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Stenosis of individual pulmonary veins
Stenosis of individual pulmonary veins Review
0/ the
literature and report 0/ a surgical case
Stenosis or atresia of the individual pulmonary veins is a rare condition that is usually fatal when untreated, even when only one side is involved. The lesion can be diagnosed at cardiac catheterization by pressure and angiographic data. The surgical approach to pulmonary vein stenosis must be flexible. The technique of repair will depend upon the local anatomy of each lesion. Those of the diaphragmatic type can be treated effectively by excision of the obstructing membrane. Increase of the vein's caliber can be achieved by patch angioplasty . When segmental stenosis or atresia is present, it may be necessary to anastomose the vein directly to the left atrium. Relief of most types of extrapulmonary venous stenosis and atresia should be possible with currently available techniques. If relief of the obstruction is not possible, undrained pulmonary tissue should be excised whenever technically feasible.
Robert M. Sade, M.D., Michael D. Freed, M.D., Edward C. Matthews, M.D., and Aldo R. Castaneda, M.D., Boston, Mass., and Portland, Maine
Stenosis or atresia of the pulmonary veins without anomalous connection is a rare cause of pulmonary artery hypertension. Of the twenty-three cases that have been reported, four have been corrected surgically,"- 19, 2(; and three of them were correctly diagnosed preoperatively.": 2(; This report describes a patient with pulmonary vein atresia whose lesion was diagnosed at cardiac catheterization and then partially corrected at operation. Case report O. E. (CHMC No. 77-75-18) was admitted to CHMC on Dec. 20, 1972, at the age of 8 months. At the age of 5 months she had been admitted to Maine Medical Center with a history of repeated pulmonary infections and failure to thrive. At that time work-up was negative with
From the Departments of Cardiovascular Surgery and Cardiology, The Children's Hospital Medical Center and Harvard Medical School, Boston, Mass. 02115, and the Maine Medical Center, Portland, Maine 04102. Received for publication Jan. 28, 1974. Address for reprints: Robert M. Sade, M.D., Department of Cardiovascular Surgery, Children's Hospital Medical Center, 300 Longwood Ave., Boston, Mass. 02115.
the exception of mild tachypnea and mild cardiomegaly on x-ray study. The electrocardiogram was normal. Because she was thought to be in mild congestive heart failure she was treated with digitalis but without improvement. Over the next 3 months she continued to have respiratory difficulties, manifested by rapid, labored breathing without fever. On readmission to Maine Medical Center at 8 months of age, she was a small, thin infant in moderate respiratory distress. A Grade 2/6 systolic murmur was audible along the left sternal border. The pulmonic second sound was normally split and mildly accentuated. An electrocardiogram showed mild right ventricular hypertrophy, and a chest x-ray film disclosed mild cardiomegaly and increased pulmonary blood flow. Cardiac catheterization was performed. There was no evidence of an intracardiac shunt. The pulmonary artery pressure was mildly elevated (50/17 mm. Hg, mean 30 rnrn. Hg), as were wedge pressures in the right and left upper pulmonary arteries (mean 22 mm. Hg). The left atrium and ventricle were not entered. Anteroposterior and lateral cineangiograms were performed by injection of contrast medium into the main pulmonary artery. There was prompt opacification of a dilated right lower pulmonary artery. The left pulmonary arteries an~ right upper and middle pulmonary arteries were quite small, less than one third the size of the right lower pul-
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A.
Upper P.V.
B.
Lt. Atria and Lower P. V. Incised
Lower P. V.
Fig. 1. A, The atretic left upper and lower pulmonary veins (P.v.) and the right upper pulmonary vein are depicted with the corresponding hypoplastic pulmonary arteries (P.A .). B, The narrowed segment of the left lower vein was opened and atresia was found; the vein was ligated and opened proximally. Then an opening was created in the adjacent left atrium. C and D, A side-to-side anastomosis of vein to left atrium was carried out.
monary artery. During the levophase, the right lower pulmonary vein drained normally into the left atrium. The other pulmonary veins were poorly visualized. The left atrium was of normal size, and the atrial appendage was in its usual position. The left ventricle was of normal size and filled promptly from the left atrium. On the basis of elevated wedge pressures, pulmonary artery hypertension, and the cineangiograms, the physicians believed that the child had obstruction to pulmonary venous return of the right upper, left upper, and left lower veins. They could not determine whether this was due to partial cor triatriatum or to obstruction of the individual pulmonary veins. Because of recurrent episodes of labored, gasping respirations associated with cyanosis, thought to be due to acute pulmonary edema, the child was transferred to Children's Hospital Medical Center for surgical intervention.
