although the cardiac deformity index was proposed to assess morphologic changes after the Nuss operation [9], detailed morphologic changes in the heart to support this improvement have not yet been reported. In this study, we compared cardiac morphology before and after the Nuss operation and analyzed the effects of correcting the chest wall deformity.
ectus excavatum (PE) is characterized by depression of the anterior chest wall including the sternum. This change is often described using a measurement of chest wall deformity such as the Haller index (HI) or the Depression index [1, 2]. Pectus excavatum may result in compression of intrathoracic organs, especially the heart and lungs. Surgical resection of abnormal costal cartilage and correction of the depressed anterior chest wall increase pulse oximetry, which is an index of a cardiac efficiency [3, 4]. Echocardiography has demonstrated significant increases in right ventricular diastolic and systolic volume indices as well as stroke volume after surgical correction [5–7]. Maagaard and colleagues [8] recently reported preoperatively maximum cardiac index during exercise was lower in patients with PE compared with healthy, age-matched control subjects. One year after operation, this had increased in patients, and 3 years postoperatively cardiac index had normalized.
Accepted for publication Oct 1, 2013. Address correspondence to Dr Lee, Department of Thoracic and Cardiovascular Surgery, Daejeon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 520-2 Daeheung-dong, Jung-gu, Daejeon 301-723, Korea; e-mail: [email protected].
Ó 2014 by The Society of Thoracic Surgeons Published by Elsevier Inc
(Ann Thorac Surg 2014;97:474–9) Ó 2014 by The Society of Thoracic Surgeons
Patients and Methods From July through December 2011, 109 patients with PE underwent the Nuss operation. Operation was performed in patients with clinical and psychological symptoms, HI greater than 3.25, or cardiac compression caused by depressed sternum on chest computed tomography. Among them were 30 females and 79 males, with an average age of 8.9 6.8 years (range, 3 to 31 years; Table 1). There were 57 patients in the preschool group (<5 years of age), 14 in the school age group (6 to 11 years of age), 26 in the adolescent group (12 to 18 years of age), and 12 in the young adulthood group (>19 years of age). The HI ranged from 2.44 to 9.87 with a mean of 4.50 1.45. Regarding the morphologic classification [10], 61 patients (56%) presented with symmetric type (type 1) and 48 patients (44%) with asymmetric type (type 2) PE. Written informed consent was obtained from each patient or parents before the operation. The study protocol 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2013.10.018
JEONG ET AL CARDIAC CHANGES AFTER THE NUSS OPERATION
Table 1. Preoperative and Postoperative Changes in the Haller Index Variable Total (n ¼ 109) Sex Male (n ¼ 79) Female (n ¼ 30) Age group <5 y (n ¼ 57) 6–11 y (n ¼ 14) 12–18 y (n ¼ 26) >18 y (n ¼ 12) Morphologic subtype Type 1 (n ¼ 61) Type 2 (n ¼ 48)
Preoperative HI
Postoperative HI
p Value
4.50 1.45
2.52 0.40
<0.001
4.31 1.92 4.30 2.41
2.46 0.57 2.51 0.58
<0.001 <0.001
0.34 0.37 0.53 0.33
<0.001 <0.001 <0.001 <0.001
2.42 0.35 2.65 0.44
<0.001 <0.001
4.69 4.19 4.34 4.30
1.53 1.37 1.54 0.80
4.49 1.26 4.51 1.69
2.50 2.28 2.58 2.69
HI ¼ Haller index.
was approved by the Institutional Review Board of the Catholic Medical Center.
Operative Technique All patients were placed in the supine position before the start of surgery. The selected sized bar was bent according to the morphology of the pectus. A crane was applied to the depressed sternum at the xiphoid for initial elevation of the sternum in case of severe depression. Tiny skin incisions were made bilaterally in the lateral chest, and hinge points were determined on both crests of the depression. Subcutaneous tunnels were created bilaterally from the skin incisions toward the hinge points. An introducer or the pectus clamp (Biomet Microfixation, Jacksonville, FL) was introduced into the pleural space through the right hinge point, was passed along the curvature of the depression with the mediastinum dissected toward the opposite hinge point, and finally passed through the hinge to the other skin incision. A 20F chest tube was passed as a guide along with the pectus clamp. The bent bar was then passed along the guide and positioned facing dorsally. The bar was subsequently turned 180 degrees to face ventrally, which elevated the sternum. The convexity of the bar was adjusted to achieve an optimal result. The bar was fixed to the bilateral reciprocal ribs using multipoint fixation
475
method. After hemostasis and irrigation, the incisions were closed in layers. This surgical technique has been described in detail in a previous publication [11]. We removed the pectus bar after 2 years for patients younger than 12 years, after 2.5 years for patients between 12 and 18 years, and after 3 years for patients older than 18 years [12].
