Eur J Cardio-thorac
Surg (1991) 5: 479-485
(0 Springer-&&g 1991
Surgical treatment of airway obstruction associated with congenital heart disease in infants and small children M. Yamaguchi,
H. Ohashi, Y. Hosokawa,
Departments of Cardiothoracic and Clinics, Kobe, Japan
Y. Oshima, C. Tsugawa, and K. Kimura
Surgery and Surgery, Kobe Children’s Hospital and Department
of Surgery, University
of Iowa Hospitals
Abstract. In the last 12 years, 21 patients age 1 month to 5 years (median, 7 months) underwent surgical treatment for severe airway obstruction associated with congenital heart disease. Plico-suspension of the pulmonary artery was carried out in 14 patients with documented severe left bronchial compression by a distended pulmonary artery together with repair of ventricular septal defects (11 patients), repair of large coronary artery fistula (l), division of ductus (1) and pulmonary artery banding (l), with subsequent significant relief of compression. Aortopexy was used in 2 patients with documented severe tracheal compression by a right aortic arch. Five patients had congenital tracheal stenoses (3 extensive, 2 localized). Two of 3 patients with associated complex intracardiac anomalies underwent concomitant repair of both lesions with the use of cardiopulmonary bypass and 1 had a tracheoplasty and pulmonary artery banding. Tracheal reconstruction with a cartilaginous graft together with repair of pulmonary artery sling was carried out in 2 infants. Nineteen patients are alive and well, at a mean follow-up of 87 months. In conclusion, we advocate early aggressive surgical intervention to both lesions to obtain a better result in the management of infants and small children with this difficult and often fatal combination. [Eur J Cardio-thorac Surg (1991) 5:479-4851 Key words: Airway obstruction
- Congenital heart disease - Plico-suspension
of pulmonary
artery - Aortopexy
-
Tracheal reconstruction
Airway obstruction in infants with congenital heart disease may complicate the natural and surgical history of the patients and significantly increases mortality and morbidity [2, 3, 5, 6, 9, 11, 13, 15, 16, 19-22, 241. The diagnosis and treatment of tracheobronchial obstructive lesions associated with congenital heart disease in infancy presents particular problems and remains a therapeutic challenge [6, 181. This paper reviews our 1Zyear surgical experience. Patients with a vascular ring without associated cardiac anomalies were excluded from this study as their treatment is standardized. Patients and methods From February 1978 to January 1990, 21 patients age 1 month to 5 years (17 patients were less than 12 months of age; median age, 7 months) had operative interventions to the airway. The clinical data are summarized in Table 1. Fourteen patients had documented severe left bronchial compression (defined as a stenosis of more than 90% of the bronchial Presented at the Poster Session of the 4th Annual Meeting of the European Association for Cardio-thoracic Surgery, Naples, September 17-19, 1990
lumen) by distended pulmonary arteries. As associated cardiac anomalies, 11 patients had large ventricular septal defects with severe pulmonary hypertension, 1 had a huge left coronary artery to right ventricular tistula, ventricular septal defect and patent ductus arteriosus. The onset of severe respiratory distress in these 14 patients ranged from age 22 days to 8 months, mean 4.1 months, and preoperatively, 12 required respirator care with endotracheal intubation for the period from 8 days to 2 years and 7 months. A 13-month-old boy (2580 g), born during the 31st week of gestation and weighing 760 g at birth, had been on respiratory for a total period of IO months on 3 occasions with bronchopulmonary dysplasia associated with a ventricular septal defect and moderate pulmonary hypertension. Another boy who underwent primary repair of a type-C esophageal atresia at 2 days of age and lower lobe lobectomy for severe lobar emphysema at 4 months of age, had been on a respirator for a period of 2 years and 7 months with respiratory distress. Cardiac catheterization, performed at 3 years of age, revealed the presence of a patent ductus arteriosus, moderate pulmonary hypertension and a dilated pulmonary artery. The diagnosis of bronchial compression by a distended pulmonary artery was established by the bronchoscopic findings of flattening of the carina and stenosis of the bronchial lumen (mainly left) due to extrinsic compression by a pulsating mass from left superior aspect. The pediatric ventilation bronchoscope’ was used for this purpose. The degree of bronchial compression was defined
1 Karl Storz Endoscopy,
USA
480 Table 1. Airway obstruction Type of airway obstruction (Number of cases) Bronchial compression by dilated pulmonary artery (14)
Tracheal compression by right aortic arch (2)
Congenital stenosis (5)
tracheal
associated
with congenital
Diagnosis
VSD, pulmonary hypertension
11 cases
heart disease: clinical summary Age at operation (median)
Operative procedure for airway obstruction
Concomitant/ (preceding) procedure
Outcome
3 -20 months (7 months)
Plico-suspension of the pulmonary artery
VSD closure
All but one alive, well
Pulmonary banding
artery
Alive, well
VSD, BPD
1 case
13 months
TEF, PDA
1 case
3 years
PDA division
Alive, well
LCA-RV tistula, pulmonary hypertension
1 case
9 months
Closure of LCA-RV fistula
Alive, well
TEF, vascular ring
1 month
Aortopexy
(Division of vascular ring)
Alive, well
TEF, aortopulmonary window
9 months
Aortopexy
(Division of aortopulmonary window)
Alive, well
Tetralogy of Fallot, severe localized tracheal stenosis
5 years
Tracheal resection and end-to-end anastomosis
Total correction of tetralogy of Fallot
Alive, well
Scimitar syndrome, ASD. pulmonary sling, extensive tracheal stenosis
5 months
Tracheal plasty with a cartilaginous graft
Repair of scimitar syndrome, ASD, pulmonary sling
Alive, well
Complete form of CAVC, subglottic stenosis
3 months
As above
Pulmonary banding
artery
Alive, well
Pulmonary sling, extensive trachea1 stenosis
6 months 8 months
As above As above + Aortopexy
Pulmonary repair
sling
Alive, well Died at home 1 yr postop.
