International Journal of Cardiology, 31(1992) 15-21 6 1991 Elsevier Science Publishers B.V. All rights reserved
CARD10
15 0167-5273/92/$05.00
01530
Lung function in atria1 septal defect after heart surgery J. sulc, M. Samhek Kardiocentntm, (Received
and A. Zapletal
University Hospital Motel, Prague. Czechosloc)akia
18 November
1991; revision
accepted
14 April 1992)
Sulc J, Samanek M, Zapletal A. Lung function in atria1 septal defect after heart surgery. Int J Cardiol 1992;37:15-21. Lung volume, indices of lung elasticity and airway patency were measured in 74 patients, 9-21 yr old (15.0 k 2.5 yr) with atria1 septal defect (secundum type) from 2-11 (5.1 k 2.5) yr after successful surgical correction. Clinical condition in all patients was classified as excellent. Heart surgery was performed at the age of 4-14.8 (9.9 $- 3.0) yr. Lung function abnormalities were found in 35 (47.3%) patients. Lung recoil pressure was significantly increased in 24 (32.4%) patients. The mean value of lung recoil pressure at 100% of total lung capacity reached 123 f 31% of the predicted value (P < 0.0001). Specific static compliance was within normal limits. Specific airway conductance was significantly reduced in 13 (17.6%) patients. Maximum expiratory flow at 25% of vital capacity was significantly reduced in 4 (5.4%) patients. Static lung volumes did not differ from reference values. Since various abnormalities of lung function tests (most frequently the tests suggested increased lung stiffness and obstruction of larger airways) were revealed in almost half of the studied children and adolescents after successful surgery for atria1 septal defect, we propose to carry out lung function tests routinely as another criterion of health conditions in these patients. Key words: Atria1 septal defect; Lung function tests
Introduction In atria1 septal defect the lungs are exposed to an increased blood flow. Pulmonary-to-systemic blood flow ratio can reach a value as high as 4: 1, but pulmonary arterial pressure remains normal or may be only moderately increased during childhood. The small pulmonary arteries are di-
Correspondence fo: J. sulc. Kardiocentrum, University Hospital Motel. V ivalu 84. 150 18 Prague 5, Czechoslovakia. Tel. 02-526581, 02-526588. Fax 42-Z-520081.
lated due to an increased blood flow and pulmonary vascular resistance is normal. A large spectrum of changes in lung function has been reported in adults and adolescents with atria1 septal defect. Both reduced and normal vital capacity and total lung capacity were observed [l-51. Increased, normal or decreased residual volume and ratio of functional residual to total lung capacity were found [2,5,6]. As expected in patients with a high pulmonary blood flow and volume, increased lung diffusion capacity was reported in the majority of studies accompanied by a decrease of lung diffusion capacity in
some [7]. Central and/or peripheral airway obstruction was revealed in patients with atria1 septal defect [2,5,6]. Reduced lung compliance was reported in some studies [2,4,6,8-121, but with almost equal frequency normal or increased lung compliance was observed [7,13-171. The latter divergencies in lung function tests might be due to differences in the methods and the subjects of the study. In all studies except one [2], lung compliance has been reported as the only indicator of lung elasticity, and moreover, was measured mostly under dynamic conditions. In some studies the assessment of airway obstruction was limited to the measurement of forced vital capacity and one-second forced expiratory volume [3,14,18]. Lung function disturbances in children with atria1 septal defect were also evaluated, mostly by simple lung function tests [4,8,11,15,19]. Inhomogeneity of the investigated patients, resulting from a wide age range and a large scatter of disturbances in pulmonary hemodynamics including high pulmonary arterial pressure [7,131, might also explain some differences in the results. The majority of lung function tests in patients with atria1 septal defect were performed in adults or adolescents. Children and infants were investigated less frequently [15,19] and some reports are based on only a very limited number of patients [9,11,15,19,20]. We did not find any study that was carried out in a representative number of children and adolescents with atria1 septal defect, by using a larger spectrum of lung function tests. The data on lung function tests after cardiac surgery for atria1 septal defect in children and adolescents are even more scarce than the data on lung function prior to surgery [16,19]. The aim of this study was to assess lung function in children and adolescents after a successful cardiac surgery for atria1 septal defect by using a larger variety of methods. We measured static lung volume, airway resistance, maximum expiratory flow rate, lung recoil pressure and static lung compliance. Materials
and Methods
Lung function was studied in 74 children (22 males, 52 females) after heart surgery for atria1