Measurement of Cardiac Morphology All patients underwent chest computed tomography before and 1 to 2 weeks after the operation. In the mediastinal window, depth of sternal depression, HI, and cardiac location and dimensional changes were measured on transverse chest computed tomographic images at the lowest point of the sternum, near the xiphosternal junction. If the measurements were impeded owing to the position of the bar, the point just below or above the bar was measured. For the leftward and rightward location changes (Fig 1), a vertical line was drawn from the middle of the vertebral spinous process, and the distances from the line to the right and left side walls of the heart were measured. To assess the anteroposterior (AP) location changes, a horizontal line was drawn at the anterior border of the vertebral body, and the distances from this line to the anterior and posterior walls of the heart were measured. Each location and directional change of the heart was calculated by subtracting the preoperative measurement from the postoperative measurement. For the dimensional changes of the heart (Fig 2), the AP and transverse lateral longest lengths were measured. The longest oblique lengths were also measured at a 45-degree angle from the horizontal. The right oblique measurement is the longest oblique length extending from the back to the anterior rightward direction, and the left oblique measurement extended in the anterior leftward direction.
Statistical Analysis Data analysis was performed with the SPSS program package (SPSS version 12.0; SPSS, Chicago, IL). Continuous variables were presented as a mean standard deviation and were compared with Student’s t tests or by one-way analysis of variance as appropriate. Correlation among groups was calculated with linear regression analysis. A probability value of less than 0.05 was considered statistically significant. Fig 1. Measurement of changes in cardiac location (A) before and (B) after the Nuss operation.
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Fig 2. Measurement of changes in cardiac dimension (A) before and (B) after the Nuss operation.
Results The difference between postoperative and preoperative HIs was statistically significant (4.50 1.45 versus 2.52 0.40; p < 0.001; Table 1), regardless of sex, age group, or morphologic subtypes. There was no significant correlation between age group and HI, or between sex and HI. Postoperative location changes of the heart were 4.97 8.03 mm in the anterior direction (p < 0.01), 0.68 8.38 mm in the posterior direction (p ¼ 0.39), 1.66 7.89 mm in the rightward direction (p ¼ 0.027), and 2.70 11.12 mm in leftward direction (p ¼ 0.01; Table 2). There was no statistical significance among age groups and location and dimensional variables (Table 3). Postoperative dimensional changes of the heart were 5.42 6.42 mm in AP length (p < 0.01), 1.03 9.63 mm in lateral length (p ¼ 0.26), 16.33 7.77 mm in right oblique length (p < 0.01), and 0.92 6.74 mm in left oblique length (p ¼ 0.15; Table 2). There were no significant correlations between location or dimensional changes and age group or sex. There was, however, a statistically significant correlation between preoperative minus postoperative HI and postoperative minus preoperative horizontal left length (y ¼ 3.91x þ 4.96; r2 ¼ 0.1918; F1,106 ¼ 25; p < 0.001; Fig 3).
Comment Although there have been studies that have examined changes in cardiovascular function after surgical
correction of PE [3–6], few have reported morphologic changes of the heart [7, 9]. This study assessed changes in location and dimension of the heart before and after the Nuss operation to better explain the relationship between morphology and function. Anatomically, the mediastinum lies between pleurae and extends from the sternum anteriorly to the thoracic vertebral column posteriorly, with the space between remaining relatively fixed. Figure 1 illustrates how PE affects this space, with the right ventricle being the most vulnerable chamber for compression. The depressed sternum also directly compresses the heart and induces leftward rotation and displacement. The location change of heart after the Nuss operation results in movement forward from the spinous process in the vertical direction (4.95 8.04 mm; p < 0.01) and movement centrally from the left side in the horizontal direction (2.71 11.13 mm; p ¼ 0.011). After the Nuss operation, the heart returns toward the normal position (Table 2). Pectus excavatum depresses the sternum and decreases the mediastinal space, thereby impairing cardiac and pulmonary function. Chu and associates [13] previously reported that the degree of sternal depression positively correlated with the degree of cardiac rotation in patients with PE. A deeper sternal depression caused the heart to move toward the left and in some cases completely into the left thoracic cavity with cardiac rotation. In our study, there were no statistically significant differences between age groups and location change
Table 2. Preoperative and Postoperative Changes in Heart Location and Dimension Variable (mm) Location change VA VP HR HL Dimensional change AP Lat Obl-Rt Obl-Lt a
Preoperative Length
Postoperative Length
Differencea
p Valueb
67.25 1.69 23.26 75.06
11.95 8.73 10.82 15.90
72.22 1 24.93 72.35
9.13 8.05 7.31 15.05
4.95 0.69 1.67 2.71
8.04 8.38 7.89 11.13
<0.01 0.395 0.027 0.011
66.79 98.31 64.98 72.11
9.98 15.56 11.15 10.53
72.22 97.28 81.31 71.18
9.13 17.33 11.19 10.59
5.42 1.04 16.33 0.93
6.42 9.69 7.77 6.74
<0.01 0.26 <0.01 0.155
Difference is postoperative minus preoperative length.
AP ¼ anteroposterior; HL ¼ horizontal left; vertical anterior; VP ¼ vertical posterior.
b
p value determined by Student’s t-test.
