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J Thorac Cardiovasc Surg 1994;107:1403-1409
© 1994 Mosby, Inc.
GENERAL THORACIC SURGERY |
Nijmegen, The Netherlands
From the Departments of Thoracic and Cardiac Surgery,a Diagnostic Radiology,c and Medical Statistics,d University Hospital Nijmegen, and University Lung Centre Dekkerswald,b Groesbeek, The Netherlands.
Received for publication Aug. 18, 1993. Accepted for publication Nov. 12, 1993. Address for reprints: W. J. Morshuis, MD, Department of Thoracic and Cardiac Surgery, University Hospital St. Radboud, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands.
Abstract
In 35 patients with pectus excavatum (aged 17.9 ± 5.6 years) pulmonary function and maximal exercise test results were compared before and at 1 year after operation. The lower posteroanterior chest diameter on the lateral x-ray film was significantly smaller than normal ( p < 0.0001) and increased significantly after operation ( p < 0.0001). Preoperatively, total lung capacity (86.0% ± 14.4%; p = 0.0001) and inspiratory vital capacity (79.7% ± 16.2; p = 0.0001) were significantly smaller than predicted and further decreased after operation (-9.2% ± 9.2%; p = 0.0001 and -6.6% ± 10.7%; p = 0.0012, respectively). Arterial blood gas values displayed normal patterns with increasing exercise both before and after operation. Only the arterial pH decreased more after operation than before ( p = 0.0026). After operation there was a significant increase in maximal oxygen uptake (oxygen uptake; p = 0.0002 and oxygen uptake per kilogram; p = 0.0025) and oxygen pulse (oxygen uptake/heart rate approximates an indirect parameter for stroke volume; p = 0.0333) during exercise, whereas the maximal work performed was unchanged. Efficiency of breathing (ratio of tidal volume/inspiratory vital capacity) at maximal exercise improved significantly after operation ( p = 0.0005). Ventilatory limitation of exercise (defined by an increase in carbon dioxide tension during exercise) was found in 43.9% of the patients before operation. A tendency of improvement was noted (not significant) after operation (difference in carbon dioxide tension 0.6 ± 0.4 kPa before versus 0.3 ± 0.5 kPa after operation). However, the group with normal preoperative carbon dioxide elimination had a ventilatory limitation of exercise after operation (difference in carbon dioxide tension -0.4 ± 0.3 kPa before versus -0.1 ± 0.3 kPa after operation; p = 0.0128) with a significant increase in oxygen consumption ( p = 0.0007). In conclusion the subjective physical improvement after operation is not explained by changes in cardiorespiratory function at exercise. The data suggest a higher work of breathing after operation. (J THORAC CARDIOVASC SURG 1994;107:1403-9)
Surgical correction of pectus excavatum has been done mainly for cosmetic and psychologic reasons. However, many patients also have physical complaints, which have been suggested to be the result of decreased cardiac filling, 
1 stroke volume, 2 and work performance. 3 Despite an increased impairment of restrictive pulmonary function after operation, 4-6 relief of physical symptoms is commonly noted and improvement of cardiorespiratory function and exercise tolerance after operation have been demonstrated. 2,7,8 Most studies on dynamic cardiorespiratory function concern small series with varying operation techniques and study protocols. Follow-up studies are not done at a defined time after operation. 6,9
This study was done to assess the degree of eventual cardiorespiratory impairment by pectus excavatum and to investigate the value of surgical correction. In a prospective study pulmonary function and exercise cardiorespiratory function test results were compared before operation and at 1-year follow-up.
PATIENTS AND METHODS
Patient population
Thirty-five consecutive patients (28 male and 7 female), operated on between January 1989 and January 1991, participated in this study. Their ages ranged from 9.3 to 29.9 years (mean 17.9 ± 5.6 years). Each patient was studied at the initial evaluation and again 12 months after surgical repair.
Methods
Pulmonary function measurements consisted of total lung capacity by the helium dilution technique, inspiratory vital capacity, residual volume, functional residual capacity, forced expiratory volume in 1 second, ratio of forced expiratory volume in 1 second to vital capacity (Pulmonet III wet spirometer, Sensormedics, Bilthoven, The Netherlands), and single-breath carbon monoxide diffusing capacity (Sensormedics 2400, Bilthoven, The Netherlands). Values were expressed in percent predicted values of Zapletal and associates 10 for children and of the EuropeanCommunity of Coal and Steel 11 for adults.