septal defect (secundum type). All patients were in excellent clinical condition at time of the study; the youngest patient was 9 and the oldest 21 yr old (15.0 k 2.5 yr). Body height varied from 125 to 185 cm with a mean of 163 (SD + 12) cm. Heart surgery was performed at the mean age of 9.9 f 3.0 (range 4.0-14.8) yr, either by direct suture (26 patients) or by pericardial patch (48 patients). Preoperative cardiac catheterization data were available in 26 patients. The mean pulmonary arterial pressure was normal (16.5 ? 4.7 mmHg). Pulmonary vascular resistance was within normal limits (1.3 + 0.7 U/m’ of body surface area). Left-to-right shunt prior to surgery was measured either at heart catheterization or by the radionuclide dilution method in 72 patients. The value of left-to-right shunt ranged between 20-75% of pulmonary blood flow (49 & 12). Mean extracorporeal circulation time was 43 _t 12 min (range 22-721, cross-clamping time was 22 ~fr9 min (range 8-49). The average duration of mechanical ventilatory support postoperatively was 10 f 5 h (range 0.5-21). The time interval from surgery to the lung function testing varied from 1.9-11.3 yr with a mean of 5.1 (SD -t 2.5) yr. Static lung volumes were derived from the measurements of thoracic gas volume in a body plethysmograph (Bodytest, Jaeger) and from lung volumes measured from the expiratory pressurevolume curve (see below). The highest vital and inspiratoty capacities taken as representative values in a subject were used for calculation of other lung volumes. Functional residual capacity was measured at end-expiratory level as thoracic gas volume. Total lung capacity was obtained as a sum of thoracic gas volume plus inspiratory capacity. Residual volume was calculated as total lung capacity minus vital capacity. Airway resistance was measured during quiet breathing simultaneously with thoracic gas volume in a body plethysmograph. It was converted to its reversal value (i.e. airway conductance), and expressed per unit of thoracic gas volume as “specific” airway conductance. Maximum expiratory flow-volume curves were obtained by recording expiratory flow rates versus lung volume changes. Patients performed a complete and rapid
17
by the shutter valve for 0.3 s. At least 5 technically good pressure-volume curves were obtained in each patient. From pressure-volume curves, lung recoil pressure was measured at 100, 90 and 60% of total lung capacity. Static lung compliance as another index of lung elasticity was obtained from the slope of the middle linear part of the pressure-volume curve. Static lung compliance expressed per unit of total lung capacity gave the value of “specific” lung compliance. The results were compared with the reference values on the basis of body height obtained in the same laboratory [21]. flow
expiration to residual volume level after maximal inspiration. At least 5 technically good curves were recorded and from these the “envelope” curve as the representative one for a subject was analyzed. From maximum expiratory flow-volume curves we measured forced vital capacity, peak expiratory flow rate, maximum expiratory flow rates at 25, 50 and 75% of forced vital capacity and at 60% of total lung capacity. We also calculated ratios of maximum expiratory flow rates and total lung capacity in order to correct the absolute values of flow rates in liters/second for lung size. Lung elasticity was assessed from the expiratory pressure-volume curves obtained as a simultaneous recording of transpulmonary pressure (measured as a difference between esophageal and mouth pressures) and lung volume changes. A latex esophageal balloon (wall thickness up to 0.1 mm, length 100 mm) was situated in the lower third of the esophagus. Detailed information was published elsewhere 1211. The pressure-volume curves were recorded at quasi-static conditions during very slow expiration with interrupted air-
TABLE
Data were analysed by using the statistical program STATGRAPHICS, version 5 (1991). The comparison of two samples (Mann-Whitney test) and the two-sample analysis test (t-test) were used. All data are presented as means _t SD. The level of statistical significance was set at P = 0.05. The results of lung function tests were further expressed as a percentage of predicted value.
1
Lung function
test results
Lung function
test
(n = 74, body height
RV/TLC Lung recoil pressure at 100% of TLC at 90% of TLC at 60% of TLC Static lung compliance/TLC expiratory
125-185). Predicted
value t%)
P
mean
SD
mean
*SD
3 63 1 (ml) 4 644 (ml) 2325 (ml) 1050 (ml) 49.3 (%I
856 104s 590 363 5.2
101 100 100 94 100
1.5 14 19 27 11
NS NS NS NS NS
22.3 t%)
6.5
94
26
NS
47.2 (cmH,O) 21.3 (cmH,O) 9.9 (cmH,O) 0.037 (ml~cmH,O~l~ml~‘)
12.5 4.4 2.2 0.010
123 107 114 101
31 20 23 29
< 0.0001 < 0.05 < 0.0001 NS
0.497(l~s~t~l-‘) o.975(l.s-t.l~‘) 0.986(I.s-‘.I-‘) 6.50.~~‘) 0.166 11 .s--’ cmH,O-’
0.166 0.278 0.313 1.9 0.064
110 114 119 99 84
35 29 35 22 32
< 0.01 < 0.0001 < 0.0001 NS < 0.0001
flow rate
25% VC/TLC 50% VC/TLC 60% TLC/TLC Peak expiratory flow rate Specific airway conductance
VC = vital capacity;
163 f 11.9 cm, range
Atria1 septal defect
vc TLC FRC RV FRC/TLC
Maximum
Statistics
TLC = total lung capacity;
I-‘)
FRC = functional
residual
capacity;
RV = residual
volume.
18
Presurgical hemodynamic and perioperative data in the patients were correlated with lung function data by the use of simple and multiple regression analysis.