Findings on admission were unchanged. An echocardiogram disclosed a normal-sized left atrium and left ventricle and a mobile mitral valve. On Dec. 22, 1972, the patient was taken to the operating room. With the child under deep hypothermia and circulatory arrest, the left atrium was opened. The four pulmonary vein orifices were normally placed, but upper vein openings were atretic, represented by a dimple in the posterior left atrial wall. The heart was retracted anteriorly, and the left lower pulmonary vein was found to be dilated proximal to its junction with the left atrium. Incision of the vessel revealed an atretic segment about 5 mm. long immediately proximal to its junction with the left atrium. A small incision was made in the left atrium just above the inferior vein orifice, and a side-to-side anastomosis of the proximal pulmonary vein to the left atrium was carried out (Fig. I). Explora-
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Fig. 2. Radionuclide angiocardiography after injection of 991lltechnicium as sodium pertechnetate into the inferior vena cava . 1, One second after inferior vena caval injection, radionuclide has appeared in the right atrium and ventricle a nd is beginning to appear in the pulmonary artery. 2, The pulmonary artery is now clearly seen, with good visualization of the right pulmonary artery and right lower lung field; there is slight visualization of the left lower lung field. 3, Radionuclide is heavily concentrated in right lower lung field, moderately so in the left lower lung field, and is .barely detectable in the upper lung fields. 4, Returning radionuclide fills the left heart and the ascending aorta. 5, The descending aorta is now apparent , with early filling of abdom inal viscera; the upper lung fields are filling mostly from bronchial flow, especially on the right. 6, Emptying of the left heart and aorta into the systemic circulation is seen. tion of the left superior pulmonary vein revealed an atretic cord extending into the pulmonary parenchyma. Exploration of the right superior pulmona ry vein revealed severe stenosi s of the vein at its emergence from the pulmonary parenchyma, as well as a segment of complete atresia about I ern, long near the atrium. The right lower pulmonary vein was inspected and found to be normal in caliber. The right upper lobe artery was ligated. Cardiopulmonary bypass was reinstituted and the patient rewarmed. Postoperatively, the patient required intensive pulmonary care and remained intubated until the fourth postoperative day . On the second day after extubation a chest x-ray film showed edema and atelectasis of the left upper lobe. The patient was treated aggre ssively with diuretic and pulmonary therapy, and the lung was completely clear 2 day s later. Throughout the postoperative per iod chest films showed a vascular pattern of pulmonary venous congestion in both the left upper and left lower lobe areas. Pulmon ary blood flow was clearly increased to the right lower lobe. At the time of discharge the right lower lobe was somewhat increased in volume and the right upper lobe somewhat diminished in volume. uHIllT ech netium pulmonary scan showed absence of flow to the right upper lung field, severe reduction of flow to the
left upper lung field, and moderate reduction of flow to the left lower lung field. The right lower lung field received a major portion of the pulmonary blood flow ( Fig. 2) . The patient was discharged on the eighteenth postoperative day. Her only medication was digoxin. The child returned to the remote community in which she lived . About 1 month after discharge she was admitted to a local hospital with pneumonia and congestive heart failure . She was treated with diuretics and digitalis. After initial improvement she apparently developed an influenza-like illness and died within a few days. No autopsy was obtained.
Discussion
There have been 23 case reports of localized pulmonary vein stenosis; ours is the twenty-fourth. The age range of these patients has been from the neonatal period to 15 years, but most were under the age of 6 years. Other data i are summarized in Table 1. ' In 7 cases, all four veins were obstructed. In 11 cases, obstruction was unilateral, and in 2 of them , only one vein was obstructed.
