Bronchopulmonary arterial communications in pulmonary atresia with ventricular septal defect

Bronchopulmonary in Pulmonary

Arterial

Communications

Atresia with Ventricular Septal Defect*

HELEN

STARKE, M.D., DAVID

PUGH, M.D. and MARVIN

Kansas

DUNN,

M.D., F.A.C.C.

City, Kansas

The case of a 23 year old woman with pulmonary atresia and ventricular septal defect is presented. A continuous murmur was produced by large bilateral anastomoses between bronchial and first order pulmonary arteries. Interesting clinical features included absence of cyanosis because of large pulmonary blood flow, and successful completion of a pregnancy. Death was due to the rupture of a large pulmonary aneurysm.

I

N

was no further medical evaluation until she was 8 years old (1952), when she was seen at the Colorado General Hospital. Reports from that institution indicate that she had no cyanosis, clubbing, or edema. Blood pressure was 100/58 mm. Hg. The jugular venous pressure was not elevated, but a right ventricular heave and apical thrust were noted. The point of maximal impulse was 2 to 3 cm. to the left of the midclavicular line in the sixth interspace. Auscultatory findings included a regular rhythm, a loud systolic ejection click and a continuous murmur that was heard over the entire chest including the back.

PATIENTS WITH PULMONARY ATRESIA main-

tenance of an adequate

pulmonary blood flow To is the major determinant of life expectancy. provide adequate pulmonary blood flow, a portion of the systemic circulation is directed to the lung through a patent ductus arteriosus or through dilated bronchial arteries.rB3 A continuous murmur is often heard as a result of this systemic artery to pulmonary artery shunt. Wood4 found a continuous murmur in each of his 15 patients with pulmonary atresia, but reports of other investigators1*5-g suggest a continuous murmur is present in only about 60 per cent of patients with this disorder. If the ductus is not patent, the continuous murmur may result from large communications between the bronchial arteries and primary or secondary divisions of the pulmonary artery.6~*~1a-16 This report concerns a 23 year old woman with pulmonary

atresia,

ventricular

Cardiac ca6heterization was performed on January 28, 1352. Although a persistent left superior vena cava was encountered, the catheter was advanced through the right atrium, right ventricle and entered a large aorta with a right-sided aortic arch. The pulmonary artery could not be entered. Pertinent oxygen and pressure data are listed in Table I. The angiocardiogram demonstrated only one vessel arising directly from the heart. It was overriding a large ventricular septal defect. The pulmonary arteries opacified from the descending aorta presumably from bronchial arteries.

septal defect and a

continuous murmur due to large bronchial to pulmonary arterial flow who died as a result of rupture of a pulmonary arterial aneurysm.

Systemic cardiac index was 2.4 and pulmonary flow was 5.0 L./min. per M.2. Since the pulmonary arteries received their entire blood supply from the aorta, pulmonary flow was estimated by using the aortic-pulmonary vein arteriovenous difference. Left to right shunt was 3.3 and right to left shunt was 0.8 L./min. per M.2.

CASE SUMMARY This Mexican-American woman was 13 years old when first seen at the University of Kansas Medical Center in 1964 with complaints of exertional dyspnea and fatigue. Cyanosis and a heart murmur were first noted when she had pneumonia at age 2 years. There

* From the Department of Medicine, Cardiology Section, University of Kansas Medical Center, Kansas City, Kans, This investigation was supported by National Institutes of Heaith Training Grant 5 TO1 HE05670-03 from the National Heart Institute. Manuscript received September 4, 1968, accepted January 29, 1969. Address for reprints: Marvin Dunn, M.D., Cardiovascular Laboratory, University of Kansas Medical Center, Rainbow Blvd. at 39th St., Kansas City, Kans. 66103. 570

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Bronchopulmonary Table

I.

Cardiac

Catheterization 02 Content (vol. %)

02 Sat. (%)

11.9 11.4 10.7 11.7 14.5 18.3 15.8 15.8

62 59 56 61 76 96 83 83

Distal SVC Proximal SVC Right atrium RV inflow RV outflow Pulmonary vein Aorta Femoral artery RV

= right ventricle;

Arterial

SVC

= superior

Communications

Atresia

571

Data Systolic Pressure (mm. Hg)

92-98 92-98 92-98 vena cava.