TABLE 2 Incidence of abnormal lung function tests (n = 74). Lung function test
Results Lung volumes The mean values of vital capacity, total lung capacity, functional residual capacity, residual volume and functional residual capacity to total lung capacity ratio did not differ from the reference values (Table 1).
Static recoil pressure at 100% TLC at 90% TLC at 60% TLC Specific airway conductance TLC vc FRC/TLC RV/TLC Maximum expiratory flow rate at 25% VC/TLC
Airway patency A significant decrease up to 84% (SD _t 32) of the predicted value (P < 0.0001) was found for specific airway conductance (Table 1). Peak expiratory flow rate reached 99.9% of the predicted value. Maximum expiratory flow rates expressed per unit of total lung capacity and measured at 25, 50% of vital capacity and 60% of total lung capacity were even higher than the reference values. Lung elasticity The mean values of lung recoil pressure measured at 100, 90 and 60% of total lung capacity were significantly increased (Table 1). The most significant increase of lung recoil was observed at the level of 100% of total lung capacity (123% of predicted value). Lung recoil pressure at 60% of total lung capacity reached 114% of the predicted value. Lung recoil pressure at 90% of total lung capacity was 107% of the predicted value (P < 0.05). The value of specific static lung compliance was normal. Frequency of abnormal lung function tests Abnormal lung function tests (i.e. deviating by more than k2 SD from the mean normal value) were found in 35 (47.3%) of 74 patients (Table 2). Lung recoil pressure was increased in 24 patients
Abnormal value (change)
Patients No.
%
decrease decrease decrease increase increase
24 14 9 13 9 7 3 4
32.4 18.9 12.2 17.6 12.2 9.5 4.1 5.4
decrease
4
5.4
35
47.3
increase
Total Abbreviations as Table 1.
(32.4%) and decreased in 2 patients, respectively. Maximum expiratory flow rates were reduced in 4 (5.4%) patients. Specific airway conductance was reduced in 13 (17.6%) patients. Vital capacity and total lung capacity were significantly decreased in 7 (9.5%) and 9 (12.2%) patients, respectively. The functional residual to total lung capacities and residual volume to total lung capacity ratios were increased significantly in 3 (4.1%) and 4 (5.4%) patients, respectively. Effect of preoperative pulmonary hemodynamics and perioperative treatment on lung function According to the preoperative hemodynamic data, the patients were arbitrarily divided into two groups, i.e. with a moderate increase (leftto-right shunt < 50% of pulmonary blood flow) and severe increase (left-to-right shunt > 50% of pulmonary blood flow) in pulmonary blood flow. More frequently (i.e. in 50% of patients) the abnormalities of lung function were found in a group with a severe increase in pulmonary blood flow. The incidence of lung function abnormalities in a group with a moderate increase in pulmonary blood flow was lower (i.e. in 44% of patients). The differences in the latter frequencies were not statistically significant.
19
There was a short duration of mechanical ventilation in most patients after surgery for atria1 septal defect. In only 13 patients, a ventilatory support lasted more than 15 h. The incidence of lung function disturbances did not differ from that observed in our whole group of patients, i.e. abnormal values of lung function tests were revealed in 6 (46%). A positive linear correlation between the ratio of functional residual capacity to total lung capacity and the time period of postoperative ventilatory support (Y = 0.415, P < 0.00, as well as a negative linear correlation between specific airway conductance and the time period of ventilatory support (r = -0.396, P < 0.041, were revealed in 42 patients with the preoperative severe increase of pulmonary blood flow. In the same patients positive linear correlations between age at surgery and static lung volumes (vital and total lung capacity) (1. = 0.424, P < 0.01 and r = 0.310, P < 0.051, were found. Negative linear correlations between the time period of mechanical ventilatory support and vital capacity (r = - 0.599, P < O.OOl>,as well as total lung capacity (r = - 0.430, P < 0.031, were observed in 32 patients with a moderate increase in pulmonary blood flow. A positive linear correlation between age at surgery and total lung capacity (Y = 0.377, P < 0.05) in the same patients was also found. Any other correlation between age at surgery, time period of surgery-to-testing and lung function parameters was not found. Discussion In almost one half of our patients lung function disturbances were revealed, despite effective surgical treatment and excellent clinical conditions at the time of lung function testing. Increased lung stiffness and obstruction of central airways were the most frequent findings. Reduced dynamic lung compliance considered as an indicator of stiff lung was found after surgery for atria1 septal defect also by Haughton [16], but the measurement was performed in the early postoperative period (up to 35 postoperative days). On the other hand, in 4 of 7 adult patients with atria1
septal defect after surgery reported by Davies and Gazetopoulos [14] there was a rise in dynamic compliance. Elastic lung recoil pressure measured at three different levels of total lung capacity is a more sensitive parameter in detecting of lung elasticity abnormalities than specific static lung compliance as was published in detail elsewhere [21]. The most pronounced deviation from the predicted value was revealed in lung recoil pressure measured at 100% of total lung capacity. Lung recoil pressure at lower levels of total lung capacity was less abnormal. Static lung compliance was even normal. Lung stiffness assessed by lung recoil pressure measurement in our patients was less pronounced than that observed in the patients with simple transposition of the great arteries [22] or with ventricular septal defect (unpublished paper). The increased lung recoil pressure indicating increased lung stiffness has