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Table I Author (date) Reye (1951) Emslie-Smith et al. 1 4 (1955) Ferencz and Dammann!" (1957) Andrews! (1957) Sherman et al. 2 9 (1958) 27
Patient's age
I
I
Veins involved
8 yr. 13 yr. 2 yr. 3 yr. 8\12 mo.
RUY, RLY, LUY, and LLY RUY and RLY LUY and LLY LUY and LLY RUY, RLY, and LLY
6 yr.
RUY, RLY, LUY, and LLY
1 yr.
Symptoms Congestive heart failure Cyanosis Cyanosis; dyspnea; failure to thrive Recurrent respiratory infections; failure to thrive Hemoptysis
Bernstein et al.! (1959) Edwards"! (1960) Case 5 Case 6 Case 7 Shone et al. 3 0 (1962) Lucas et al. 2 1 (1963) Jue et al.!S (1965) Singshinsuk et al. 3 1 (1966) MoHer et al. 2 :J (1966) Contis et al.v (1967)
1Y2 yr. 10 yr. 7 mo. 6 yr. 8 wk. 6 yr. 6 mo. 12 yr.
RUY, LCY RCY RUY, RUY, LUY RUY, RUY, RUY,
l\;lakib et al. 24 (1967)
6 wk.
LLY
Nakib et al. 2 4 (1967) Snellen and Bruins"> (1968) Becker et al." (1970)
2 yr. 13 yr. Stillborn
LCY RCY RUY, RLY, LUY, and LLY
None related to vein obstruction Cyanosis
Kawashima et al.l!' (1971)
15 yr.
RUY and LCY
Binet et al.a (1972) Park et al. 2 r> (1973) Park et al. 2<> (1973) Sade et al. (1974)
5 yr. 1 yr. 12 yr. 10 mo.
RUY RUY RUY, RUY,
Cyanosis; frequent respiratory infections Hemoptysis; recurrent cough
RLY, LUY, and LLY
RLY, LUY, and LLY RLY, LUY, and LLY LUY, and LLY RLY, and LLY LUY, and LL Y
and RLY and RLY RLY, LUY, and LLY LUY, and LLY
Cyanosis; failure to thrive Cyanosis and cyanotic spells Recurrent respiratory distress None Congestive heart failure; recurrent pneumonia
Recurrent respiratory infections
Legend: RUV, Right upper vein. RLV, Right lower vein. ReV, Right common vein. LUV, Left upper vein. LLV, Left lower vein, Ventricular septal defect. A-V, Atrioventricular. PFO. Patent foramen ovale.
In 6 cases, including the present one, all veins but one were stenotic or atretic. The anatomy of the obstruction is variable. There are a number of possibilities: a complete diaphragm at the venoatrial junction or in the vein proximal to the atrium; a partially obstructing diaphragm; a stenotic localized segment of vein; or atresia of the entire extra pulmonary vessel. Many individual patients have had different types of obstructions in different veins. Further obstruction of a stenotic vein may be produced by local thrombus." " Histologically, thickening of the intima by avascular cellular fibrous tissue often is the cause of obstruction 11; in some cases the vein is reduced to a fibrotic atretic cord. t
An obstructing diaphragm may contain scattered muscle bundles surrounded by connective tissue, in addition to intimal fibrosis." Usually, no inflammatory cells are present. In 14 cases from this group of patients, other cardiac anomalies were associated. These are summarized in Table I. Etiology
Pulmonary venous obstruction can be congenital or acquired. In acquired disease, the interior of the pulmonary veins may be obstructed by left atrial mural thrombus, myxoma," or pulmonary veno-occlusive disease'"'; on the other hand, the veins may be compressed extrinsically by neoplasms,
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Associated cardiac lesions
Surgery
Outcome
None PDA None Tricuspid atresia; TGA None
Death Death Death Death Death
None
Death
Small ASD Mitral atresia; ASD; VSD Persistent common A-V canal Large ASD Tetralogy of Fallot Pulmonary artery sling None ASD None
Death Death Death Death Postop, death Postop. death Alive and asymptomatic Death Death
Atresia of aortic and mitral valves; coarctation of aorta Coarctation of aorta with hypoplastic arch VSD Corrected TGA; Ebstein-like left A-V valve; muscular VSD; premature closure of PFO ASD; VSD None VSD None
Repai r of tetralogy of Fallot Exploratory right thoracotomy
Death Repair of VSD
Death Not stated Death
Relief of RUV and LeV stenoses
Alive 2 yr. postop.