Exercise testing was done on a previously calibrated, electronically braked cycle ergometer (Angio, Lode, Groningen, The Netherlands). The patient pedaled at 60 to 70 rpm with 1-minute incremental workload intervals. The increment of the workloads was based on 10% of the patient's expected performance. 12 All patients were encouraged to exercise to exhaustion. The degree of effort was assessed subjectively by one of the investigators (H.F.) during the test and objectively by comparing the patient's maximal heart rate (HR), blood gas values, and lactate production.
The following indices of cardiopulmonary function were recorded at rest, at every 3 minutes during exercise, at maximal exercise, and at 3 minutes after maximal exercise: HR, respiratory rate, blood pressure, oxygen uptake (VO 2), carbon dioxide output, minute ventilation, tidal volume, and systemic arterial blood gas values (blood samples from brachial artery [Corning 170, Medfield, Mass.]), and oxygen saturation (Oxyshuttle, Sensormedics, Bilthoven, The Netherlands). Ventilatory indices at rest and during exercise were measured with an Oxygen 4 apparatus (Mijnhart, Maarsbergen, The Netherlands). HR was computed by a Cardiorater electrocardiogram monitor (Cardiac Recorders Ltd., London, England).
The presence of sternal depression and the degree of depression were evaluated from the lateral chest radiographs. We used a modification of the vertebral index, described by previous workers, 13 to classify the deformity. On a line from the xiphisternal junction perpendicular on the vertebral body, the lower vertebral index (LVI) was calculated by dividing the vertebral body diameter at that level by the distance from the xiphisternal junction on the backside of the vertebral body. 14 Derveaux and colleagues 14 measured the LVI in a group of 250 healthy persons and found it to be age-dependent. Predicted values for the age groups can be calculated by the formula 0.193 (1 - 0.326 X e-0.258 x age). Age-corrected deviations from normal (
LVI) were calculated by dividing the difference between measured LVI and predicted LVI for that age by the standard deviation around the mean value at that age. A positive value means that the LVI is higher than normal and thus the posteroanterior diameter is less than normal.
Surgical technique
Our technique is based on the Daniel technique 15 with a fewmodifications. 16,17 The operation consists of subperichondral resection of all deformed rib cartilages, transverse sternotomy and division of the intercostal bundles at the outer limit of the chondrectomy, and suturing the edge of this broad sheet of muscle and perichondrium to the anterior surface of the chest wall more laterally and under tension, elevating and stabilizing the sternum, which is retrosternally supported by a homologous rib cartilage to provide for some overcorrection.
Statistical analysis
Categorical data were arranged in contingency tables, and the Fisher's exact test or the 
2 test was used for significance.Probability values (p values) less than 0.05 were considered significant. The test of McNemar was used for paired dichotomous observations. Continuous data were analyzed with the Kruskal-Wallis test, the Mann-Whitney U test, the signed rank test, and the Spearman rank correlation coefficient.
RESULTS
Symptoms
Cardiorespiratory symptoms were present in a considerable percentage of patients before operation. One year after operation most symptoms dissappeared or were less severe. Psychologic cosmetic complaints were also frequently seen and included feelings of shame, hiding the deformity, preoccupation, affected self-image, and verbal reactions on exposing the bare chest. These symptoms were also positively influenced by the operation (Table I).
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18 Type I symmetric and localized deformity was seen in 29.4% of patients, type II symmetric but diffuse deformity in 23.5%, and type III localized or diffuse asymmetric deformity in 47.1%. Deformity was considered severe in 58.8%, moderate in 29.4%, and mild in 11.8%.
Operative results
Results of operation were graded according to the method of Humphreys and Jaretzki 19 in which the cosmetic result and the presence of symptoms is taken into account. Satisfactory results were obtained in all patients.
Chest radiographic measurements
Measurements of sternal depression on lateral chest radiographs are detailed in Table II. When corrected for age (d), the LVI was higher than predicted (p = 0.0000), reflecting a smaller posteroanterior diameter at that level. The diameter significantly increased after operation (p < 0.0001), but was still smaller than predicted for that age (p = 0.0001). There was no significant relation between severity, as established by physical examination, and LVI. No significant relationship was found between preoperative LVI and preoperative static pulmonary function measurements. There was no relation between postoperative increase in posteroanterior diameter and postoperative changes in static pulmonary function test results.