VSD = ventricular septal defect; PDA = patent ductus arteriosus; BPD = bronchopulmonary dysplasia; TEF = tracheoesophageal LCA = left coronary artery; RV = right ventricle; ASD = atria1 septal defect: CAVC = common atrioventricular canal
Fig. 1 A-D. Diagrammatic portrayal of plico-suspension of the pulmonary artery. A Site of compression in patient with hypertensive, distended pulmonary artery is indicated by a stippled area. B and C the main and left pulmonary arteries are plicated to normal size with a horizontal mattress and running over and over sutures. D the plicated portion of the pulmonary artery is then suspended left anterosuperiorly to the chest wall with 4 suspension sutures as mild, moderate or severe, depending on the severity of stenosis; mild: stenosis occupying less than 50% of the bronchial lumen, moderate: 50-90% stenosis, severe: more than 90% stenosis to complete occlusion at zero airway pressure (Fig. 2 A). In this series, only a patient with severe bronchial compression was considered as a candidate for surgical intervention.
fistula;
Severe tracheal compression by the right aortic arch was documented in 2 patients. One infant underwent primary repair of the type-C esophageal atresia at 3 days of age and division of a large left ductus at 21 days of age for a vascular ring with persistent dorsal aortic arch, aberrant left subclavian artery, left ductus and right aortic arch (Type 3-B of Stewart and Edwards’s classification). Because of persistent dyspnea and retraction after feeding, the infant underwent bronchoscopy which demonstrated tracheal obstruction caused by a left posterior deviation of the trachea, protrusion of the right anterior tracheal wall into the lumen, with nearly complete occlusion during expiration resulting from compression by the right aortic arch (Fig. 3A). Another infant also underwent primary repair of the type-C esophageal atresia at 1 day of age and closure of an aortopulmonary window at 11 days of age. Because of persistent, recurrent respiratory insufficiency, the infant underwent tracheostomy at 2 months of age and repeated bronchoscopic examinations confirmed the diagnosis of severe tracheal compression by the right aortic arch. Five patients had trachea1 stenoses of congenital origin (3 with extensive and 1 with localized stenoses due to complete cartilaginous rings and 1 with subglottic stenosis). Three had associated complex intracardiac anomalies and 2 others had pulmonary artery slings (Table 1). All infants had symptoms of severe respiratory distress since the early months of life. The diagnosis of tracheal stenosis was established by bronchoscopy combined with plain tomography, computed axial tomographic scan of the chest, and bronchography if necessary (Figs. 4,5). Data for the first 2 patients with associated complex intracardiac anomalies and 1 patient with pulmonary artery sling in this group have been previously reported [26, 271.
481
Fig. 2 A, B. Bronchoscopic views of carina and bilateral bronchi before (A) and after (B) the plico-suspension of pulmonary artery in a 7-month-old infant with ventricular septal defect and severe pulmonary hypertension. A flattening of the carina and severe stenosis of the left bronchus is obvious. B note the opened carina and the left bronchus with patent lumen
Fig. 3 A, B. Bronchoscopic views of trachea before (A) and after (B) the aortopexy in a l-month-old infant. A left posterior deviation of the trachea with protrusion of the right anterior tracheal wall into the lumen is indicated by urrows. B the lumen of the trachea is widely patent with disappearance of protrusion from right anterior aspect
Results of surgical intervention
(1) Severe bronchial compression by the distended pulmonary artery: Plico-suspension of the pulmonary artery [28] has been employed in all patients with this entity in conjunction with patch closure of the ventricular septal defects (11 patients), pulmonary artery banding (l), division of the ductus (1) and closure of the left coronary artery-to-right ventricular fistula (1). The distended main and left pulmonary arteries were plicated to normal size with horizontal mattress and additional running overand-over sutures. The plicated portion of the pulmonary artery was then suspended left-anterosuperiorly to the chest wall with 4 suspension sutures (Fig. l A-D) [28]. The effectiveness of this procedure for relief of bronchial compression was confirmed by intraoperative bronchoscopy before and after the procedure (Figs. 2A, B).
Fig. 4. Tomogram of the chest demonstrating extensive tracheal stenosis in an infant with scimitar syndrome and pulmonary artery. sling. Arrow indicate the area of tracheal stenosis
482
Fig. SA, B. Computed axial tomogrztphic scan of the chest in the same patient as Fig. 4. Arrow indicates trachea just aabove (A) and in the middle of the stenotic area
(B)
Table 2. Results
of repair of ventricular septal defect associated with severe bronchial compression in infants Plico-suspension
of the pulmonary
artery
No
Yes Number of patients
10 (1 early death)
Age at operation
6.1 (range 3-9) months kg
5.0 (range 3-8) months
Body weight
4.4 (2.7-5.7)
Preoperative intubation
8110
316
Duration of postoperative intubation
14.7 (7-30) days
84.4 (20 - 194) days
5.4 (4.5-6.9)
kg
All but one, who died of sepsis on the 16th postoperative day, have survived the procedure with successful early extubation and are well at a mean follow-up of 99 months (18 to 150 months). To evaluate the effect of plico-suspension of the pulmonary artery on the postoperative course of the patients, various pre- and postoperative ciinical parameters of 10 infants who had this procedure concomitantly with repair of the ventricular septal defect in the current series
were compared to those of 6 infants with documented severe left bronchial compression associated with ventricular septal defect and severe pulmonary hypertension, and who only had repair of the ventricular septal defect in the 4-year period preceding February 1978 (Table 2). The mortality was lower and the period of postoperative respiratory care with endotracheal intubation was significantly shorter in the former than in the latter group of infants. (2) Tracheal compression by the right aortic arch: In both infants, surgical suspension of the ascending aorta to the right side of the sternum (aortopexy) [8] was carried out under bronchoscopic control with excellent subsequent relief of airway obstruction (Figs. 3 A, B). Both patients are well 9 years and 10 years, respectively, after operation. (3) Congenital tracheal stenosis: Two of 3 patients with associated complex intracardiac anomalies underwent concomitant repair of both lesions with the use of cardiopulmonary bypass [26]. In the first child (Syear-old), resection of the stenotic segment of the trachea (15 mm) and reconstruction by end-to-end anastomosis was accomplished on bypass following intracardiac repair of the tetralogy of Fallot. In the second patient, (Smonth-old), total reconstruction of an extensive tracheal stenosis using a large cartilaginous graft was carried out, also on bypass, following repair of cardiac defects by rerouting
483
Fig. 6. Diagrammatic portrayal of repair of pulmonary artery sling and tracheoplasty for extensive tracheal stenosis with a cartilaginous graft (stippled area)