been observed as the most typical finding in patients with idiopathic pulmonary fibrosis [21] having characteristic histological features. However, lung biopsy was not carried out in our patients with atria1 septal defect. Therefore, it is rather difficult to draw any conclusion on anatomical abnormalities of the lung parenchyma causing the observed increase of lung recoil pressure. We might hypothesize, that the growth of the elastic and collagen tissue can be changed in a developing lung exposed to an increased pulmonary blood flow since birth [2,23]. The increase in pulmonary blood flow, accompanied by an increased blood volume [24] and engorgement of the capillary network, might also contribute to the abnormalities in the elastic properties of the lung [6,25]. There is no reason to explain the increased lung stiffness by the surgical procedure itself. The hear: and thorax were always exposed by central sternotomy, thus avoiding any damage of the lungs. A reduced maximal expiratory flow rate at 25% of vital capacity found in only 5% of our patients, implied a normal patency of peripheral airways in the majority of patients after surgery for atria1 septal defect. It might be due to the normalizing of pulmonary blood flow and volume. Another relevant observation was a decreased airway conductance indicating an obstruction of
20
the larger airways in 18% of our patients. A tracheal intubation (especially followed by possible infection) may be a cause of airway obstruction [26]. Although only a short period of mechanical ventilation (OS-21 h) in our group was ascertained, we assume that it might be harmful, resulting in specific conductance reduction but clinically silent. Hyperinflation, indicated by increased ratios of functional residual to total lung capacities, and of residual volume to total lung capacity and observed in 5% of our patients, was similar in adults with uncorrected atria1 septal defect [2,5,6]. The abnormal pulmonary hemodynamics characterized by high pulmonary blood flow preoperatively and the postoperative mechanical ventilation might also contribute on these abnormalities. This assumption is supported by the positive linear correlation between functional residual to total lung capacities ratio and duration of mechanical ventilation (r = 0.415, P < 0.01). Other parameters of lung function were normal in the majority of patients. This is in accordance with their excellent clinical condition. The disturbance of lung function in about half of our patients after a successfully corrected atria1 septal defect, led to some doubts about the generally accepted opinion that this cardiac malformation is one of a few perfectly correctable congenital heart diseases.
Acknowledgments We thank Marie Spirova and Kvi?ta Kozerova for technical assistance during the study.
References Bedell GN, Adams RV. Pulmonary diffusing capacity during rest and exercise. A study of normal persons and persons with atria1 septal defect, pregnancy and pulmonary disease. J Clin Invest 1962,41:1908-1914. DeTroyer A, Yernault J-C, Engkert M. Mechanics of breathing in patients with atria1 septal defect. Am Rev Resp Dis 1977;15:413-421. Schofield PM, Barber PV. Kingston T. Preoperative and postoperative pulmonary function tests in patients with atria1 septal defect and their relation to pulmonary artery
pressure and pulmonary:systemic flow ratio. Br Heart J 1985;54:577-582. 4 Turin0 GM. Pulmonary distensibility in mitral stenosis and congenital heart disease. J Clin Invest 1956;35:740. 5 Yoshioka T, Kunieda T, Naito M. Fukunaga Y, Okubo S, Nakanishi S. Effects of pulmonary hemodynamics on lung function in adult patients with atrial septal defect. Jap Circ J 1985;49:960-966. P, Anthonisen NR, Macklem PT. 6 Wood TF, McLeod Mechanics of breathing in mitral stenosis. Am Rev Resp Dis 1971;104:52-60. 7 Mcllroy MB, Apthorp GH. Pulmonary function in pulmonary hypertension. Br Heart J 19X$20:397-402. 8 Ayres SM, Kozam RL, Lukas DS. Mechanics and work of breathing in atrial septal defect. Circulation 1960;22:718719. 9 Girardet JP, Gaultier C, Boule M, Magnier S, Duclos M, Fontaine JL. Perturbations fonctionnelles respiratoires chez les enfants porteurs de cardiopathies avec shunt gauche-droite. Arch Mal Coeur 1981;74:1147-1155. JM, Verstraeten J, Pannier R. La compliance 10 Verstraeten pulmonaire chez les sujets adultes presentant une cardiopathie congenitale. Arch Mal Coeur 1964;57:1409-1420. 11 Wallgren G, Geubelle F, Koch G. Studies of the mechanics of breathing in children with congenital heart lesions. Acta Paediat 1960;49:415-425. 12 Woolf CR. Pulmonary function in adults with intracardiac septal defect. Circulation 1963;27:261-267. 13 Davies H, Williams J, Wood P. Lung stiffness in states of abnormal pulmonary blood flow and pressure. Br Heart J 1962:24:129-138. N. Lung function in patients with 14 Davies H, Gazetopoulos left-to-right shunts. Br Heart J 1967;29:317-326. 15 Griffin AJ, Ferrara JD, Lax JO, Cassels DE. Pulmonary compliance - an index of cardiovascular status in infancy. Am J Dis Child 1972;123:89-95. V. Changes in pulmonary compliance in pa16 Haughton tients undergoing cardiac surgery. Dis Chest 1968;53:617628. 17 Larmi TKI, Appelquist R. The influence of cardiac surgery on the mechanical properties of the lungs. Stand J Clin Lab Invest 1961:13:174-179. 18 Cowen ME, Jeffrey RR, Drakeley MJ, Mercer JL, Meade JB, Fabri BM. The results of surgery for atria1 septal defect in patients aged fifty years and over. Eur Heart J 1990;11:29-34. 19 Bucci G, Cook CD. Studies of respiratory physiology in children. VI. Lung diffusing capacity, diffusing capacity of the pulmonary membrane and pulmonary capillary blood volume in congenital heart disease. J Clin Invest 1961;40:1431-1441. 20 Bancalari E, Jesse MJ, Gelband H, Garcia 0. Lung mechanics in congenital heart disease with increased and decreased pulmonary blood flow. J Pediat 1977;90:192195. 21 Zapletal A, Samanek M, Paul T. Lung function in children and adolescents. Basel: Karger, 1987.