HR ¼ horizontal right;
Lat ¼ lateral;
Obl-Lt ¼ oblique left;
Obl-Rt ¼ oblique right;
VA ¼
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Table 3. Location and Dimensional Changes According to the Age Groups Age Groups (y) Variable
<5 (n ¼ 57)
Location change (mm) D-VA 4.32 D-VP 1.54 D-HR 1.30 D-HL 3.12 Dimensional change (mm) D-AP 5.18 qD-Lat 1.82 D-Obl-Rt 16.23 D-Obl-Lt 0.35 a
6–11 (n ¼ 14)
12–18 (n ¼ 26)
>18 (n ¼ 12)
All (n ¼ 109)
p Valuea
9.24 10.06 8.38 10.88
5.36 0.07 0.36 0.07
7.15 4.91 8.33 9.14
5.60 0.67 2.74 4.49
6.35 6.31 7.13 12.55
6.36 0.36 2.64 0.45
6.50 6.86 7.05 11.22
4.95 0.69 1.67 2.71
8.04 8.38 7.89 11.13
>0.05 >0.05 >0.05 >0.05
6.42 8.44 8.58 6.26
5.36 0.29 15.64 4.14
7.15 6.01 5.27 7.15
5.59 1.74 15.78 1.63
6.35 12.64 7.52 7.24
6.36 3.09 19.09 1.90
6.50 10.76 6.83 6.06
5.42 1.04 16.33 0.93
6.42 9.69 7.77 6.74
>0.05 >0.05 >0.05 >0.05
p value determined by one-way analysis of variance (ANOVA).
AP ¼ anteroposterior; D ¼ postoperative length minus preoperative length; HL ¼ horizontal left; HR ¼ horizontal right; lateral; Obl-Lt ¼ oblique left; Obl-Rt ¼ oblique right; VA ¼ vertical anterior; VP ¼ vertical posterior.
variables, which explains the finding that all age groups equally returned to the normal heart position after the Nuss operation (Table 3). Therefore, we think there is no age restriction in determining when the Nuss operation is indicated. Surgical correction of PE using the RavitchShamberger technique results in a significant increase in end-diastolic right ventricular area and volume (47% and 88%, respectively) and a significantly increased left ventricular ejection fraction (14%; p < 0.001) as assessed on echocardiography [14]. Sigalet and colleagues [6] and Coln and coworkers [15] previously reported improved cardiac function in children and adults who underwent the Nuss operation. End-diastolic right ventricular area and volume correlates with decompression of the sternum and the resultant significant increase in right ventricular diastolic and stroke volume indices [5]. Maagaard and associates [8] reported maximum cardiac index
Lat ¼
during exercise was lower in patients with PE preoperatively compared with healthy, age-matched control subjects. One year after operation, this had increased in patients and 3 years postoperatively cardiac index had normalized. This normalization of cardiac output during exercise may be related to the larger thoracic cavity created by the surgical procedure. Our study also showed a significant dimensional increase in the postoperative AP and right oblique directions (5.42 6.42 mm, 16.33 7.77 mm, respectively; p < 0.01). Haller and colleagues [1] reported all patients who required operative correction for PE had an index greater than 3.25, whereas matched normal control subjects all had an index less than 3.25. Despite findings of improved right ventricular function after operative correction of PE, clinical variables and a correlation with HI have not yet been established [16]. Using noninvasive echocardiogram and electrocardiogram during exercise,
Fig 3. Linear regression analysis of the difference between postoperative and preoperative horizontal left dimension (D-HL) and the difference between preoperative and postoperative Haller index (D-HI) shows a negative correlation between these terms. (D-HI ¼ preoperative-postoperative Haller index; D-HL ¼ postoperative-preoperative horizontal left.)
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a postoperative HI of less than 3.25 completely alleviated cardiac compression [7]. Swanson and coworkers [17] also reported that 41% of patients with PE had cardiac limitations, with a mean HI with isolated cardiac dysfunction of 3.6. However, the authors did not correlate HI with cardiac dysfunction because postoperative cardiopulmonary exercise testing was not performed, and they were thus unable to assess associations of preoperative HI severity with physiologic improvement after repair. Our results show that the difference between preoperative and postoperative HI was significantly decreased (4.50 1.45 versus 2.52 0.40; p < 0.001; Table 1), regardless of sex, age group, or morphologic subtypes. We did not correlate HI with cardiac functional improvement. However, we did identify a negative correlation between preoperative and postoperative HI and postoperative and preoperative horizontal left length. This indicates that a greater postoperative change in HI reflects a return of the heart to the normal position. In conclusion, HI was significantly decreased after the Nuss operation. The location of the heart shifted positively in the anterior and rightward directions and negatively in the leftward direction. Cardiac dimension also increased in the AP and right oblique lengths. Therefore, the heart appears to return to the normal cardiac position and shape soon after the Nuss operation, and these morphologic changes may contribute to improvement in cardiac function.
References 1. Haller JA Jr, Kramer SS, Lietman SA. Use of CT scans in selection of patients for pectus excavatum surgery: a preliminary report. J Pediatr Surg 1987;22:904–6. 2. Lee CS, Park HJ, Lee SY. New computerized tomogram (CT) indices for pectus excavatum: tools for assessing modified techniques for asymmetry in Nuss repair. Chest 2004;126(4 Suppl):777S. 3. Cahill JL, Lees GM, Robertson HT. A summary of preoperative and postoperative cardiorespiratory performance in patients undergoing pectus excavatum and carinatum repair. J Pediatr Surg 1984;19:430–3.