the pulmonary venous blood from the right lung to the left atrium by covering the opening of a scimitar vein into the inferior vena cava and the atria1 septal defect with a generous patch and repair of the pulmonary artery sling by division of the anomalous artery and end-to-side reimplantation into the main pulmonary artery (Fig. 6). In the third patient, (3-month-old) with a complete form of common atrioventricular canal defect, the localized subglottic stenosis was enlarged by a cartilaginous graft together with pulmonary artery banding. The patient subsequently underwent successful definitive repair of the common atrioventricular canal defect. The postoperative course was uneventful in all 3 patients and they are doing well 45, 38 and 51 months, respectively, after operation. Two infants had a combination of pulmonary artery sling and extensive tracheal stenosis due to complete cartilaginous rings (ring/sling complex). Tracheal reconstruction with a cartilaginous graft and repair of the pulmonary artery sling with division and reimplantation of the left pulmonary artery into the main pulmonary artery was carried out in both patients with excellent subsequent relief of symptoms [27]. Tracheal reconstruction was effected with the use of extracorporeal membrane oxygenator in 1 patient. One patient had a recurrence of respiratory distress due to tracheomalacia and subsequently underwent aortopexy as a second operation 4 months later. The postoperative course was uneventful but he died suddenly at home 1 year after the initial operation of lower respiratory infection. The other patient is doing well 8 months after operation. Discussion
Airway obstruction in infants with congenital heart disease may complicate the natural and surgical history of the patients and significantly increases mortality and morbidity following surgical intervention to the cardiac lesions [2, 3, 5, 69, 11, 13, 15, 16, 19-22, 241. Early and
accurate preoperative diagnosis of the airway lesion is mandatory to plan the appropriate treatment to avoid complications. In general, infants’ airways are more susceptible to extrinsic compression as the cartilaginous, muscular and elastic supports of airway are weak and the bronchial lumen is small [9, 10, 15, 241. Resistance to air flow through the bronchial lumen is inversely proportional to the fourth power of radius. Therefore, relatively slight degrees of compression or intraluminal narrowing of the small bronchi of young infants will result in bronchial obstruction than in older children whose airways are larger. The airway of young infants contains relatively more mucous glands than that of adults, and there are age differences in chemical composition of the mucus [lo]. Furthermore, the pores of Kohn and canals of Lambert, which normally allow collateral ventilation in the event of bronchial obstruction, are poorly developed in infants [lo, 151.As a consequence, small amounts of edema, mucus or inflammatory debris may markedly narrow or completely occlude a infant’s bronchus or bronchiole resulting in air trapping or atelectasis. Severe airway compression occurring in infants with congenital heart disease as a result of altered hemodynamics or anomalous relationship between the tracheobronchial tree and vascular structures are well documented in patients with vascular ring, tetralogy of Fallot with absent pulmonary valve, or with various congenital heart diseases with increased pulmonary blood flow and pulmonary hypertension as seen in our patients [2,3,5,6, 9, 11, 13, 15, 16, 19-22, 241. The presence of severe bronchial compression is suspected by the onset of recurrent severe respiratory distress characterized by stridor and wheezing in the early months of life, findings of persistent atelectasis or occasionally of air trapping in the left lung and hyperinflation of the right lung with shift of the heart and mediastinum to the left on a chest X-ray, blurring of the bronchial tree in the affected area on the frontal view and narrowing in the lateral view of high voltage chest roentgenograms. Bronchographic or bronchoscopic examination is mandatory for accurate diagnosis. We consider bronchoscopy using a pediatric ventilation bronchoscope the safest, most helpful and definitive diagnostic tool in critical infants with airway obstruction associated with congenital heart disease. The place for tracheobronchography which requires extreme care during the procedure to avoid aggravating the condition of the compromized airway in these high-risk infants, is very limited in our experience. In all infants with potential airway compression or stenosis, we suggest that preoperative bronchoscopy be considered as one of the routine evaluations, and when the nature of obstruction becomes evident, the operation must be planned to avoid postoperative complications. In the case of severe left bronchial compression by a distended pulmonary artery, we successfully relieved the bronchial compression by plico-suspension of the pulmonary artery concomitantly with a corrective or palliative operation for the congenital cardiac defects [28]. Although we have not experienced a case, a recent report [6] emphasized the effectiveness of left pulmonary artery
484
transection and prolongation with a prosthetic conduit for this type of lesion, but this technique has a disadvantage, so that it would eventually require replacement of the conduit as the patient grows. It is well known that in infants with severe prolonged airway compression, the deformity and pliabilaity of the tracheobronchial wall may persist for a considerable period of time even after the removal of causative factors by operation until the airway recovers stiffness to maintain patency [3,28]. This fact accounts for the increased postoperative mortality and morbidity due to respiratory distress after operation for a cardiac anomaly, if an effective measure to relieve airway obstruction has not been undertaken simultaneously. The result of this current study underscores the effectiveness of concomitant plico-suspension of the pulmonary artery for decreasing the mortality and shortening the period of postoperative respiratory care in infants with severe bronchial compression associated with congenital heart disease. In 2 cases with tracheal compression by the right aortic arch, both in infants with previous primary repair of a congenital tracheoesophageal fistula and correction of associated cardiovascular anomalies, and in 1 case with tracheomalacia following complete reconstruction of extensive tracheal stenosis and pulmonary artery sling, we attempted aortopexy as reported by Filler et al. [8]. Satisfactory relief of the tracheal compression was obtained in all cases as reported by others [4, 8, 231. A combination of severe congenital tracheal stenosis and congenital heart disease still remains a therapeutic challenge [6, 181.It was only recently that successful reconstructive surgery for stenosis of the intrathoracic trachea in infants and small children has been reported [I, 7, 12, 14, 17, 18, 251. In infants and small children with a combination of stenosis of the intrathoracic trachea and complex congenital heart disease, the situation becomes more complicated. Surgical intervention for this combination in a staged fashion had been accompanied by a poor prognosis because the presence of the other untreated lesion usually poses problems in postoperative management [6, 181. We attempted simultaneous repair of tracheal stenoses at the time of surgery for congenital cardiac lesions in 5 patients: at the time of repair of complex cardiac anomalies with the aid of cardiopulmonary bypass in 2 patients [26], at the time of repair of pulmonary artery sling in 2 patients [27] (in 1 with the aid of extracorporeal membrane oxygenation), and at the time of pulmonary artery banding for a complete form of atrioventricular canal defect. The promising results we have obtained suggest that obstructive lesions of the trachea are amenable to appropriate reconstruction at the time of surgery for cardiac lesions with the aid of cardiopulmonary bypass, if necessary. In conclusion, we advocate the following to minimize the potentially deleterious effects of airway obstruction associated with congenital heart disease: (1) early preoperative identification of infants with potential airway obstruction and accurate definitive diagnosis with the use of the pediatric ventilation bronchoscope, (2) selection of appropriate surgical procedures specific to the type and cause of airway obstruction, and (3) early aggressive con-
comitant repair of both lesions, with the aid of cardiopulmonary bypass if necessary, to obtain a better outcome in the surgical management of infants and small children with this difficult and often fatal combination.