Relief Patch Patch Relief
Alive 6 mo. postop, Postop. death Alive Postop. death
of RUV and RLV stenoses angioplasty of both involved veins angioplasty of all veins (age 12 yr.) of LLV stenosis only
_CV, Left common vein. PDA, Patent ductus arteriosus. TGA, Transposition of the great arteries. ASD, Atrial septal defect. VSD,
mediastinal fibrous masses,'> or by fibrosis resulting from chronic pulmonary infections.") It is occasionally difficult to determine whether specific stenoses are congenital or acquired since evidence may be adduced to support both possibilities in an individual case:' However, most cases of pulmonary venous stenosis and atresia are probably congenital. The evidence for this was summarized by Shone": (1) Clinical evidence of the lesion usually begins at a young age; (2) other congenital anomalies are frequently associated; (3) there is usually little or no evidence of active inflammation; and (4) the obstructive lesion occurring in normally connecting veins is similar to that seen in
veins connecting with structures other than the left atrium. Additional evidence of congenital origin was suggested by Kawashima's") case, in which the configuration of the stenosis was diaphragmatic; there were scattered muscle bundles and no inflammatory infiltrates in the resected tissue. In one of his cases (Case 5), Edwards 11 noted that the elastic configuration of the pulmonary artery was like that of the aorta, which indicated that pulmonary artery hypertension had been present since birth. Definite proof that pulmonary venous stenosis can be congenital was, provided by Becker's" case. Becker described a stillborn fetus with multiple anomalies of the heart,
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including severe stenosis of all pulmonary veins. The involved veins had marked intimal thickening similar to that which has been described in many of the other reported cases. A variant of congenital pulmonary vein obstruction is one in which there is stenosis or atresia of the veins throughout both their intrapulmonary and extrapulmonary courses." We are concerned here with the more frequent localized type in which only the extrapulmonary veins are involved, since this is the only lesion that can at present be approached surgically. Embryology
The foregut lies next to the dorsal aorta in a 3 mm. embryo and passes through the posterior aspect of a mass of mesenchymal cells. Surrounding the foregut is an abundant supply of capillaries, the splanchnic plexus, which has numerous connections with the dorsal aorta. At the 3 mm. stage of the embryo, the lung makes its first appearance as a bud growing outward from the caudal end of the laryngotracheal groove on the ventr \1 surface of the foregut, adjacent to the liver bud. Both buds carry with them a network of capillaries from the splanchnic plexus.!" At the 4 mm. stage, the lung bud divides into two primary bronchi. When the embryo is 7 mm. long, the lobe buds have appeared, two on the left and three on the right. Growth of the lung continues in a ventral and caudal direction; during this process it loses connections with the splanchnic plexus and the aorta. Pulmonary arteries and veins are formed in situ around the developing lung, and only later do the arteries connect with the sixth aortic arch to form the pulmonary arterial circulation.:' By the 3 mm. stage a diverticulum has formed in the future left atrial portion of the sinoatrial region." The diverticulum, or common pulmonary vein," grows toward the developing lungs and ultimately connects with the pulmonary veins, which are already well formed. When this drainage pathway is established, the early connections between the splanchnic plexus and the umbilicovi-
telline (abdominal visceral) and cardinal (somatic) venous systems become of secondary importance and are largely lost. Small connections may persist normally as bronchial venous channels, or major connections may persist abnormally as in total anomalous pulmonary venous connection and various forms of bronchopulmonary sequestration. H As the left atrium grows rapidly, the common pulmonary vein is absorbed into its posterior wall and the pulmonary veins enter the left atrium individually. The veins on one side occasionally form a single channel before entering the atrium. A wide variety of obstructive lesions of the pulmonary venous drainage may occur, depending upon the stage at which normal embryogenesis is interrupted. ' ! If atresia of the common pulmonary vein occurs very early, a major drainage route can be established via either the umbilicovitelline or cardinal venous systems (total anomalous pulmonary venous connection with infra- or supracardiac drainage). If stenosis occurs later, the result may be stenosis of the common pulmonary vein (cor triatriatum with or without anomalous connection to the right atrium). If stenosis occurs very late, after absorption of the common pulmonary vein into the left atrium, the result is stenosis or atresia of individual pulmonary veins. Pathophysiology