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4. Quigley PM, Haller JA Jr, Jelus KL, Loughlin GM, Marcus CL. Cardiorespiratory function before and after corrective surgery in pectus excavatum. J Pediatr 1996;128:638–43. 5. Kowalewski J, Barcikowski S, Brocki M. Cardiorespiratory function before and after operation for pectus excavatum: medium-term results. Eur J Cardiothorac Surg 1998;13:275–9. 6. Sigalet DL, Montgomery M, Harder J. Cardiopulmonary effects of closed repair of pectus excavatum. J Pediatr Surg 2003;38:380–5. 7. Coln E, Carrasco J, Coln D. Demonstrating relief of cardiac compression with the Nuss minimally invasive repair for pectus excavatum. J Pediatr Surg 2006;41:683–6. 8. Maagaard M, Tang M, Ringgaard S, et al. Normalized cardiopulmonary exercise function in patients with pectus excavatum three years after operation. Ann Thorac Surg 2013;96:272–8. 9. Kim M, Lee KY, Park HJ, et al. Development of new cardiac deformity indexes for pectus excavatum on computerized tomography: feasibility for pre- and post-operative evaluation. Yonsei Med J 2009;50:385–90. 10. Park HJ, Lee SY, Lee CS, Youm W, Lee KR. The Nuss procedure for pectus excavatum: evolution of techniques and early results on 322 patients. Ann Thorac Surg 2004;77: 289–95. 11. Park HJ, Jeong JY, Jo WM, et al. Minimally invasive repair of pectus excavatum: a novel morphology-tailored, patientspecific approach. J Thorac Cardiovasc Surg 2010;139: 379–86. 12. Park HJ, Sung SW, Park JK, Kim JJ, Jeon HW, Wang YP. How early can we repair pectus excavatum: the earlier the better? Eur J Cardiothorac Surg 2012;42:667–72. 13. Chu ZG, Yu JQ, Yang ZG, Peng LQ, Bai HL, LI XM. Correlation between sternal depression and cardiac rotation in pectus excavatum: evaluation with helical CT. AJR Am J Roentgenol 2010;195:W76–80. 14. Krueger T, Chassot PG, Christodoulou M, Cheng C, Ris HB, Magnusson L. Cardiac function assessed by transesophageal echocardiography during pectus excavatum repair. Ann Thorac Surg 2010;89:240–3. 15. Coln D, Gunning T, Ramsay M, Swygert T, Vera R. Early experience with the Nuss minimally invasive correction of pectus excavatum in adults. World J Surg 2002;26:1217–21. 16. Kowalewski J, Brocki M, Dryjanski T, Zolynski K, Koktysz R. Pectus excavatum: increase of right ventricular systolic, diastolic, and stroke volumes after surgical repair. J Thorac Cardiovas Surg 1999;118:87–93. 17. Swanson JW, Avansino JR, Phillips GS, et al. Correlating Haller Index and cardiopulmonary disease in pectus excavatum. Am J Surg 2012;203:660–4.
INVITED COMMENTARY In the present study, Jeong and colleagues [1] performed minimally invasive repair of pectus excavatum in 109 patients and discovered that both the shape and the location of the heart shifted significantly as measured by preoperative and postoperative computed tomography of the chest. The first part has been known for some time from several echocardiographic studies that observed how the diameter of the heart increased when anatomic compression by the funnel chest was released. The observation that the location of the heart shifts postoperatively is new, although this is what most surgeons would expect after correction of this frequent chest wall deformity. The actual anatomic shift, however, was modest (measured in millimeters), and one may question how accurate their measurements were, as judged from
Ó 2014 by The Society of Thoracic Surgeons Published by Elsevier Inc
the figures presented but likely also because more than 50% of their patient population were children younger than 5 years. Corrective surgery for pectus excavatum in this age group is controversial, to say the least, and even though repair in very young children has been reported previously, such cases make the exception. It is certainly far from the clinical approach presented, wherein the majority of 109 patients operated on over a 6-month period were children younger than 5 years. The authors are known to operate on very young children—sometimes just 1-year-old babies—and one may speculate what the indications were in this group of patients, but this was not discussed in detail. Surely, most if not all of these toddlers would not have complained about physical
0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2013.11.013
Cardiac Morphologic Changes After the Nuss Operation for Correction of Pectus Excavatum Jin Yong Jeong, MD, Hyung Joo Park, MD, Jongho Lee, MD, Jae Kil Park, MD, and Keon Hyeon Jo, MD Department of Thoracic and Cardiovascular Surgery, Incheon St. Mary’s Hospital, Incheon; Department of Thoracic and Cardiovacular Surgery, Seoul St. Mary’s Hospital, Seoul; Department of Thoracic and Cardiovacular Surgery, Daejeon St. Mary’s Hospital, Daejeon; and College of Medicine, The Catholic University of Korea, Seoul, Republic of Korea
Background. Pectus excavatum results in compression of the heart and may compromise cardiac function. Several studies have shown that surgical correction improves cardiac function as assessed on echocardiography. However, morphologic changes to support this have not been reported. Methods. Between July and December 2011, 109 patients underwent the Nuss operation. We measured the Haller index and other variables. To identify the location of the heart within the chest cavity, the distances from the middle of the spine to the right and left heart walls and from the anterior border of the spine to the anterior and posterior heart walls were measured. To characterize dimensional changes, the anteroposterior, transverse lateral, and right and left oblique longest lengths were measured. Results. The postoperative Haller index was significantly different from the preoperative one (2.52 ± 0.40
versus 4.50 ± 1.45; p < 0.001). The location changes in the anterior, rightward, and leftward directions were 4.97 ± 8.03 mm (p < 0.01), 1.66 ± 7.89 mm (p [ 0.027), and L2.70 ± 11.12 mm (p [ 0.01), respectively. The dimensional changes in anteroposterior and right oblique lengths were 5.42 ± 6.42 mm and 16.33 ± 7.77 mm (p < 0.01), respectively. Conclusions. The heart moved positively in the anterior and rightward directions and negatively in the leftward direction, and the anteroposterior and right oblique dimensions were increased after surgical correction. These data suggest that the heart tends to return to a normal position and shape, and that these changes may contribute to improvement in cardiac function.