References 1. Akl BF, Yabek SM, Berman W Jr (1984) Total tracheal reconstruction in a three-month-old infant. J Thorac Cardiovasc Surg 87: 543-546 2. Backer C, Ilbawi MN, Idriss FS, De Leon SY (1989) Vascular anomalies causing tracheoesophageal compression: review of experience in children. J Thorac Cardiovasc Surg 97: 725-731 3. Bradham RR, Sealy WC, Young WG (1968) Respiratory distress associated with anomalies of the aortic arch. Surg Gynecol Obstet 126:9-14 4. Campbell DN, Lilly JR, Heiser JC, Clarke DR (1983) The surgery of pulmonary artery “sling”. J Pediatr Surg 18:855856 5. Cohen SR, Landing BH (1976) Tracheostenosis and bronchial abnormalities associated with pulmonary artery sling. Ann Otol 85:482-590 6. Corno A, Giamberti A, Giannico S, Marino B, Rossi E, Marcelletti C, Kirklin JK (1990) Airway obstruction associated with congenital heart disease in infancy. J Thorac Cardiovasc Surg 99: 1091-1098 I. Ein SH, Friedberg J, Williams WG, Rearon B, Baker GA, Mancer K (1982) Tracheoplasty -a new operation for complete congenital tracheal stenosis. J Pediatr Surg 17: 872-878 8. Filler RM, Rosselo PJ, Lebowitz RL (1976) Life-threatening anoxic spells caused by tracheal compression after repair of esophageal atresia: correction by surgery. J Pediatr Surg 11:739-748 9. Fischer DR, Neches WH, Beerman LB, Fricker FJ, Siewers RD, Lenox CC, Park SG (1984) Tetralogy of Fallot with absent pulmonic valve: analysis of 17 patients. Am J Cardio153: 14331437 10. Griscom NT, Wohl MEB, Kirkpatrick JA (1978) Lower respiratory infections: how infants differ from adults. Radio1 Clin North Am 16: 367-387 11. Habbema L, Losekoot TG, Becker AE (1980) Respiratory distress due to the bronchial compression in persistent truncus arteriosus. Chest 77:230-232 12. Idriss FS, DeLeon SY, Ilbawi MN, Gerson CR, Tucker GF, Hollinger L (1984) Tracheoplasty with pericardial patch for extensive tracheal stenosis in infants and children. J Thorac Cardiovasc Surg 88: 527-536 13. Jones JC, Almond CH, Snyder HM, Meyer SW, Patrick JR (1965) Lobar emphysema and congenital heart disease in infancy. J Thorac Cardiovasc Surg 49: I-IO 14. Kimura K, Mukohara N, Tsugawa C, Matsumoto Y, Sugimura C, Murata H, Itoh H (1982) Tracheoplasty for congenital stenosis of the entire trachea. J Pediatr Surg 17: 869-871 15. Lakier JB, Stanger P, Heymann MA, Hoffman JIE, Rudolph AM (1974) Tetralogy of Fallot with absent pulmonary valve: natural history and hemodynamic considerations. Circulation 50: 167-175 16. Leape LL, Ching N, Holder TM (1970) Lobar emphysema and patent ductus arteriosus. Pediatrics 46: 97- 101 17. Mattingly WT Jr, Belin RP, Todd EP (1981) Surgical repair of congenital trachea1 stenosis in an infant. J Thorac Cardiovasc Surg 81:738-740 18. Nakayama DK, Harrison M, de Lorimier AA, Brasch RC, Fishman NH (1982) Reconstructive surgery for obstructive lesions of the intrathoracic trachea in infants and small children. J Pediatr Surg 17: 854-868 19. Nikaidoh H, Riker WL, Idriss FS (1972) Surgical management of “vascular rings.” Arch Surg 105: 327-333
485 20. Pontius RG (1963) Bronchial obstruction of congenital origin. Am J Surg 106:8-14 21. Rivkin LM, Read RC, Lillehei CW. Varco RL (1957) Massive atelectasis of the lung in children with congenital heart disease. J Thorac Cardiovasc Surg 34: 116-125 22. Sade RM, Rosenthal A, Fellows K, Castaneda AR (1975) Pulmonary artery sling. J Thorac Cardiovasc Surg 69: 333-346 23. Schwartz MZ, Filler RM (1980) Tracheal compression as a cause of apnea following repair of tracheoesophageal tistula: treatment by aortopexy. J Pediatr Surg 15: 842-848 24. Stanger P, Lucas RV, Edwards JE (1969) Anatomic factors causing respiratory distress in acyanotic congenital cardiac disease, special reference to bronchial obstruction. Pediatrics 43: 760-769 25. Weber TR, Eigen H, Scott PH, Krishna G, Grosfeld JL (1982) Resection of congenital tracheal stenosis involving the carina. J Thorac Cardiovasc Surg 84: 200-203 26. Yamaguchi M, Oshima Y, Hosokawa Y, Ohashi H, Tsugawa C, Nishijima E, Tsubota N (1990) Concomitant repair of congenital tracheal stenosis and complex cardiac anomaly in small children. J Thorac Cardiovasc Surg 100: 181- 187
27. Yamaguchi M, Oshima Y, Ienaga T, Tsugawa C, Kimura K, Matsumoto Y (1986) Successful repair of pulmonary sling associated with congenital tracheal stenosis in an 8-month-old infant. J Jpn Assoc Thorac Cardiovasc Surg 38: 85-89 (in Japanese) 28. Yamaguchi M, Nishiyama N, Hosokawa Y, Tachibana H, Horikoshi K, Toriyama A, Mito H, Tei G, Ohashi H, Ogawa K (1981) Plication and suspension of the pulmonary artery for severe left bronchial compression in infant with ventricular septal defect. J Jpn Assoc Thorac Cardiovasc Surg 29: 86-98 (in Japanese)
Masahiro Yamaguchi, MD Department of Cardiothoracic Kobe Children’s Hospital Takakuradai l-l-l, Suma-ku Kobe 654 Japan
Surgery
Surg (1991) 5: 479-485
(0 Springer-&&g 1991
Surgical treatment of airway obstruction associated with congenital heart disease in infants and small children M. Yamaguchi,
H. Ohashi, Y. Hosokawa,
Departments of Cardiothoracic and Clinics, Kobe, Japan
Y. Oshima, C. Tsugawa, and K. Kimura
Surgery and Surgery, Kobe Children’s Hospital and Department
of Surgery, University
of Iowa Hospitals