The functional pathology of pulmonary venous obstruction-" and of pulmonary edema" has been reviewed recently. Any lesion that elevates the pulmonary venous pressure produces medial hypertrophy in the pulmonary veins. The elevated pressure is transmitted to the pulmonary capillary beds; when hydrostatic pressure exceeds oncotic pressure, fluid leaves the vascular compartment and is removed from the interstitial spaces by pulmonary lymphatics. When the amount of fluid leaving the capillaries exceeds the lung's capacity for lymph flow, pulmonary edema ensues. Four mechanisms are available to compensate for the effects of venous hypertension: (1) increase of pul-
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monary lymphatic flow; (2) development of collateral communications with the bronchial venous system; (3) alteration of pulmonary capillary permeability; and (4) decrease in pulmonary blood flow to areas with venous obstruction, produced by increased arteriolar resistance. This last mechanism may result in increased pressure in the pulmonary artery. Pulmonary artery hypertension can be due to muscular medial hypertrophy of the pulmonary arterioles or, when those anatomic changes are absent, to increased periarterial tissue pressure from local edema or increased arterial tone. Ferencz':' was the first to note that the pulmonary arterial changes are bilateral even when venous stenosis is unilateral. The precise mechanism that mediates this phenomenon is not known.' It has been demonstrated experimentally that distention of only one pulmonary vein produces marked pulmonary arteriolar constriction by reflex reaction, despite the fact that there is no change in pulmonary venous pressure." Ligation of one pulmonary vein results in pulmonary artery hypertension with muscular hypertrophy of small pulmonary arteries in both lungs. These anatomic changes occur within 3 weeks of vein ligation. "', The effect of pulmonary artery hypertension on proximal structures includes dilatation of the entire pulmonary arterial tree, hypertrophy of the pulmonary arterial wall, and hypertrophy of the right ventricle. Right ventricular failure and right atrial enlargement may also occur.
Clinical picture The clinical picture of pulmonary vein obstruction resembles that seen with any lesion which produces pulmonary venous hypertension. Symptoms usually reflect respiratory involvement, such as recurrent respiratory infections, progressive dyspnea, cyanosis, and hemoptysis. About two thirds of these patients have associated malformations of the heart (see Table I); symptoms of associated lesions may predominate. One patient had surgical correction of tetralogy
of Fallot and died postoperatively because of unrecognized pulmonary vein stenosis. n Signs of pulmonary artery hypertension and right ventricular hypertrophy, such as systolic ejection click and loud pulmonary component of the second heart sound, are often present. The electrocardiogram usually shows evidence of right ventricular hypertrophy, sometimes associated with right atrial enlargement, but pulmonary venous stenosis alone does not produce left atrial enlargement or left ventricular hypertrophy. The plain chest film shows a normal or slightly enlarged heart, with increased pulmonary venous markings. Huge tortuous pulmonary veins may be present." The left atrium and ventricle are not enlarged, although the right ventricle and right atrium may be. The main pulmonary artery is prominent. The lung fields may have a finely reticulated vascular pattern; occasionally, there is the appearance of pulmonary edema. Kerley B lines are sometimes present. The possibility of diagnosing this lesion by cardiac catheterization and angiocardiography was suggested by Shone.:" A diagnosis was achieved in 4 of the reported cases" "n,:n as well as in our case. When pulmonary venous obstruction is present, cardiac catheterization should demonstrate pulmonary arterial hypertension, a high pulmonary capillary wedge pressure, and a normal left atrial pressure. Selective angiography of the main pulmonary artery should show no filling or delay of flow from one or more pulmonary veins. It may be possible to visualize the obstructing lesion itself. Selective angiography of the pulmonary veins can demonstrate obstructing lesions." Our patient had both pulmonary artery hypertension and a high pulmonary wedge pressure. Angiocardiography with injection of the main pulmonary artery provided early and distinct visualization of the right inferior pulmonary vein but poor visualization of the others. No evidence of a bichambered left atrium could be seen. I Al}other successfully diagnbsed case, that of Binet,' also involved pulmonary artery
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hypertension with elevated pulmonary capillary wedge pressure. Selective angiography of the two branch pulmonary arteries revealed normal left vasculature; however, on the right there was to-and-fro motion of the contrast material in the right pulmonary artery with reflux into the main pulmonary trunk. Opacification of the small blood vessels gave a "dead tree appearance." The diagnosis was made at catheterization in 2 other patients by recording pressures in each pulmonary vein simultaneously with wedge pressures in corresponding pulmonary arteries. Stenosis at the venoatrial junction was angiographically demonstrated with selective pulmonary vein injections.:" In an unoperated patient," pulmonary artery hypertension was noted but wedge pressures were not measured. Later review of the angiogram distinctly showed focal stenoses in major intrapulmonary branches of both upper veins, as well as severe stenosis of the left lower vein at its junction with the left atrium.