P
Although the cardiac deformity index was proposed to assess morphologic changes after the Nuss operation [9], detailed morphologic changes in the heart to support this improvement have not yet been reported. In this study, we compared cardiac morphology before and after the Nuss operation and analyzed the effects of correcting the chest wall deformity.
ectus excavatum (PE) is characterized by depression of the anterior chest wall including the sternum. This change is often described using a measurement of chest wall deformity such as the Haller index (HI) or the Depression index [1, 2]. Pectus excavatum may result in compression of intrathoracic organs, especially the heart and lungs. Surgical resection of abnormal costal cartilage and correction of the depressed anterior chest wall increase pulse oximetry, which is an index of a cardiac efficiency [3, 4]. Echocardiography has demonstrated significant increases in right ventricular diastolic and systolic volume indices as well as stroke volume after surgical correction [5–7]. Maagaard and colleagues [8] recently reported preoperatively maximum cardiac index during exercise was lower in patients with PE compared with healthy, age-matched control subjects. One year after operation, this had increased in patients, and 3 years postoperatively cardiac index had normalized.
Accepted for publication Oct 1, 2013. Address correspondence to Dr Lee, Department of Thoracic and Cardiovascular Surgery, Daejeon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 520-2 Daeheung-dong, Jung-gu, Daejeon 301-723, Korea; e-mail: [email protected].
Ó 2014 by The Society of Thoracic Surgeons Published by Elsevier Inc
(Ann Thorac Surg 2014;97:474–9) Ó 2014 by The Society of Thoracic Surgeons
Patients and Methods From July through December 2011, 109 patients with PE underwent the Nuss operation. Operation was performed in patients with clinical and psychological symptoms, HI greater than 3.25, or cardiac compression caused by depressed sternum on chest computed tomography. Among them were 30 females and 79 males, with an average age of 8.9 6.8 years (range, 3 to 31 years; Table 1). There were 57 patients in the preschool group (<5 years of age), 14 in the school age group (6 to 11 years of age), 26 in the adolescent group (12 to 18 years of age), and 12 in the young adulthood group (>19 years of age). The HI ranged from 2.44 to 9.87 with a mean of 4.50 1.45. Regarding the morphologic classification [10], 61 patients (56%) presented with symmetric type (type 1) and 48 patients (44%) with asymmetric type (type 2) PE. Written informed consent was obtained from each patient or parents before the operation. The study protocol 0003-4975/$36.00 http://dx.doi.org/10.1016/j.athoracsur.2013.10.018
JEONG ET AL CARDIAC CHANGES AFTER THE NUSS OPERATION
Table 1. Preoperative and Postoperative Changes in the Haller Index Variable Total (n ¼ 109) Sex Male (n ¼ 79) Female (n ¼ 30) Age group <5 y (n ¼ 57) 6–11 y (n ¼ 14) 12–18 y (n ¼ 26) >18 y (n ¼ 12) Morphologic subtype Type 1 (n ¼ 61) Type 2 (n ¼ 48)
Preoperative HI
Postoperative HI
p Value
4.50 1.45
2.52 0.40
<0.001
4.31 1.92 4.30 2.41
2.46 0.57 2.51 0.58
<0.001 <0.001
0.34 0.37 0.53 0.33
<0.001 <0.001 <0.001 <0.001
2.42 0.35 2.65 0.44
<0.001 <0.001
4.69 4.19 4.34 4.30
1.53 1.37 1.54 0.80
4.49 1.26 4.51 1.69
2.50 2.28 2.58 2.69
HI ¼ Haller index.
was approved by the Institutional Review Board of the Catholic Medical Center.
Operative Technique All patients were placed in the supine position before the start of surgery. The selected sized bar was bent according to the morphology of the pectus. A crane was applied to the depressed sternum at the xiphoid for initial elevation of the sternum in case of severe depression. Tiny skin incisions were made bilaterally in the lateral chest, and hinge points were determined on both crests of the depression. Subcutaneous tunnels were created bilaterally from the skin incisions toward the hinge points. An introducer or the pectus clamp (Biomet Microfixation, Jacksonville, FL) was introduced into the pleural space through the right hinge point, was passed along the curvature of the depression with the mediastinum dissected toward the opposite hinge point, and finally passed through the hinge to the other skin incision. A 20F chest tube was passed as a guide along with the pectus clamp. The bent bar was then passed along the guide and positioned facing dorsally. The bar was subsequently turned 180 degrees to face ventrally, which elevated the sternum. The convexity of the bar was adjusted to achieve an optimal result. The bar was fixed to the bilateral reciprocal ribs using multipoint fixation
475
method. After hemostasis and irrigation, the incisions were closed in layers. This surgical technique has been described in detail in a previous publication [11]. We removed the pectus bar after 2 years for patients younger than 12 years, after 2.5 years for patients between 12 and 18 years, and after 3 years for patients older than 18 years [12].