Abstract. In the last 12 years, 21 patients age 1 month to 5 years (median, 7 months) underwent surgical treatment for severe airway obstruction associated with congenital heart disease. Plico-suspension of the pulmonary artery was carried out in 14 patients with documented severe left bronchial compression by a distended pulmonary artery together with repair of ventricular septal defects (11 patients), repair of large coronary artery fistula (l), division of ductus (1) and pulmonary artery banding (l), with subsequent significant relief of compression. Aortopexy was used in 2 patients with documented severe tracheal compression by a right aortic arch. Five patients had congenital tracheal stenoses (3 extensive, 2 localized). Two of 3 patients with associated complex intracardiac anomalies underwent concomitant repair of both lesions with the use of cardiopulmonary bypass and 1 had a tracheoplasty and pulmonary artery banding. Tracheal reconstruction with a cartilaginous graft together with repair of pulmonary artery sling was carried out in 2 infants. Nineteen patients are alive and well, at a mean follow-up of 87 months. In conclusion, we advocate early aggressive surgical intervention to both lesions to obtain a better result in the management of infants and small children with this difficult and often fatal combination. [Eur J Cardio-thorac Surg (1991) 5:479-4851 Key words: Airway obstruction
- Congenital heart disease - Plico-suspension
of pulmonary
artery - Aortopexy
-
Tracheal reconstruction
Airway obstruction in infants with congenital heart disease may complicate the natural and surgical history of the patients and significantly increases mortality and morbidity [2, 3, 5, 6, 9, 11, 13, 15, 16, 19-22, 241. The diagnosis and treatment of tracheobronchial obstructive lesions associated with congenital heart disease in infancy presents particular problems and remains a therapeutic challenge [6, 181. This paper reviews our 1Zyear surgical experience. Patients with a vascular ring without associated cardiac anomalies were excluded from this study as their treatment is standardized. Patients and methods From February 1978 to January 1990, 21 patients age 1 month to 5 years (17 patients were less than 12 months of age; median age, 7 months) had operative interventions to the airway. The clinical data are summarized in Table 1. Fourteen patients had documented severe left bronchial compression (defined as a stenosis of more than 90% of the bronchial Presented at the Poster Session of the 4th Annual Meeting of the European Association for Cardio-thoracic Surgery, Naples, September 17-19, 1990
lumen) by distended pulmonary arteries. As associated cardiac anomalies, 11 patients had large ventricular septal defects with severe pulmonary hypertension, 1 had a huge left coronary artery to right ventricular tistula, ventricular septal defect and patent ductus arteriosus. The onset of severe respiratory distress in these 14 patients ranged from age 22 days to 8 months, mean 4.1 months, and preoperatively, 12 required respirator care with endotracheal intubation for the period from 8 days to 2 years and 7 months. A 13-month-old boy (2580 g), born during the 31st week of gestation and weighing 760 g at birth, had been on respiratory for a total period of IO months on 3 occasions with bronchopulmonary dysplasia associated with a ventricular septal defect and moderate pulmonary hypertension. Another boy who underwent primary repair of a type-C esophageal atresia at 2 days of age and lower lobe lobectomy for severe lobar emphysema at 4 months of age, had been on a respirator for a period of 2 years and 7 months with respiratory distress. Cardiac catheterization, performed at 3 years of age, revealed the presence of a patent ductus arteriosus, moderate pulmonary hypertension and a dilated pulmonary artery. The diagnosis of bronchial compression by a distended pulmonary artery was established by the bronchoscopic findings of flattening of the carina and stenosis of the bronchial lumen (mainly left) due to extrinsic compression by a pulsating mass from left superior aspect. The pediatric ventilation bronchoscope’ was used for this purpose. The degree of bronchial compression was defined
1 Karl Storz Endoscopy,
USA
480 Table 1. Airway obstruction Type of airway obstruction (Number of cases) Bronchial compression by dilated pulmonary artery (14)
Tracheal compression by right aortic arch (2)
Congenital stenosis (5)
tracheal
associated
with congenital
Diagnosis
VSD, pulmonary hypertension
11 cases
heart disease: clinical summary Age at operation (median)
Operative procedure for airway obstruction
Concomitant/ (preceding) procedure
Outcome
3 -20 months (7 months)
Plico-suspension of the pulmonary artery
VSD closure
All but one alive, well
Pulmonary banding
artery
Alive, well
VSD, BPD
1 case
13 months
TEF, PDA
1 case
3 years
PDA division
Alive, well
LCA-RV tistula, pulmonary hypertension
1 case
9 months
Closure of LCA-RV fistula
Alive, well
TEF, vascular ring
1 month
Aortopexy
(Division of vascular ring)
Alive, well
TEF, aortopulmonary window
9 months
Aortopexy
(Division of aortopulmonary window)
Alive, well
Tetralogy of Fallot, severe localized tracheal stenosis
5 years
Tracheal resection and end-to-end anastomosis
Total correction of tetralogy of Fallot
Alive, well
Scimitar syndrome, ASD. pulmonary sling, extensive tracheal stenosis
5 months
Tracheal plasty with a cartilaginous graft
Repair of scimitar syndrome, ASD, pulmonary sling
Alive, well
Complete form of CAVC, subglottic stenosis
3 months
As above
Pulmonary banding
artery
Alive, well
Pulmonary sling, extensive trachea1 stenosis
6 months 8 months
As above As above + Aortopexy
Pulmonary repair
sling
Alive, well Died at home 1 yr postop.