Surgery The possibility of surgical repair of venous stenosis was suggested as early as 1958."" The first successful repair was that of Kawashima, n who reported the case of a 15-year-old boy with a history of repeated respiratory infections during childhood, a heart murmur starting at the age of 5 years, and cyanosis starting at the age of 10 years. The diagnosis at cardiac catheterization was atrial septal defect. At operation, a large atrial septal defect was found, through which a diaphragmatic obstruction of the right upper pulmonary vein was seen. An obstructing localized thickening was also present at the entry of a common left venous trunk into the left atrium. The right upper vein diaphragm was excised and the thickening at the left vein orifice was incised. The atrial septal defect was closed. A large ventricular septal defect was discovered and repaired with a patch. The patient had done well for 2 years after operation at the time of that report, except for one episode of hemoptysis 4 months postoperatively. A late
postoperative lung scan showed slightly diminished flow in the left upper lung but no difference between the right upper and right lower lung fields. The second successful repair, reported by Binet, ii was performed in a 5-year-old child who had a history of repeated hemoptysis and respiratory infections. The findings at cardiac catheterization and angiocardiography have been described above. The diagnosis of stenosis of the right pulmonary veins was made, and the patient was operated upon. The upper and lower pulmonary veins joined to form a common vein which entered the left atrium. Two diaphragmatic obstructions were found, one in each vein immediately before the common vein was formed. The diaphragms were excised and the veins were patched open with a single piece of pericardium. Cardiopulmonary bypass was available but was not necessary. Despite pulmonary complications in the first few postoperative days, the child was doing well 6 months after operation. The 2 patients reported by Park'" underwent patch angioplasty of localized stenoses. One patient, a l-year-old infant, had both right pulmonary veins repaired but died postoperatively. At autopsy, thrombosis at the operative site was found. The second patient had repair of a ventricular septal defect at the age of 21 months; but postoperatively, the child continued to have pulmonary artery hypertension. When he was 12 years old, obstruction of the pulmonary veins was found and was relieved by patch angioplasty. Signs of pulmonary hypertension subsided postoperatively. Our patient is the fifth to have had surgical repair of pulmonary vein stenosis. It is unfortunate that an autopsy could not be obtained. It would be of great interest to know whether the left lower vein was still patent at the time of death. Her death was probably related directly to the fact that the atresia of both upper veins could not be relieved by operation. There is no clear-cut answer to the problem of dealing with uncorrectable obstructive lesions. The three alternative solutions are as follows: (1) to
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leave the involved lung undisturbed; (2) to ligate the pulmonary artery to the involved lung; or (3) to excise all pulmonary tissue with impaired venous drainage. Leaving residual stenosis without other intervention seems unwise for two reasons: First, any severe stenosis or atresia of a pulmonary vein appears to be lethal, since in most reported cases death has occurred during childhood, even when only one or two veins were involved; second, experimental evidence, cited above, suggests that obstruction of only one pulmonary vein is enough to lead to severe bilateral pulmonary vascular obstructive disease. One intervention that might reduce venous hypertension is ligation of the pulmonary arterial inflow. This procedure seemed to offer some protection to the right upper lobe in our patient; in the early postoperative period, she experienced transient severe edema and atelectasis in only the left upper lobe, which had an intact pulmonary artery. However, pulmonary artery ligation does not interrupt the bronchial artery flow, and it is possible that pulmonary venous hypertension could continue despite pulmonary artery ligation. Experimental data suggest that obstruction of both pulmonary arterial and venous supplies results in a high incidence of pulmonary infarction, whether the bronchial arteries are open or ligated." Therefore, we suggest that the procedure offering the best chance for long-term survival is excision of any lobe or lung from which free venous drainage cannot be established.