21 22 Samhnek M, Sulc J, Zapletal A. Lung function in simple complete transposition after intracardiac repair. Int J Cardiol 1989;24:13-17. 33 Rabinowitch M, Keane JF, Norwood WI, Castaneda AR, Reid L. Vascular structure in lung tissue obtained at biopsy correlated with pulmonary hemodynamic findings after repair of congenital heart defects. Circulation 1984;69:655-667. 24 Englert M. Pulmonary capillary blood volume in conditions with high pulmonary blood flow: pneumonectomy
and congenital cardiac malformations with left to right shunt. In: Progr. Resp. Res., vol. 5. Basel: Karger. 1970;338-345. 25 Giannelli S, Ayres SM. Buehler ME. Effect of pulmonary blood flow upon lung mechanics. J Clin Invest 1967;46:1625-1642. 26 Corno A. Giamberti A, Giannico S et al. Airway obstruction associated with congenital heart disease in infancy. J Thor Cardiovasc Surg 1990;99:1091-1098.
CARD10
15 0167-5273/92/$05.00
01530
Lung function in atria1 septal defect after heart surgery J. sulc, M. Samhek Kardiocentntm, (Received
and A. Zapletal
University Hospital Motel, Prague. Czechosloc)akia
18 November
1991; revision
accepted
14 April 1992)
Sulc J, Samanek M, Zapletal A. Lung function in atria1 septal defect after heart surgery. Int J Cardiol 1992;37:15-21. Lung volume, indices of lung elasticity and airway patency were measured in 74 patients, 9-21 yr old (15.0 k 2.5 yr) with atria1 septal defect (secundum type) from 2-11 (5.1 k 2.5) yr after successful surgical correction. Clinical condition in all patients was classified as excellent. Heart surgery was performed at the age of 4-14.8 (9.9 $- 3.0) yr. Lung function abnormalities were found in 35 (47.3%) patients. Lung recoil pressure was significantly increased in 24 (32.4%) patients. The mean value of lung recoil pressure at 100% of total lung capacity reached 123 f 31% of the predicted value (P < 0.0001). Specific static compliance was within normal limits. Specific airway conductance was significantly reduced in 13 (17.6%) patients. Maximum expiratory flow at 25% of vital capacity was significantly reduced in 4 (5.4%) patients. Static lung volumes did not differ from reference values. Since various abnormalities of lung function tests (most frequently the tests suggested increased lung stiffness and obstruction of larger airways) were revealed in almost half of the studied children and adolescents after successful surgery for atria1 septal defect, we propose to carry out lung function tests routinely as another criterion of health conditions in these patients. Key words: Atria1 septal defect; Lung function tests
Introduction In atria1 septal defect the lungs are exposed to an increased blood flow. Pulmonary-to-systemic blood flow ratio can reach a value as high as 4: 1, but pulmonary arterial pressure remains normal or may be only moderately increased during childhood. The small pulmonary arteries are di-
Correspondence fo: J. sulc. Kardiocentrum, University Hospital Motel. V ivalu 84. 150 18 Prague 5, Czechoslovakia. Tel. 02-526581, 02-526588. Fax 42-Z-520081.