Measurement of Cardiac Morphology All patients underwent chest computed tomography before and 1 to 2 weeks after the operation. In the mediastinal window, depth of sternal depression, HI, and cardiac location and dimensional changes were measured on transverse chest computed tomographic images at the lowest point of the sternum, near the xiphosternal junction. If the measurements were impeded owing to the position of the bar, the point just below or above the bar was measured. For the leftward and rightward location changes (Fig 1), a vertical line was drawn from the middle of the vertebral spinous process, and the distances from the line to the right and left side walls of the heart were measured. To assess the anteroposterior (AP) location changes, a horizontal line was drawn at the anterior border of the vertebral body, and the distances from this line to the anterior and posterior walls of the heart were measured. Each location and directional change of the heart was calculated by subtracting the preoperative measurement from the postoperative measurement. For the dimensional changes of the heart (Fig 2), the AP and transverse lateral longest lengths were measured. The longest oblique lengths were also measured at a 45-degree angle from the horizontal. The right oblique measurement is the longest oblique length extending from the back to the anterior rightward direction, and the left oblique measurement extended in the anterior leftward direction.
Statistical Analysis Data analysis was performed with the SPSS program package (SPSS version 12.0; SPSS, Chicago, IL). Continuous variables were presented as a mean standard deviation and were compared with Student’s t tests or by one-way analysis of variance as appropriate. Correlation among groups was calculated with linear regression analysis. A probability value of less than 0.05 was considered statistically significant. Fig 1. Measurement of changes in cardiac location (A) before and (B) after the Nuss operation.
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Fig 2. Measurement of changes in cardiac dimension (A) before and (B) after the Nuss operation.
Results The difference between postoperative and preoperative HIs was statistically significant (4.50 1.45 versus 2.52 0.40; p < 0.001; Table 1), regardless of sex, age group, or morphologic subtypes. There was no significant correlation between age group and HI, or between sex and HI. Postoperative location changes of the heart were 4.97 8.03 mm in the anterior direction (p < 0.01), 0.68 8.38 mm in the posterior direction (p ¼ 0.39), 1.66 7.89 mm in the rightward direction (p ¼ 0.027), and 2.70 11.12 mm in leftward direction (p ¼ 0.01; Table 2). There was no statistical significance among age groups and location and dimensional variables (Table 3). Postoperative dimensional changes of the heart were 5.42 6.42 mm in AP length (p < 0.01), 1.03 9.63 mm in lateral length (p ¼ 0.26), 16.33 7.77 mm in right oblique length (p < 0.01), and 0.92 6.74 mm in left oblique length (p ¼ 0.15; Table 2). There were no significant correlations between location or dimensional changes and age group or sex. There was, however, a statistically significant correlation between preoperative minus postoperative HI and postoperative minus preoperative horizontal left length (y ¼ 3.91x þ 4.96; r2 ¼ 0.1918; F1,106 ¼ 25; p < 0.001; Fig 3).
Comment Although there have been studies that have examined changes in cardiovascular function after surgical
correction of PE [3–6], few have reported morphologic changes of the heart [7, 9]. This study assessed changes in location and dimension of the heart before and after the Nuss operation to better explain the relationship between morphology and function. Anatomically, the mediastinum lies between pleurae and extends from the sternum anteriorly to the thoracic vertebral column posteriorly, with the space between remaining relatively fixed. Figure 1 illustrates how PE affects this space, with the right ventricle being the most vulnerable chamber for compression. The depressed sternum also directly compresses the heart and induces leftward rotation and displacement. The location change of heart after the Nuss operation results in movement forward from the spinous process in the vertical direction (4.95 8.04 mm; p < 0.01) and movement centrally from the left side in the horizontal direction (2.71 11.13 mm; p ¼ 0.011). After the Nuss operation, the heart returns toward the normal position (Table 2). Pectus excavatum depresses the sternum and decreases the mediastinal space, thereby impairing cardiac and pulmonary function. Chu and associates [13] previously reported that the degree of sternal depression positively correlated with the degree of cardiac rotation in patients with PE. A deeper sternal depression caused the heart to move toward the left and in some cases completely into the left thoracic cavity with cardiac rotation. In our study, there were no statistically significant differences between age groups and location change
Table 2. Preoperative and Postoperative Changes in Heart Location and Dimension Variable (mm) Location change VA VP HR HL Dimensional change AP Lat Obl-Rt Obl-Lt a
Preoperative Length
Postoperative Length
Differencea
p Valueb
67.25 1.69 23.26 75.06
11.95 8.73 10.82 15.90
72.22 1 24.93 72.35
9.13 8.05 7.31 15.05
4.95 0.69 1.67 2.71
8.04 8.38 7.89 11.13
<0.01 0.395 0.027 0.011
66.79 98.31 64.98 72.11
9.98 15.56 11.15 10.53
72.22 97.28 81.31 71.18
9.13 17.33 11.19 10.59
5.42 1.04 16.33 0.93
6.42 9.69 7.77 6.74
<0.01 0.26 <0.01 0.155
Difference is postoperative minus preoperative length.