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Table III. Total lung capacity and inspiratory vital capacity were significantly smaller than predicted before operation. Because both actually measured values and predicted values changed because of the operation and growth, respectively, the postoperative changes are given as percentages of predicted. Pulmonary function further decreased after operation. No change was found in airway patency (forced expiratory volume in 1 second/inspiratory vital capacity) after operation.
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Table IV).
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20 The arterial pH and base excess (BE) displayednormal patterns with increasing exercise. 20 The "change" of PaO 2 and PaCO 2 during exercise was expressed by its value at maximum exercise minus its value at rest (PaO 2 and PaCO 2) and preoperative and postoperative mean values are listed in Table V. The pH and BE are measured as the value at 3 minutes after maximal exercise minus the value at rest, inasmuch as they are the result of intracellular lactate production, which takes some time to be measured in the arterial blood. Most changes during exercise were similar for both preoperative and postoperative studies, except for pH, which increased significantly after operation.
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Table V). Values for VO 2 and VO 2/kg at rest were not different before and after operation (difference of postoperative minus preoperative value for VO 2; -0.034, p = 0.3277; for VO 2/kg; -0.248, p = 0.6984). At maximal exercise, oxygen consumption significantly increased after operation (preoperative value 31.1 ± 2.0 ml/min/kg, postoperative value 34.0 ± 8.1 ml/min/kg; p = 0.0035).
At maximal exercise, ventilatory frequency (breaths/ minute) did not significantly change after operation; however, minute ventilation (BTPS*; liters/minute) increased significantly (Table V). Ventilatory equivalent for oxygen (minute ventilation/VO 2) at maximal exercise was not different for both groups (28.4 ± 7.0 versus 28.3 ± 6.3). Efficiency of ventilatory gas exchange was calculated by dividing the ratio of tidal volume (minute ventilation/ventilatory frequency) at maximal exercise by measured inspiratory vital capacity and was found to improve significantly after operation (0.39 ± 0.08 versus 0.45 ± 0.09; p = 0.0005). The change of dead space volume as a ratio of tidal volume during exercise was not different when compared before and after operation (Table V).
Diffusion capacity was assessed by the alveolar-arterial oxygen tension difference (A-aDO 2). The change of A-aDO2 during exercise as expressed by its value at maximum exercise minus its value at rest (A-aDO2) is detailed in Table V. No significant deviation was found.
Physical fitness was approximated by the ratio of maximal work level/HR and maximal work level/BE (Table VI). No significant differences were found between preoperative and postoperative values.
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PaCO 2 greater than 0 and was found in 43.9% (15 of 35) of the patients before operation versus 46.9% (15 of 32) after operation. Exercise characteristics of this specific group of patients are detailed in Table VII, A. A tendency of improvement (not significant) is noted after operation (PaCO 2 0.61 ± 0.46 kPa before versus 0.31 ± 0.50 kPa after operation). Exercise characteristics of the patients without ventilatory limitation (PaCO 2 of 0 or less) are listed in Table VII, B. In this group, elimination of carbon dioxide was found to be significantly reduced at exercise after operation with significant increases in VO 2 and consequently in carbon dioxide production and minute ventilation. In 4 of 32 patients a preoperative ventilatory limitation of exercise disappeared. In 5 of 32 patients a ventilatory limitation was present after operation, which was not present in the preoperative state. In 23 of 32 no change occurred in the ventilatory status at maximal exercise.
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21 was observed in 22.9% of patients before and 36.4% after operation (not significant). For this specific group of patients forced expiratory volume in 1 second/inspiratory vital capacity and maximal expiratory flow at 50% of inspiratory vital capacity, both expressed as percentage of predicted, were compared with the values in patients without this phenomenon, before and after operation. No significant difference was found in forced expiratory volume in 1 second/inspiratory vital capacity and maximal expiratory flow at 50% of inspiratory vital capacity, both determined as a percentage of predicted, between patients with or without "second wind" or before or after operation. DISCUSSION
Restrictive impairment of pulmonary function, expressed by reduced total lung capacity and inspiratory vital capacity, is commonly noted in pectus excavatum, 6,7,22 although normalfunctions are also found. 5,23 We also found evidence of a restricted ventilation, which was not ameliorated by operation. The significant reduction in total lung capacity and inspiratory vital capacity after operation was also found by others 3,5,6,24 and is probably a result of increased postoperative restriction of the chest wall. 3,5,14
The commonly found symptomatic improvement after operation is difficult to explain, 7,8,17 when despite a significant increase of posteroanterior diameter of the chest, as found in this study, lung volumes demonstrate a definite decrease after operation.