VSD = ventricular septal defect; PDA = patent ductus arteriosus; BPD = bronchopulmonary dysplasia; TEF = tracheoesophageal LCA = left coronary artery; RV = right ventricle; ASD = atria1 septal defect: CAVC = common atrioventricular canal
Fig. 1 A-D. Diagrammatic portrayal of plico-suspension of the pulmonary artery. A Site of compression in patient with hypertensive, distended pulmonary artery is indicated by a stippled area. B and C the main and left pulmonary arteries are plicated to normal size with a horizontal mattress and running over and over sutures. D the plicated portion of the pulmonary artery is then suspended left anterosuperiorly to the chest wall with 4 suspension sutures as mild, moderate or severe, depending on the severity of stenosis; mild: stenosis occupying less than 50% of the bronchial lumen, moderate: 50-90% stenosis, severe: more than 90% stenosis to complete occlusion at zero airway pressure (Fig. 2 A). In this series, only a patient with severe bronchial compression was considered as a candidate for surgical intervention.
fistula;
Severe tracheal compression by the right aortic arch was documented in 2 patients. One infant underwent primary repair of the type-C esophageal atresia at 3 days of age and division of a large left ductus at 21 days of age for a vascular ring with persistent dorsal aortic arch, aberrant left subclavian artery, left ductus and right aortic arch (Type 3-B of Stewart and Edwards’s classification). Because of persistent dyspnea and retraction after feeding, the infant underwent bronchoscopy which demonstrated tracheal obstruction caused by a left posterior deviation of the trachea, protrusion of the right anterior tracheal wall into the lumen, with nearly complete occlusion during expiration resulting from compression by the right aortic arch (Fig. 3A). Another infant also underwent primary repair of the type-C esophageal atresia at 1 day of age and closure of an aortopulmonary window at 11 days of age. Because of persistent, recurrent respiratory insufficiency, the infant underwent tracheostomy at 2 months of age and repeated bronchoscopic examinations confirmed the diagnosis of severe tracheal compression by the right aortic arch. Five patients had trachea1 stenoses of congenital origin (3 with extensive and 1 with localized stenoses due to complete cartilaginous rings and 1 with subglottic stenosis). Three had associated complex intracardiac anomalies and 2 others had pulmonary artery slings (Table 1). All infants had symptoms of severe respiratory distress since the early months of life. The diagnosis of tracheal stenosis was established by bronchoscopy combined with plain tomography, computed axial tomographic scan of the chest, and bronchography if necessary (Figs. 4,5). Data for the first 2 patients with associated complex intracardiac anomalies and 1 patient with pulmonary artery sling in this group have been previously reported [26, 271.
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Fig. 2 A, B. Bronchoscopic views of carina and bilateral bronchi before (A) and after (B) the plico-suspension of pulmonary artery in a 7-month-old infant with ventricular septal defect and severe pulmonary hypertension. A flattening of the carina and severe stenosis of the left bronchus is obvious. B note the opened carina and the left bronchus with patent lumen
Fig. 3 A, B. Bronchoscopic views of trachea before (A) and after (B) the aortopexy in a l-month-old infant. A left posterior deviation of the trachea with protrusion of the right anterior tracheal wall into the lumen is indicated by urrows. B the lumen of the trachea is widely patent with disappearance of protrusion from right anterior aspect
Results of surgical intervention
(1) Severe bronchial compression by the distended pulmonary artery: Plico-suspension of the pulmonary artery [28] has been employed in all patients with this entity in conjunction with patch closure of the ventricular septal defects (11 patients), pulmonary artery banding (l), division of the ductus (1) and closure of the left coronary artery-to-right ventricular fistula (1). The distended main and left pulmonary arteries were plicated to normal size with horizontal mattress and additional running overand-over sutures. The plicated portion of the pulmonary artery was then suspended left-anterosuperiorly to the chest wall with 4 suspension sutures (Fig. l A-D) [28]. The effectiveness of this procedure for relief of bronchial compression was confirmed by intraoperative bronchoscopy before and after the procedure (Figs. 2A, B).
Fig. 4. Tomogram of the chest demonstrating extensive tracheal stenosis in an infant with scimitar syndrome and pulmonary artery. sling. Arrow indicate the area of tracheal stenosis
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Fig. SA, B. Computed axial tomogrztphic scan of the chest in the same patient as Fig. 4. Arrow indicates trachea just aabove (A) and in the middle of the stenotic area
(B)
Table 2. Results
of repair of ventricular septal defect associated with severe bronchial compression in infants Plico-suspension
of the pulmonary
artery
No
Yes Number of patients
10 (1 early death)
Age at operation
6.1 (range 3-9) months kg
5.0 (range 3-8) months
Body weight
4.4 (2.7-5.7)
Preoperative intubation
8110
316
Duration of postoperative intubation
14.7 (7-30) days
84.4 (20 - 194) days
5.4 (4.5-6.9)
kg
All but one, who died of sepsis on the 16th postoperative day, have survived the procedure with successful early extubation and are well at a mean follow-up of 99 months (18 to 150 months). To evaluate the effect of plico-suspension of the pulmonary artery on the postoperative course of the patients, various pre- and postoperative ciinical parameters of 10 infants who had this procedure concomitantly with repair of the ventricular septal defect in the current series
were compared to those of 6 infants with documented severe left bronchial compression associated with ventricular septal defect and severe pulmonary hypertension, and who only had repair of the ventricular septal defect in the 4-year period preceding February 1978 (Table 2). The mortality was lower and the period of postoperative respiratory care with endotracheal intubation was significantly shorter in the former than in the latter group of infants. (2) Tracheal compression by the right aortic arch: In both infants, surgical suspension of the ascending aorta to the right side of the sternum (aortopexy) [8] was carried out under bronchoscopic control with excellent subsequent relief of airway obstruction (Figs. 3 A, B). Both patients are well 9 years and 10 years, respectively, after operation. (3) Congenital tracheal stenosis: Two of 3 patients with associated complex intracardiac anomalies underwent concomitant repair of both lesions with the use of cardiopulmonary bypass [26]. In the first child (Syear-old), resection of the stenotic segment of the trachea (15 mm) and reconstruction by end-to-end anastomosis was accomplished on bypass following intracardiac repair of the tetralogy of Fallot. In the second patient, (Smonth-old), total reconstruction of an extensive tracheal stenosis using a large cartilaginous graft was carried out, also on bypass, following repair of cardiac defects by rerouting
483
Fig. 6. Diagrammatic portrayal of repair of pulmonary artery sling and tracheoplasty for extensive tracheal stenosis with a cartilaginous graft (stippled area)