Examination in 7964 in the outpatient department of the University of Kansas Medical Center disclosed essentially the same findings as those recorded earlier. The electrocardiogram showed right axis deviation and biventricular hypertrophy. Fluoroscopy revealed moderate cardiomegaly, generalized chamber enlargement, and dilatation of the right and left pulmonary arteries and ascending aorta. Clinical Course: She was not seen after initial clinic visit until September 1965, when she was in the fifth month of pregnancy. Exertional dyspnea (one flight of stairs) became troublesome during the third or fourth month of pregnancy, but there was no overt heart failure. Blood pressure was 100/50 mm. Hg and pulse 72 to 80/min. Cyanosis was not observed. Hemoglobin was 13.0 to 15.8 gm./lOO ml. and hematocrit was 41 per cent. On January 11, 1966, a normal 2,600 gm. male child was delivered without difficulty and on January 18, tubal ligation was performed. The patient was not seen until August 7, 1967, when she returned because of a continuous pain under the left breast after she had fallen down a flight of stairs. Rales were noted at the left base. No fractures were found. A chest roentgenogram showed generalized cardiomegaly (Fig. 1). Huge discrete perihilar nodular masses were thought to be vascular shadows, but there were no distal vascular markings. The possibility of an aneurysm of the pulmonary artery was considered. Patchy and linear infiltrates visible throughout the lung fields suggested cardiac decompensation. The patient declined admission to the hospital and did not return for follow-up examination. On October 8 she suddenly collapsed, lost consciousness at home and was dead on arrival at the emergency room. AUTOPSY DATA Multiple congenital anomalies of the heart and great vessels were observed. There was an overriding aorta and an interventricular septal defect 1 by 2.5 cm. in diameter in the membranous portion of the septum. The pulmonary artery arose from the correct location and was completely separate from VOLUME 24, OCTOBER 1969

in Pulmonary

Figure 1. Chest roentgenogram (posteroanterior shows large pulmonary arteries.

view)

the aorta. However, the pulmonary valve was only 0.5 cm. in diameter and was completely atretic. The right and left pulmonary arteries became aneurysmally dilated and tortuous immediately distal to the bifurcation of the main pulmonary artery. The pulmonary arteries then narrowed to a diameter of 1 cm. immediately distal to the aneurysms but proximal to the site of anastomoses with the bronchial arteries. The site of the anastomosis of the left bronchial to pulmonary artery measured 0.8 cm. in diameter, that of the right, 0.7 cm. (Fig. 2). A huge aneurysm measuring 8 by 5 cm. in the left pulmonary artery was filled with laminated thrombus. A similar aneurysm measuring 7 by 4 cm. in the right pulmonary artery had ruptured through the lobular septums of the middle and lower lobes resulting in massive intrapleural hemorrhage (2,500 cc. of blood). Microscopically there was marked intimal proliferation and marked hypertrophy of the media of the pulmonary arteries and arterioles, thus suggesting long-standing pulmonary hypertension (Fig. 3). Recent and old thrombi, some with recanalization, were seen in the pulmonary arterial branches. There were small ulcerations of the intima in the pulmonary arteries in the region of the aneurysm. DISCUSSION Pulmonary

atresia has been considered

tively uncommon ease. cases

However, of

form Abbott,5

congenital

of congenital

a rela-

heart dis-

in 1,000 autopsies

heart

disease,

found

of 40

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Starke

et al. tion to the lungs through the bronchial arteries in 21 cases of pulmonary atresia or pulmonary stenosis. East et aL2i demonstrated enlargement of bronchial arteries in 2 patients with pulmonary atresia who survived to 33 and 20 years of age, respectively. In neither instance was the ductus patent, but the bronchial arteries were 10 to 15 mm. in diameter. Normally no anastomoses exist between bronchial and pulmonary arteries except through the capillary plexus to which both contribute. Miller25 demonstrated this in normal dogs by injecting dyecolored gelatin into the pulmonary artery or pulmonary vein. The bronchial artery filled only from the pulmonary vein injection but never from the pulmonary artery injection, thereby indicating that no anastomoses exist between the bronchial and pulmonary arteries except through the capillary plexus. Wood and Millerz6 confirmed this finding in man. On the other hand, they were able to demonstrate large vascular shunts between bronchial and pulmonary arterial systems in certain instances of pulmonary and cardiac disease. In normal human subjects the bronchial artery contribution to the total pulmonary blood flow is too insignificant to

Figure 2. Photograph of autopsy specimen shows site of communication between bronchial artery and pulmonary artery. Ao = aorta; BA = bronchial artery; PA = pulmonary artery.