Castile, Staats, and Westbrook 22 found that VO 2 during exercise exceeded predicted values at greater work loads in five patients with symptomatic pectus excavatum, whereas two patients without symptoms did not show the same process. These investigators suggested that these findings in patients with symptomatic deformities were caused by decreased chest wall compliance and an increased work of breathing. However, in experimental studies by Mead and associates 25 no difference in chest wall compliance was found between patients with pectus excavatum and normal persons. In exercise studies on 19 patients with pectus deformities, Cahill, Lees, and Robertson 7 reported a significant improvement in total exercise time and maximal VO 2 after operation in 14 patients with pectus excavatum, whereas no change was observed in 5 patients with pectus carinatum. In addition, at any given HR, the patients with pectus excavatum demonstrated a lower HR and higher minute ventilation after operation. In contrast, Gyllensward and colleagues 3 found no significant differences between normal subjects and patients with pectus excavatum compared before and after operation with regard to exercise tolerance assessed by the work performed at a HR of 170 beats/min. Wynn and associates 6 stressed the importance of studying patients at a defined time after operation, thereby controlling for changes in somatic size and physical fitness. They also provided for a control group of four patients not operated on. Exercise duration and work performed (percent of predicted) increased significantly in a small group of eight patients after surgical correction. Although not significant, there was a small increase in maximal VO 2 and a slight increase in minute ventilation in both groups.
In our study, a large group of patients with pectus excavatum was studied before and 1 year after operation. Rather than indexing values for body size we prefer to measure the change during exercise, expressed as the value at maximum exercise minus the value at rest. 20 After operation a significant increase was found inmaximal VO 2 during exercise, whereas the maximal work performed was unchanged. We further noticed a slightly higher increase in BE (lactate), a minimally greater increase in PaCO 2, and a significant decrease in pH after operation, showing significantly higher acidification during exercise. Because the maximal work load was virtually unchanged after operation, this might indicate that relatively more anaerobic work had to be done for the same exercise performance. Because the oxygen uptake at rest was unchanged, the significant increase in VO 2 after operation together with increased acidification at exercise may suggest that more muscle activity is needed at maximal exercise that does not contribute to external work load, which may indicate an increased activity of the ventilatory musculature. This is supported by the observation that minute ventilation was significantly increased after operation. Ventilatory equivalent for oxygen did not change, reflecting an unchanged extraction of oxygen, despite a further decrease of total lung capacity and inspiratory vital capacity after operation. At maximal exercise, the efficiency of breathing expressed in terms of the ratio tidal volume/inspiratory vital capacity improved significantly after operation, suggesting a reduction of dead space ventilation. However, when measuring the change in dead space volume as a ratio of tidal volume during exercise using the Bohr equation, we found no difference between preoperative and postoperative values. The increased work of respiration in patients with pectus excavatum after operation in studies mentioned herein, which was also found in our study, was considered to be caused by decreased chest wall compliance after operation.
In the group with preoperative ventilatory limitation we noted a tendency of improvement after operation (not significant), without a change in oxygen consumption. It is striking, however, that the group with normal preoperative carbon dioxide elimination had a ventilatory limitation after operation, with a significant increase in oxygen consumption and consequently in carbon dioxide production. Minute ventilation also increases, but not enough to cope with the increased carbon dioxide production, resulting in a rise in PaCO 2. Because the external workload is unchanged, the extra oxygen consumption is most probably needed for the extra ventilation.