Occasionally, selective angiography of a pulmonary vein can demonstrate the lesion. The surgical approach to pulmonary vein stenosis must be flexible. The technique of repair will depend upon the local anatomy of each lesion. Those of the diaphragmatic type can be treated effectively by excision of the obstructing membrane. Increase of the vein's caliber can be effectively achieved by patch angioplasty. When segmental stenosis or atresia is present, it may be necessary to anastomose the vein directly to the left atrium. Relief of most types of extrapulmonary venous stenosis and atresia should be possible with currently available techniques. If relief of the obstruction is not possible, undrained pulmonary tissue should be excised whenever technically feasible. We gratefully acknowledge the contribution of Salvatore Treves, M.D., in performing and interpreting the radionuclide angiocardiogram. REFERENCES
2 3
4 5
Summary
Stenosis or atresia of individual pulmonary veins is a rare condition that is usually fatal when untreated, even when only one side is involved. The lesion can be diagnosed at cardiac catheterization by the findings of ( 1) pulmonary artery hypertension, (2) elevated pulmonary capillary wedge pressure, (3) normal left atrial pressure, and (4) angiography of the main pulmonary artery showing either no filling or delay of emptying of one or more pulmonary veins.
6
7
8
9
Andrews, E. C., Jr.: Five Cases of an Undescribed Form of Pulmonary Interstitial Fibrosis Caused by Obstruction of the Pulmonary Veins, Johns Hopkins Med. J. 100: 28, 1957. Auer, J.: The Development of the Human Pulmonary Vein and Its Major Variations, Anat. Rec. 101: 581, 1948. Becker, A. R., Becker, M. J., and Edwards, J. E.: Occlusion of the Pulmonary Veins, "Mitral" Insufficiency, and Ventricular Septal Defect: Functional Resemblance to Ventricular Aneurysm, Am. J. Dis. Child. 120: 557, 1970. Bernstein, J., Nolke, A. C., and Reed, J. 0.: Extrapulmonic Stenosis of the Pulmonary Veins, Circulation 19: 891, 1959. Binet, 1. P., Bouchard, F., Langlois, 1., Cheto· chine, F., Conso, J. F., and Pottemain, M.: Unilateral Congenital Stenosis of the Pulmonary Veins: A Very Rare Cause of Pulmonary Hypertension, 1. THORAc. CARDIOVASC. SURG. 63: 397, 1972. Blesovsky, A.: Pulmonary Sequestration: A Report of an Unusual Case and a Review of the Literature, Thorax 22: 351, 1967. Braun, K., and Stern, S.: Functional Significance of the Pulmonary Venous System, Am. J. Cardio!. 20: 56, 1967. Bremer, J. L.: An Acknowledgment of Federow's Work on ·the Pulmonary Arteries, Anat, Rec. 6: 491, 1912. Contis, G., Fung, R. H., Vawter, G. F., and
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13
14
15
16
17
18
19