lated due to an increased blood flow and pulmonary vascular resistance is normal. A large spectrum of changes in lung function has been reported in adults and adolescents with atria1 septal defect. Both reduced and normal vital capacity and total lung capacity were observed [l-51. Increased, normal or decreased residual volume and ratio of functional residual to total lung capacity were found [2,5,6]. As expected in patients with a high pulmonary blood flow and volume, increased lung diffusion capacity was reported in the majority of studies accompanied by a decrease of lung diffusion capacity in
some [7]. Central and/or peripheral airway obstruction was revealed in patients with atria1 septal defect [2,5,6]. Reduced lung compliance was reported in some studies [2,4,6,8-121, but with almost equal frequency normal or increased lung compliance was observed [7,13-171. The latter divergencies in lung function tests might be due to differences in the methods and the subjects of the study. In all studies except one [2], lung compliance has been reported as the only indicator of lung elasticity, and moreover, was measured mostly under dynamic conditions. In some studies the assessment of airway obstruction was limited to the measurement of forced vital capacity and one-second forced expiratory volume [3,14,18]. Lung function disturbances in children with atria1 septal defect were also evaluated, mostly by simple lung function tests [4,8,11,15,19]. Inhomogeneity of the investigated patients, resulting from a wide age range and a large scatter of disturbances in pulmonary hemodynamics including high pulmonary arterial pressure [7,131, might also explain some differences in the results. The majority of lung function tests in patients with atria1 septal defect were performed in adults or adolescents. Children and infants were investigated less frequently [15,19] and some reports are based on only a very limited number of patients [9,11,15,19,20]. We did not find any study that was carried out in a representative number of children and adolescents with atria1 septal defect, by using a larger spectrum of lung function tests. The data on lung function tests after cardiac surgery for atria1 septal defect in children and adolescents are even more scarce than the data on lung function prior to surgery [16,19]. The aim of this study was to assess lung function in children and adolescents after a successful cardiac surgery for atria1 septal defect by using a larger variety of methods. We measured static lung volume, airway resistance, maximum expiratory flow rate, lung recoil pressure and static lung compliance. Materials
and Methods
Lung function was studied in 74 children (22 males, 52 females) after heart surgery for atria1
septal defect (secundum type). All patients were in excellent clinical condition at time of the study; the youngest patient was 9 and the oldest 21 yr old (15.0 k 2.5 yr). Body height varied from 125 to 185 cm with a mean of 163 (SD + 12) cm. Heart surgery was performed at the mean age of 9.9 f 3.0 (range 4.0-14.8) yr, either by direct suture (26 patients) or by pericardial patch (48 patients). Preoperative cardiac catheterization data were available in 26 patients. The mean pulmonary arterial pressure was normal (16.5 ? 4.7 mmHg). Pulmonary vascular resistance was within normal limits (1.3 + 0.7 U/m’ of body surface area). Left-to-right shunt prior to surgery was measured either at heart catheterization or by the radionuclide dilution method in 72 patients. The value of left-to-right shunt ranged between 20-75% of pulmonary blood flow (49 & 12). Mean extracorporeal circulation time was 43 _t 12 min (range 22-721, cross-clamping time was 22 ~fr9 min (range 8-49). The average duration of mechanical ventilatory support postoperatively was 10 f 5 h (range 0.5-21). The time interval from surgery to the lung function testing varied from 1.9-11.3 yr with a mean of 5.1 (SD -t 2.5) yr. Static lung volumes were derived from the measurements of thoracic gas volume in a body plethysmograph (Bodytest, Jaeger) and from lung volumes measured from the expiratory pressurevolume curve (see below). The highest vital and inspiratoty capacities taken as representative values in a subject were used for calculation of other lung volumes. Functional residual capacity was measured at end-expiratory level as thoracic gas volume. Total lung capacity was obtained as a sum of thoracic gas volume plus inspiratory capacity. Residual volume was calculated as total lung capacity minus vital capacity. Airway resistance was measured during quiet breathing simultaneously with thoracic gas volume in a body plethysmograph. It was converted to its reversal value (i.e. airway conductance), and expressed per unit of thoracic gas volume as “specific” airway conductance. Maximum expiratory flow-volume curves were obtained by recording expiratory flow rates versus lung volume changes. Patients performed a complete and rapid
17
by the shutter valve for 0.3 s. At least 5 technically good pressure-volume curves were obtained in each patient. From pressure-volume curves, lung recoil pressure was measured at 100, 90 and 60% of total lung capacity. Static lung compliance as another index of lung elasticity was obtained from the slope of the middle linear part of the pressure-volume curve. Static lung compliance expressed per unit of total lung capacity gave the value of “specific” lung compliance. The results were compared with the reference values on the basis of body height obtained in the same laboratory [21]. flow
expiration to residual volume level after maximal inspiration. At least 5 technically good curves were recorded and from these the “envelope” curve as the representative one for a subject was analyzed. From maximum expiratory flow-volume curves we measured forced vital capacity, peak expiratory flow rate, maximum expiratory flow rates at 25, 50 and 75% of forced vital capacity and at 60% of total lung capacity. We also calculated ratios of maximum expiratory flow rates and total lung capacity in order to correct the absolute values of flow rates in liters/second for lung size. Lung elasticity was assessed from the expiratory pressure-volume curves obtained as a simultaneous recording of transpulmonary pressure (measured as a difference between esophageal and mouth pressures) and lung volume changes. A latex esophageal balloon (wall thickness up to 0.1 mm, length 100 mm) was situated in the lower third of the esophagus. Detailed information was published elsewhere 1211. The pressure-volume curves were recorded at quasi-static conditions during very slow expiration with interrupted air-
TABLE
Data were analysed by using the statistical program STATGRAPHICS, version 5 (1991). The comparison of two samples (Mann-Whitney test) and the two-sample analysis test (t-test) were used. All data are presented as means _t SD. The level of statistical significance was set at P = 0.05. The results of lung function tests were further expressed as a percentage of predicted value.