the pulmonary venous blood from the right lung to the left atrium by covering the opening of a scimitar vein into the inferior vena cava and the atria1 septal defect with a generous patch and repair of the pulmonary artery sling by division of the anomalous artery and end-to-side reimplantation into the main pulmonary artery (Fig. 6). In the third patient, (3-month-old) with a complete form of common atrioventricular canal defect, the localized subglottic stenosis was enlarged by a cartilaginous graft together with pulmonary artery banding. The patient subsequently underwent successful definitive repair of the common atrioventricular canal defect. The postoperative course was uneventful in all 3 patients and they are doing well 45, 38 and 51 months, respectively, after operation. Two infants had a combination of pulmonary artery sling and extensive tracheal stenosis due to complete cartilaginous rings (ring/sling complex). Tracheal reconstruction with a cartilaginous graft and repair of the pulmonary artery sling with division and reimplantation of the left pulmonary artery into the main pulmonary artery was carried out in both patients with excellent subsequent relief of symptoms [27]. Tracheal reconstruction was effected with the use of extracorporeal membrane oxygenator in 1 patient. One patient had a recurrence of respiratory distress due to tracheomalacia and subsequently underwent aortopexy as a second operation 4 months later. The postoperative course was uneventful but he died suddenly at home 1 year after the initial operation of lower respiratory infection. The other patient is doing well 8 months after operation. Discussion
Airway obstruction in infants with congenital heart disease may complicate the natural and surgical history of the patients and significantly increases mortality and morbidity following surgical intervention to the cardiac lesions [2, 3, 5, 69, 11, 13, 15, 16, 19-22, 241. Early and
accurate preoperative diagnosis of the airway lesion is mandatory to plan the appropriate treatment to avoid complications. In general, infants’ airways are more susceptible to extrinsic compression as the cartilaginous, muscular and elastic supports of airway are weak and the bronchial lumen is small [9, 10, 15, 241. Resistance to air flow through the bronchial lumen is inversely proportional to the fourth power of radius. Therefore, relatively slight degrees of compression or intraluminal narrowing of the small bronchi of young infants will result in bronchial obstruction than in older children whose airways are larger. The airway of young infants contains relatively more mucous glands than that of adults, and there are age differences in chemical composition of the mucus [lo]. Furthermore, the pores of Kohn and canals of Lambert, which normally allow collateral ventilation in the event of bronchial obstruction, are poorly developed in infants [lo, 151.As a consequence, small amounts of edema, mucus or inflammatory debris may markedly narrow or completely occlude a infant’s bronchus or bronchiole resulting in air trapping or atelectasis. Severe airway compression occurring in infants with congenital heart disease as a result of altered hemodynamics or anomalous relationship between the tracheobronchial tree and vascular structures are well documented in patients with vascular ring, tetralogy of Fallot with absent pulmonary valve, or with various congenital heart diseases with increased pulmonary blood flow and pulmonary hypertension as seen in our patients [2,3,5,6, 9, 11, 13, 15, 16, 19-22, 241. The presence of severe bronchial compression is suspected by the onset of recurrent severe respiratory distress characterized by stridor and wheezing in the early months of life, findings of persistent atelectasis or occasionally of air trapping in the left lung and hyperinflation of the right lung with shift of the heart and mediastinum to the left on a chest X-ray, blurring of the bronchial tree in the affected area on the frontal view and narrowing in the lateral view of high voltage chest roentgenograms. Bronchographic or bronchoscopic examination is mandatory for accurate diagnosis. We consider bronchoscopy using a pediatric ventilation bronchoscope the safest, most helpful and definitive diagnostic tool in critical infants with airway obstruction associated with congenital heart disease. The place for tracheobronchography which requires extreme care during the procedure to avoid aggravating the condition of the compromized airway in these high-risk infants, is very limited in our experience. In all infants with potential airway compression or stenosis, we suggest that preoperative bronchoscopy be considered as one of the routine evaluations, and when the nature of obstruction becomes evident, the operation must be planned to avoid postoperative complications. In the case of severe left bronchial compression by a distended pulmonary artery, we successfully relieved the bronchial compression by plico-suspension of the pulmonary artery concomitantly with a corrective or palliative operation for the congenital cardiac defects [28]. Although we have not experienced a case, a recent report [6] emphasized the effectiveness of left pulmonary artery
484
transection and prolongation with a prosthetic conduit for this type of lesion, but this technique has a disadvantage, so that it would eventually require replacement of the conduit as the patient grows. It is well known that in infants with severe prolonged airway compression, the deformity and pliabilaity of the tracheobronchial wall may persist for a considerable period of time even after the removal of causative factors by operation until the airway recovers stiffness to maintain patency [3,28]. This fact accounts for the increased postoperative mortality and morbidity due to respiratory distress after operation for a cardiac anomaly, if an effective measure to relieve airway obstruction has not been undertaken simultaneously. The result of this current study underscores the effectiveness of concomitant plico-suspension of the pulmonary artery for decreasing the mortality and shortening the period of postoperative respiratory care in infants with severe bronchial compression associated with congenital heart disease. In 2 cases with tracheal compression by the right aortic arch, both in infants with previous primary repair of a congenital tracheoesophageal fistula and correction of associated cardiovascular anomalies, and in 1 case with tracheomalacia following complete reconstruction of extensive tracheal stenosis and pulmonary artery sling, we attempted aortopexy as reported by Filler et al. [8]. Satisfactory relief of the tracheal compression was obtained in all cases as reported by others [4, 8, 231. A combination of severe congenital tracheal stenosis and congenital heart disease still remains a therapeutic challenge [6, 181.It was only recently that successful reconstructive surgery for stenosis of the intrathoracic trachea in infants and small children has been reported [I, 7, 12, 14, 17, 18, 251. In infants and small children with a combination of stenosis of the intrathoracic trachea and complex congenital heart disease, the situation becomes more complicated. Surgical intervention for this combination in a staged fashion had been accompanied by a poor prognosis because the presence of the other untreated lesion usually poses problems in postoperative management [6, 181. We attempted simultaneous repair of tracheal stenoses at the time of surgery for congenital cardiac lesions in 5 patients: at the time of repair of complex cardiac anomalies with the aid of cardiopulmonary bypass in 2 patients [26], at the time of repair of pulmonary artery sling in 2 patients [27] (in 1 with the aid of extracorporeal membrane oxygenation), and at the time of pulmonary artery banding for a complete form of atrioventricular canal defect. The promising results we have obtained suggest that obstructive lesions of the trachea are amenable to appropriate reconstruction at the time of surgery for cardiac lesions with the aid of cardiopulmonary bypass, if necessary. In conclusion, we advocate the following to minimize the potentially deleterious effects of airway obstruction associated with congenital heart disease: (1) early preoperative identification of infants with potential airway obstruction and accurate definitive diagnosis with the use of the pediatric ventilation bronchoscope, (2) selection of appropriate surgical procedures specific to the type and cause of airway obstruction, and (3) early aggressive con-
comitant repair of both lesions, with the aid of cardiopulmonary bypass if necessary, to obtain a better outcome in the surgical management of infants and small children with this difficult and often fatal combination.