AP ¼ anteroposterior; HL ¼ horizontal left; vertical anterior; VP ¼ vertical posterior.
b
p value determined by Student’s t-test.
HR ¼ horizontal right;
Lat ¼ lateral;
Obl-Lt ¼ oblique left;
Obl-Rt ¼ oblique right;
VA ¼
JEONG ET AL CARDIAC CHANGES AFTER THE NUSS OPERATION
477
Table 3. Location and Dimensional Changes According to the Age Groups Age Groups (y) Variable
<5 (n ¼ 57)
Location change (mm) D-VA 4.32 D-VP 1.54 D-HR 1.30 D-HL 3.12 Dimensional change (mm) D-AP 5.18 qD-Lat 1.82 D-Obl-Rt 16.23 D-Obl-Lt 0.35 a
6–11 (n ¼ 14)
12–18 (n ¼ 26)
>18 (n ¼ 12)
All (n ¼ 109)
p Valuea
9.24 10.06 8.38 10.88
5.36 0.07 0.36 0.07
7.15 4.91 8.33 9.14
5.60 0.67 2.74 4.49
6.35 6.31 7.13 12.55
6.36 0.36 2.64 0.45
6.50 6.86 7.05 11.22
4.95 0.69 1.67 2.71
8.04 8.38 7.89 11.13
>0.05 >0.05 >0.05 >0.05
6.42 8.44 8.58 6.26
5.36 0.29 15.64 4.14
7.15 6.01 5.27 7.15
5.59 1.74 15.78 1.63
6.35 12.64 7.52 7.24
6.36 3.09 19.09 1.90
6.50 10.76 6.83 6.06
5.42 1.04 16.33 0.93
6.42 9.69 7.77 6.74
>0.05 >0.05 >0.05 >0.05
p value determined by one-way analysis of variance (ANOVA).
AP ¼ anteroposterior; D ¼ postoperative length minus preoperative length; HL ¼ horizontal left; HR ¼ horizontal right; lateral; Obl-Lt ¼ oblique left; Obl-Rt ¼ oblique right; VA ¼ vertical anterior; VP ¼ vertical posterior.
variables, which explains the finding that all age groups equally returned to the normal heart position after the Nuss operation (Table 3). Therefore, we think there is no age restriction in determining when the Nuss operation is indicated. Surgical correction of PE using the RavitchShamberger technique results in a significant increase in end-diastolic right ventricular area and volume (47% and 88%, respectively) and a significantly increased left ventricular ejection fraction (14%; p < 0.001) as assessed on echocardiography [14]. Sigalet and colleagues [6] and Coln and coworkers [15] previously reported improved cardiac function in children and adults who underwent the Nuss operation. End-diastolic right ventricular area and volume correlates with decompression of the sternum and the resultant significant increase in right ventricular diastolic and stroke volume indices [5]. Maagaard and associates [8] reported maximum cardiac index
Lat ¼
during exercise was lower in patients with PE preoperatively compared with healthy, age-matched control subjects. One year after operation, this had increased in patients and 3 years postoperatively cardiac index had normalized. This normalization of cardiac output during exercise may be related to the larger thoracic cavity created by the surgical procedure. Our study also showed a significant dimensional increase in the postoperative AP and right oblique directions (5.42 6.42 mm, 16.33 7.77 mm, respectively; p < 0.01). Haller and colleagues [1] reported all patients who required operative correction for PE had an index greater than 3.25, whereas matched normal control subjects all had an index less than 3.25. Despite findings of improved right ventricular function after operative correction of PE, clinical variables and a correlation with HI have not yet been established [16]. Using noninvasive echocardiogram and electrocardiogram during exercise,
Fig 3. Linear regression analysis of the difference between postoperative and preoperative horizontal left dimension (D-HL) and the difference between preoperative and postoperative Haller index (D-HI) shows a negative correlation between these terms. (D-HI ¼ preoperative-postoperative Haller index; D-HL ¼ postoperative-preoperative horizontal left.)
GENERAL THORACIC
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GENERAL THORACIC
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JEONG ET AL CARDIAC CHANGES AFTER THE NUSS OPERATION
a postoperative HI of less than 3.25 completely alleviated cardiac compression [7]. Swanson and coworkers [17] also reported that 41% of patients with PE had cardiac limitations, with a mean HI with isolated cardiac dysfunction of 3.6. However, the authors did not correlate HI with cardiac dysfunction because postoperative cardiopulmonary exercise testing was not performed, and they were thus unable to assess associations of preoperative HI severity with physiologic improvement after repair. Our results show that the difference between preoperative and postoperative HI was significantly decreased (4.50 1.45 versus 2.52 0.40; p < 0.001; Table 1), regardless of sex, age group, or morphologic subtypes. We did not correlate HI with cardiac functional improvement. However, we did identify a negative correlation between preoperative and postoperative HI and postoperative and preoperative horizontal left length. This indicates that a greater postoperative change in HI reflects a return of the heart to the normal position. In conclusion, HI was significantly decreased after the Nuss operation. The location of the heart shifted positively in the anterior and rightward directions and negatively in the leftward direction. Cardiac dimension also increased in the AP and right oblique lengths. Therefore, the heart appears to return to the normal cardiac position and shape soon after the Nuss operation, and these morphologic changes may contribute to improvement in cardiac function.