1
Lung function
test results
Lung function
test
(n = 74, body height
RV/TLC Lung recoil pressure at 100% of TLC at 90% of TLC at 60% of TLC Static lung compliance/TLC expiratory
125-185). Predicted
value t%)
P
mean
SD
mean
*SD
3 63 1 (ml) 4 644 (ml) 2325 (ml) 1050 (ml) 49.3 (%I
856 104s 590 363 5.2
101 100 100 94 100
1.5 14 19 27 11
NS NS NS NS NS
22.3 t%)
6.5
94
26
NS
47.2 (cmH,O) 21.3 (cmH,O) 9.9 (cmH,O) 0.037 (ml~cmH,O~l~ml~‘)
12.5 4.4 2.2 0.010
123 107 114 101
31 20 23 29
< 0.0001 < 0.05 < 0.0001 NS
0.497(l~s~t~l-‘) o.975(l.s-t.l~‘) 0.986(I.s-‘.I-‘) 6.50.~~‘) 0.166 11 .s--’ cmH,O-’
0.166 0.278 0.313 1.9 0.064
110 114 119 99 84
35 29 35 22 32
< 0.01 < 0.0001 < 0.0001 NS < 0.0001
flow rate
25% VC/TLC 50% VC/TLC 60% TLC/TLC Peak expiratory flow rate Specific airway conductance
VC = vital capacity;
163 f 11.9 cm, range
Atria1 septal defect
vc TLC FRC RV FRC/TLC
Maximum
Statistics
TLC = total lung capacity;
I-‘)
FRC = functional
residual
capacity;
RV = residual
volume.
18
Presurgical hemodynamic and perioperative data in the patients were correlated with lung function data by the use of simple and multiple regression analysis.
TABLE 2 Incidence of abnormal lung function tests (n = 74). Lung function test
Results Lung volumes The mean values of vital capacity, total lung capacity, functional residual capacity, residual volume and functional residual capacity to total lung capacity ratio did not differ from the reference values (Table 1).
Static recoil pressure at 100% TLC at 90% TLC at 60% TLC Specific airway conductance TLC vc FRC/TLC RV/TLC Maximum expiratory flow rate at 25% VC/TLC
Airway patency A significant decrease up to 84% (SD _t 32) of the predicted value (P < 0.0001) was found for specific airway conductance (Table 1). Peak expiratory flow rate reached 99.9% of the predicted value. Maximum expiratory flow rates expressed per unit of total lung capacity and measured at 25, 50% of vital capacity and 60% of total lung capacity were even higher than the reference values. Lung elasticity The mean values of lung recoil pressure measured at 100, 90 and 60% of total lung capacity were significantly increased (Table 1). The most significant increase of lung recoil was observed at the level of 100% of total lung capacity (123% of predicted value). Lung recoil pressure at 60% of total lung capacity reached 114% of the predicted value. Lung recoil pressure at 90% of total lung capacity was 107% of the predicted value (P < 0.05). The value of specific static lung compliance was normal. Frequency of abnormal lung function tests Abnormal lung function tests (i.e. deviating by more than k2 SD from the mean normal value) were found in 35 (47.3%) of 74 patients (Table 2). Lung recoil pressure was increased in 24 patients
Abnormal value (change)
Patients No.
%
decrease decrease decrease increase increase
24 14 9 13 9 7 3 4
32.4 18.9 12.2 17.6 12.2 9.5 4.1 5.4
decrease
4
5.4
35
47.3
increase
Total Abbreviations as Table 1.
(32.4%) and decreased in 2 patients, respectively. Maximum expiratory flow rates were reduced in 4 (5.4%) patients. Specific airway conductance was reduced in 13 (17.6%) patients. Vital capacity and total lung capacity were significantly decreased in 7 (9.5%) and 9 (12.2%) patients, respectively. The functional residual to total lung capacities and residual volume to total lung capacity ratios were increased significantly in 3 (4.1%) and 4 (5.4%) patients, respectively. Effect of preoperative pulmonary hemodynamics and perioperative treatment on lung function According to the preoperative hemodynamic data, the patients were arbitrarily divided into two groups, i.e. with a moderate increase (leftto-right shunt < 50% of pulmonary blood flow) and severe increase (left-to-right shunt > 50% of pulmonary blood flow) in pulmonary blood flow. More frequently (i.e. in 50% of patients) the abnormalities of lung function were found in a group with a severe increase in pulmonary blood flow. The incidence of lung function abnormalities in a group with a moderate increase in pulmonary blood flow was lower (i.e. in 44% of patients). The differences in the latter frequencies were not statistically significant.