examples of this defect (30 with associated ventricular septal defect) compared to 110 cases of pulmonary stenosis of all types. Keith et a1.g compiled 7 series of autopsy reports which included 418 cases of tetralogy of Fallot and 95 cases of pulmonary atresia with ventricular septal defect. Taussig’? studied those patients with tetralogy of Fallot with anatomic or functional pulmonary atresia and noted that death generally occurred between 3 and 14 months of age. There have been notable exceptions of longevity, however, which depended on adequate pulmonary circulation either through a patent ductus arteriosus or through the development of adequate collateral vessels.4*5J8-23 Peacock% was among the first to demonstrate dilated bronchial arteries in pulmonary stenosis and pulmonary atresia. In 1 of his cases the ductus was closed but the pulmonary artery was supplied by the left subclavian artery; in another, several large vessels arose from the aorta and supplied the lungs. Christeller’* demonstrated the development of a collateral circula-

Figure 3. Photomicrografih of the lung demonstrates medial hypertrophy and intimal proliferation of a typical pulmonary arteriole. (X 115, reduced by 15 per cent.) THE

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Bronchopulmonary

Arterial

Communications

6

G Figure 4. Four mm. cat embryo demonstrates embryologic basis for potential communication between bronchial and pulmonary arterial communications. BAA = bronchial artery anlagen; G = gut; L = lung bud; 4 = fourth aortic arch; 6 = sixth aortic arch.

measure, but the bronchial

arteries may contribute 25 per cent of the total pulmonary blood flow in patients with tetralogy of Fallot.27J8 There is an embryologic basis for potential communication between bronchial and pulmonary vasculaturezg (Fig. 4). The primitive pulmonary plexus which is destined to become the capillary plexus served by the pulmonary artery is derived from ventral branches of the dorsal aorta and is formed before the pulmonary artery. There is a stage in the development of the pulmonary artery and regression of the ventral branches of the dorsal aorta when the plexus is actively supplied by both and anastomoses between pulmonary artery and branches from the aorta occur. It is possible that in the developing fetus with pulmonary atresia the immature vascular networks may unite to produce communications between larger bronchial and pulmonary arteries as well as between smaller ones. A continuous murmur is relatively infrequent in tetralogy of Fallot, but is common in pulmonary atresia. Taussig l7 stated that a continuous murmur depended on continuous blood flow from the aorta to vessels of collateral circulation to the lungs. This, in turn, is dependent on the systemic VOLUME 24,

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blood pressure, the size of the vessels to the lungs, and the pulmonary vascular resistance. Since the size of the collateral vessels tends to increase with the growth of the individual, it is not uncommon for a continuous murmur to appear for the first time during infancy or early childhood. The muscular layer of the pulmonary arteries is thin in patients with pulmonary atresia and sometimes the bronchial arteries are thin-walled, Best and Heath30 measured the mean relative thickness of the media in 4 cases of cyanotic congenital heart disease without pulmonary hypertension and found a mean relative thickness (of media expressed in per cent of external diameter) of 2.0 to 2.5 per cent compared to the normal thickness of 5 per cent. Our patient illustrates several interesting features of pulmonary atresia with ventricular septal defect. Cyanosis was never appreciable, thus indicating that she had a large pulmonary blood flow. Although the ductus was closed, there were large communications between the bronchial and pulmonary arteries bilaterally, and a pressure gradient must have coexisted to produce the continuous murmur. The sequence of events leading to our patient’s death and the pathologic jndings may have occurred as follows: The large anastomoses between the bronchial and pulmonary arteries may have permitted a large pulmonary flow under a high head of pressure. Since the pulmonary arteries were congenitally thin, the combination of high flow and high pressure may have contributed to the formation of the aneurysms. It is, of course, possible that the aneurysms were congenital and gradually increased in size. One can only speculate about the relation between the trauma that occurred two months before the patient’s death and the subsequent dissection and rupture of the aneurysm. A degree of pulmonary hypertension was confirmed pathologically by the marked increase in the thickness of the media of the pulmonary arteries. The thromboses of the small arteries in the lungs were both recent and old and some showed “glomerular” recanalization. In cyanotic congenital heart disease with low pulmonary blood flow, small vessel thrombosis with evidence of recanalization has been attributed to stagnation resulting from decreased volume of blood, decreased flow and increased viscosity associated with high hematocrit.31 In our patient these pathologic findings were more likely due to pulmonary hypertension and to peripheral emboli from clots in the large pulmonary arteries. If

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there had been an increase in pulmonary vascular resistance, more marked cyanosis and polycythemia would have been likely because of the decreased pulmonary flow. ACKNOWLEDGMENT We acknowledge our appreciation to Dr. S. Gilbert Blount, Jr., Professor of Medicine, University of Colorado, Denver, Colo., for his consultation and permission to publish the catheterization data from his laboratory.

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