References 1. Haller JA Jr, Kramer SS, Lietman SA. Use of CT scans in selection of patients for pectus excavatum surgery: a preliminary report. J Pediatr Surg 1987;22:904–6. 2. Lee CS, Park HJ, Lee SY. New computerized tomogram (CT) indices for pectus excavatum: tools for assessing modified techniques for asymmetry in Nuss repair. Chest 2004;126(4 Suppl):777S. 3. Cahill JL, Lees GM, Robertson HT. A summary of preoperative and postoperative cardiorespiratory performance in patients undergoing pectus excavatum and carinatum repair. J Pediatr Surg 1984;19:430–3.
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4. Quigley PM, Haller JA Jr, Jelus KL, Loughlin GM, Marcus CL. Cardiorespiratory function before and after corrective surgery in pectus excavatum. J Pediatr 1996;128:638–43. 5. Kowalewski J, Barcikowski S, Brocki M. Cardiorespiratory function before and after operation for pectus excavatum: medium-term results. Eur J Cardiothorac Surg 1998;13:275–9. 6. Sigalet DL, Montgomery M, Harder J. Cardiopulmonary effects of closed repair of pectus excavatum. J Pediatr Surg 2003;38:380–5. 7. Coln E, Carrasco J, Coln D. Demonstrating relief of cardiac compression with the Nuss minimally invasive repair for pectus excavatum. J Pediatr Surg 2006;41:683–6. 8. Maagaard M, Tang M, Ringgaard S, et al. Normalized cardiopulmonary exercise function in patients with pectus excavatum three years after operation. Ann Thorac Surg 2013;96:272–8. 9. Kim M, Lee KY, Park HJ, et al. Development of new cardiac deformity indexes for pectus excavatum on computerized tomography: feasibility for pre- and post-operative evaluation. Yonsei Med J 2009;50:385–90. 10. Park HJ, Lee SY, Lee CS, Youm W, Lee KR. The Nuss procedure for pectus excavatum: evolution of techniques and early results on 322 patients. Ann Thorac Surg 2004;77: 289–95. 11. Park HJ, Jeong JY, Jo WM, et al. Minimally invasive repair of pectus excavatum: a novel morphology-tailored, patientspecific approach. J Thorac Cardiovasc Surg 2010;139: 379–86. 12. Park HJ, Sung SW, Park JK, Kim JJ, Jeon HW, Wang YP. How early can we repair pectus excavatum: the earlier the better? Eur J Cardiothorac Surg 2012;42:667–72. 13. Chu ZG, Yu JQ, Yang ZG, Peng LQ, Bai HL, LI XM. Correlation between sternal depression and cardiac rotation in pectus excavatum: evaluation with helical CT. AJR Am J Roentgenol 2010;195:W76–80. 14. Krueger T, Chassot PG, Christodoulou M, Cheng C, Ris HB, Magnusson L. Cardiac function assessed by transesophageal echocardiography during pectus excavatum repair. Ann Thorac Surg 2010;89:240–3. 15. Coln D, Gunning T, Ramsay M, Swygert T, Vera R. Early experience with the Nuss minimally invasive correction of pectus excavatum in adults. World J Surg 2002;26:1217–21. 16. Kowalewski J, Brocki M, Dryjanski T, Zolynski K, Koktysz R. Pectus excavatum: increase of right ventricular systolic, diastolic, and stroke volumes after surgical repair. J Thorac Cardiovas Surg 1999;118:87–93. 17. Swanson JW, Avansino JR, Phillips GS, et al. Correlating Haller Index and cardiopulmonary disease in pectus excavatum. Am J Surg 2012;203:660–4.
INVITED COMMENTARY In the present study, Jeong and colleagues [1] performed minimally invasive repair of pectus excavatum in 109 patients and discovered that both the shape and the location of the heart shifted significantly as measured by preoperative and postoperative computed tomography of the chest. The first part has been known for some time from several echocardiographic studies that observed how the diameter of the heart increased when anatomic compression by the funnel chest was released. The observation that the location of the heart shifts postoperatively is new, although this is what most surgeons would expect after correction of this frequent chest wall deformity. The actual anatomic shift, however, was modest (measured in millimeters), and one may question how accurate their measurements were, as judged from
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the figures presented but likely also because more than 50% of their patient population were children younger than 5 years. Corrective surgery for pectus excavatum in this age group is controversial, to say the least, and even though repair in very young children has been reported previously, such cases make the exception. It is certainly far from the clinical approach presented, wherein the majority of 109 patients operated on over a 6-month period were children younger than 5 years. The authors are known to operate on very young children—sometimes just 1-year-old babies—and one may speculate what the indications were in this group of patients, but this was not discussed in detail. Surely, most if not all of these toddlers would not have complained about physical
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