19
There was a short duration of mechanical ventilation in most patients after surgery for atria1 septal defect. In only 13 patients, a ventilatory support lasted more than 15 h. The incidence of lung function disturbances did not differ from that observed in our whole group of patients, i.e. abnormal values of lung function tests were revealed in 6 (46%). A positive linear correlation between the ratio of functional residual capacity to total lung capacity and the time period of postoperative ventilatory support (Y = 0.415, P < 0.00, as well as a negative linear correlation between specific airway conductance and the time period of ventilatory support (r = -0.396, P < 0.041, were revealed in 42 patients with the preoperative severe increase of pulmonary blood flow. In the same patients positive linear correlations between age at surgery and static lung volumes (vital and total lung capacity) (1. = 0.424, P < 0.01 and r = 0.310, P < 0.051, were found. Negative linear correlations between the time period of mechanical ventilatory support and vital capacity (r = - 0.599, P < O.OOl>,as well as total lung capacity (r = - 0.430, P < 0.031, were observed in 32 patients with a moderate increase in pulmonary blood flow. A positive linear correlation between age at surgery and total lung capacity (Y = 0.377, P < 0.05) in the same patients was also found. Any other correlation between age at surgery, time period of surgery-to-testing and lung function parameters was not found. Discussion In almost one half of our patients lung function disturbances were revealed, despite effective surgical treatment and excellent clinical conditions at the time of lung function testing. Increased lung stiffness and obstruction of central airways were the most frequent findings. Reduced dynamic lung compliance considered as an indicator of stiff lung was found after surgery for atria1 septal defect also by Haughton [16], but the measurement was performed in the early postoperative period (up to 35 postoperative days). On the other hand, in 4 of 7 adult patients with atria1
septal defect after surgery reported by Davies and Gazetopoulos [14] there was a rise in dynamic compliance. Elastic lung recoil pressure measured at three different levels of total lung capacity is a more sensitive parameter in detecting of lung elasticity abnormalities than specific static lung compliance as was published in detail elsewhere [21]. The most pronounced deviation from the predicted value was revealed in lung recoil pressure measured at 100% of total lung capacity. Lung recoil pressure at lower levels of total lung capacity was less abnormal. Static lung compliance was even normal. Lung stiffness assessed by lung recoil pressure measurement in our patients was less pronounced than that observed in the patients with simple transposition of the great arteries [22] or with ventricular septal defect (unpublished paper). The increased lung recoil pressure indicating increased lung stiffness has been observed as the most typical finding in patients with idiopathic pulmonary fibrosis [21] having characteristic histological features. However, lung biopsy was not carried out in our patients with atria1 septal defect. Therefore, it is rather difficult to draw any conclusion on anatomical abnormalities of the lung parenchyma causing the observed increase of lung recoil pressure. We might hypothesize, that the growth of the elastic and collagen tissue can be changed in a developing lung exposed to an increased pulmonary blood flow since birth [2,23]. The increase in pulmonary blood flow, accompanied by an increased blood volume [24] and engorgement of the capillary network, might also contribute to the abnormalities in the elastic properties of the lung [6,25]. There is no reason to explain the increased lung stiffness by the surgical procedure itself. The hear: and thorax were always exposed by central sternotomy, thus avoiding any damage of the lungs. A reduced maximal expiratory flow rate at 25% of vital capacity found in only 5% of our patients, implied a normal patency of peripheral airways in the majority of patients after surgery for atria1 septal defect. It might be due to the normalizing of pulmonary blood flow and volume. Another relevant observation was a decreased airway conductance indicating an obstruction of
20
the larger airways in 18% of our patients. A tracheal intubation (especially followed by possible infection) may be a cause of airway obstruction [26]. Although only a short period of mechanical ventilation (OS-21 h) in our group was ascertained, we assume that it might be harmful, resulting in specific conductance reduction but clinically silent. Hyperinflation, indicated by increased ratios of functional residual to total lung capacities, and of residual volume to total lung capacity and observed in 5% of our patients, was similar in adults with uncorrected atria1 septal defect [2,5,6]. The abnormal pulmonary hemodynamics characterized by high pulmonary blood flow preoperatively and the postoperative mechanical ventilation might also contribute on these abnormalities. This assumption is supported by the positive linear correlation between functional residual to total lung capacities ratio and duration of mechanical ventilation (r = 0.415, P < 0.01). Other parameters of lung function were normal in the majority of patients. This is in accordance with their excellent clinical condition. The disturbance of lung function in about half of our patients after a successfully corrected atria1 septal defect, led to some doubts about the generally accepted opinion that this cardiac malformation is one of a few perfectly correctable congenital heart diseases.
Acknowledgments We thank Marie Spirova and Kvi?ta Kozerova for technical assistance during the study.
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