References 1. Akl BF, Yabek SM, Berman W Jr (1984) Total tracheal reconstruction in a three-month-old infant. J Thorac Cardiovasc Surg 87: 543-546 2. Backer C, Ilbawi MN, Idriss FS, De Leon SY (1989) Vascular anomalies causing tracheoesophageal compression: review of experience in children. J Thorac Cardiovasc Surg 97: 725-731 3. Bradham RR, Sealy WC, Young WG (1968) Respiratory distress associated with anomalies of the aortic arch. Surg Gynecol Obstet 126:9-14 4. Campbell DN, Lilly JR, Heiser JC, Clarke DR (1983) The surgery of pulmonary artery “sling”. J Pediatr Surg 18:855856 5. Cohen SR, Landing BH (1976) Tracheostenosis and bronchial abnormalities associated with pulmonary artery sling. Ann Otol 85:482-590 6. Corno A, Giamberti A, Giannico S, Marino B, Rossi E, Marcelletti C, Kirklin JK (1990) Airway obstruction associated with congenital heart disease in infancy. J Thorac Cardiovasc Surg 99: 1091-1098 I. Ein SH, Friedberg J, Williams WG, Rearon B, Baker GA, Mancer K (1982) Tracheoplasty -a new operation for complete congenital tracheal stenosis. J Pediatr Surg 17: 872-878 8. Filler RM, Rosselo PJ, Lebowitz RL (1976) Life-threatening anoxic spells caused by tracheal compression after repair of esophageal atresia: correction by surgery. J Pediatr Surg 11:739-748 9. Fischer DR, Neches WH, Beerman LB, Fricker FJ, Siewers RD, Lenox CC, Park SG (1984) Tetralogy of Fallot with absent pulmonic valve: analysis of 17 patients. Am J Cardio153: 14331437 10. Griscom NT, Wohl MEB, Kirkpatrick JA (1978) Lower respiratory infections: how infants differ from adults. Radio1 Clin North Am 16: 367-387 11. Habbema L, Losekoot TG, Becker AE (1980) Respiratory distress due to the bronchial compression in persistent truncus arteriosus. Chest 77:230-232 12. Idriss FS, DeLeon SY, Ilbawi MN, Gerson CR, Tucker GF, Hollinger L (1984) Tracheoplasty with pericardial patch for extensive tracheal stenosis in infants and children. J Thorac Cardiovasc Surg 88: 527-536 13. Jones JC, Almond CH, Snyder HM, Meyer SW, Patrick JR (1965) Lobar emphysema and congenital heart disease in infancy. J Thorac Cardiovasc Surg 49: I-IO 14. Kimura K, Mukohara N, Tsugawa C, Matsumoto Y, Sugimura C, Murata H, Itoh H (1982) Tracheoplasty for congenital stenosis of the entire trachea. J Pediatr Surg 17: 869-871 15. Lakier JB, Stanger P, Heymann MA, Hoffman JIE, Rudolph AM (1974) Tetralogy of Fallot with absent pulmonary valve: natural history and hemodynamic considerations. Circulation 50: 167-175 16. Leape LL, Ching N, Holder TM (1970) Lobar emphysema and patent ductus arteriosus. Pediatrics 46: 97- 101 17. Mattingly WT Jr, Belin RP, Todd EP (1981) Surgical repair of congenital trachea1 stenosis in an infant. J Thorac Cardiovasc Surg 81:738-740 18. Nakayama DK, Harrison M, de Lorimier AA, Brasch RC, Fishman NH (1982) Reconstructive surgery for obstructive lesions of the intrathoracic trachea in infants and small children. J Pediatr Surg 17: 854-868 19. Nikaidoh H, Riker WL, Idriss FS (1972) Surgical management of “vascular rings.” Arch Surg 105: 327-333
485 20. Pontius RG (1963) Bronchial obstruction of congenital origin. Am J Surg 106:8-14 21. Rivkin LM, Read RC, Lillehei CW. Varco RL (1957) Massive atelectasis of the lung in children with congenital heart disease. J Thorac Cardiovasc Surg 34: 116-125 22. Sade RM, Rosenthal A, Fellows K, Castaneda AR (1975) Pulmonary artery sling. J Thorac Cardiovasc Surg 69: 333-346 23. Schwartz MZ, Filler RM (1980) Tracheal compression as a cause of apnea following repair of tracheoesophageal tistula: treatment by aortopexy. J Pediatr Surg 15: 842-848 24. Stanger P, Lucas RV, Edwards JE (1969) Anatomic factors causing respiratory distress in acyanotic congenital cardiac disease, special reference to bronchial obstruction. Pediatrics 43: 760-769 25. Weber TR, Eigen H, Scott PH, Krishna G, Grosfeld JL (1982) Resection of congenital tracheal stenosis involving the carina. J Thorac Cardiovasc Surg 84: 200-203 26. Yamaguchi M, Oshima Y, Hosokawa Y, Ohashi H, Tsugawa C, Nishijima E, Tsubota N (1990) Concomitant repair of congenital tracheal stenosis and complex cardiac anomaly in small children. J Thorac Cardiovasc Surg 100: 181- 187
27. Yamaguchi M, Oshima Y, Ienaga T, Tsugawa C, Kimura K, Matsumoto Y (1986) Successful repair of pulmonary sling associated with congenital tracheal stenosis in an 8-month-old infant. J Jpn Assoc Thorac Cardiovasc Surg 38: 85-89 (in Japanese) 28. Yamaguchi M, Nishiyama N, Hosokawa Y, Tachibana H, Horikoshi K, Toriyama A, Mito H, Tei G, Ohashi H, Ogawa K (1981) Plication and suspension of the pulmonary artery for severe left bronchial compression in infant with ventricular septal defect. J Jpn Assoc Thorac Cardiovasc Surg 29: 86-98 (in Japanese)
Masahiro Yamaguchi, MD Department of Cardiothoracic Kobe Children’s Hospital Takakuradai l-l-l, Suma-ku Kobe 654 Japan
Surgery