In this study the increase during exercise of the oxygen pulse, as an indirect parameter for stroke volume, was significantly greater after operation. Increase in oxygen pulse is a result of an increase in stroke volume and/or an increase in arterial–mixed venous oxygen difference (Fick equation). Increased arterial–mixed venous oxygen difference would indicate a higher peripheral oxygen extraction. The peripheral working muscles would be more hypoxic, which would lead to an increased lactate and BE. Because this was not found, it is highly likely that the increased oxygen pulse is a result of increased stroke volume. Previous studies have clearly shown a reduced stroke volume response during exercise in patients with pectus excavatum. 1-3 Bevegård 1 demonstrated a lower increase in stroke volume from rest to exercise in patients with pectus excavatum, as compared with that in normal subjects. He attributed this impaired ventricular filling to a lower efficiency of the respiratory pump. Beiser and colleagues 2 provided more evidence that the cardiac function of patients with pectus excavatum is impaired during exercise. Cardiac catheterization in a small group of patients with pectus excavatum showed a significant increase in the cardiac index after operation when they performed exercise in a sitting position, presumably on the basis of an increased stroke volume. The observed decrease in HR at any given work rate after operation, as observed by Cahill, Lees, and Robertson, 7 would support the hypothesis that some of the improvement in exercise capacity is the result of an increase in cardiac stroke volume. In contrast, Peterson and associates 8 found no effect of operation on cardiac index or left and right ventricular ejection fraction at rest or during exercise. These findings are consistent with those of studies in which no apparent abnormalities of cardiac output or stroke volume responses were found at rest or during exercise in patients with pectus excavatum either before or after operation as compared with those responses in normal subjects. 6,26
In conclusion this study was unable to clarify the subjective physical improvement that is commonly found after surgical correction of pectus excavatum. Preoperative lung function was found to be restricted. Despite an increase of restriction after operation, the work performance was unchanged. Oxygen consumption at exercise increased, most probably as a result of a higher work of breathing.
References
This article has been cited by other articles:
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  M. H. Malek, D. E. Berger, W. D. Marelich, J. W. Coburn, T. W. Beck, and T. J. Housh Pulmonary function following surgical repair of pectus excavatum: a meta-analysis. Eur. J. Cardiothorac. Surg., October 1, 2006; 30(4): 637 - 643. [Abstract] [Full Text] [PDF]
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 H. Iida, Y. Sudo, Y. Yamada, Y. Matsushita, K. Eda, and Y. Inoue Nonprosthetic Surgical Repair of Pectus Excavatum Ann. Thorac. Surg., August 1, 2006; 82(2): 451 - 456. [Abstract] [Full Text] [PDF]
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 M. H. Malek, D. E. Berger, T. J. Housh, W. D. Marelich, J. W. Coburn, and T. W. Beck Cardiovascular function following surgical repair of pectus excavatum: a metaanalysis. Chest, August 1, 2006; 130(2): 506 - 516. [Abstract] [Full Text] [PDF]
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 B. Wallaert, B. Cavestri, C. Fournier, R. Neviere, and B. Aguilaniu Positional hyperventilation-induced hypoxaemia in pectus excavatum. Eur. Respir. J., July 1, 2006; 28(1): 243 - 247. [Abstract] [Full Text] [PDF]
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M. H. Malek, E. W. Fonkalsrud, and C. B. Cooper Ventilatory and Cardiovascular Responses to Exercise in Patients With Pectus Excavatum Chest, September 1, 2003; 124(3): 870 - 882. [Abstract] [Full Text] [PDF]
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 J. Kowalewski, M. Brocki, T. Dryjanski, K. Zolynski, and R. Koktysz PECTUS EXCAVATUM: INCREASE OF RIGHT VENTRICULAR SYSTOLIC, DIASTOLIC,AND STROKE VOLUMES AFTER SURGICAL REPAIR J. Thorac. Cardiovasc. Surg., July 1, 1999; 118(1): 87 - 93. [Abstract] [Full Text] [PDF]
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 A. Chandra, S. Srivastava, and D. Dilip Spirometric Changes Following Open-Heart Surgery on Rheumatic Mitral Valves Asian Cardiovasc Thorac Ann, March 1, 1998; 6(1): 28 - 33. [Abstract] [Full Text] [PDF]
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J. Kowalewski, S. Barcikowski, and M. Brocki Cardiorespiratory function before and after operation for pectus excavatum: Medium-term results Eur. J. Cardiothorac. Surg., March 1, 1998; 13(3): 275 - 279. [Abstract] [Full Text] [PDF]
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