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Nadas, A. S.: Stenosis and Obstruction of the Pulmonary Vein Associated With Pulmonary Artery Hypertension, Am. J. Cardio!. 20: 718, 1967. Diamond, I.: The Hamman-Rich Syndrome in Childhood: Report of a Case With Unilateral Pulmonary Arterial and Venous Stenosis and Arteriovenous Occlusion, Pediatrics 22: 279, 1958. Edwards, J. E.: Congenital Stenosis of Pulmonary Veins, Lab. Invest. 9: 46, 1960. Edwards, J. E., and Burchell, H. B.: Multilobar Pulmonary Venous Obstruction With Pulmonary Hypertension: "Protective" Arterial Lesions in the Involved Lobes, Arch. Intern. Med. 87: 372, 1951. Ellis, F. H., Grindlay, J. H., and Edwards, J. E.: The Bronchial Arteries: II. Their Role in Pulmonary Embolism and Infarction, Surgery 31: 167, 1952. Emslie-Smith, D., Hill, I. G. W., and Lowe, K. G.: Unilateral Membranous Pulmonary Venous Occlusion, Pulmonary Hypertension and Patent Ductus Arteriosus, Br. Heart J. 17: 79, 1955. Ferencz, C., and Dammann, J. F., Jr.: Significance of the Pulmonary Vascular Bed in Congenital Heart Disease: V. Lesion of the Left Side of the Heart Causing Obstruction of the Pulmonary Venous Return, Circulation 16: 1046, 1957. Huntington, G. S.: The Morphology of the Pulmonary Artery in the Mammalia, Anat. Rec. 6: 491, 1919. Hyman, A. L., and Sanchez, G.: Alterations in Pulmonary Vasculature and Urine Produced by Acute Distention of a Single Pulmonary Vein in Intact Dogs, Circulation 30: 98, 1964 (Supp!. III). Jue, K. L., Raghib, G., Amplatz, K., Adams, P., Jr., and Edwards, J. E.: Anomalous Origin of the Left Pulmonary Artery From the Right Pulmonary Artery, Am. J. Roentgeno!. Radium Ther. Nuc!. Med. 95: 598, 1965. Kawashima, Y., Ueda, T., Naito, Y, Morikawa, E., and Manabe, H.: Stenosis of Pulmonary Veins: Report of a Patient Surgically Corrected, Ann. Thor. Surg. 12: 196, 1971. Lucas, R. V., Jr.: Congenital Causes of Pulmonary Venous Obstruction, Cardiovasc. Clin. 4: 79, 1972.
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21 Lucas, R. V., Jr., Anderson, R. c., Amplatz, K., Adams, P., Jr., and Edwards, J. E.: Congenital Causes of Pulmonary Venous Obstruction, Pediatr. Clin. North Am. 10: 781, 1963. 22 Lucas, R. V., Jr., Woolfrey, B. P., Anderson, R. C., Lester, R. G., and Edwards, J. E.: Atresia of the Common Pulmonary Veins, Pediatrics 29: 729, 1962. 23 Moller, J. H., Noren, G. R., David, P. R., Amplatz, K., Kanjuh, V. I., and Edwards, J. E.: Congenital Stenosis of the Individual Pulmonary Veins, Am. Heart J. 72: 530, 1966. 24 Nakib, A., Moller, J. H., Kanjuh, V. I., and Edwards, J. E.: Anomalies of the Pulmonary Veins, Am. J. Cardio!. 20: 77, 1967. 25 Narkiewicz, M., Chadzypangiotis, D., Wrzolkowa, T., and Kabasik, A.: Sequelae of Lung Lobar Vein Ligation in Cat, Pol. Med. J. 11: 1252, 1972. 26 Park, S. C., Neches, W. H., Lenox, C. c., Zuberbuhler, J. R., Siewers, R. W., and Bahnson, H. T.: Successful Preoperative Diagnosis and Surgical Repair of Pulmonary Vein Stenosis, Circulation 48: 33, 1973 (Suppl, IV). 27 Reye, R. D. K.: Congenital Stenosis of Pulmonary Veins in Their Extrapulmonary Course, Med. J. Aust. 1: 801, 1951. 28 Robin, E. D., Cross, C. E., and Zelis, R.: Pulmonary Edema (Second of Two Parts) N. Engl. J. Med. 288: 292, 1973. 29 Sherman, F. E., Stengel, W. F., and Bauersfeld, S. R.: Congenital Stenosis of Pulmonary Veins at Their Atrial Junctions, Am. Heart J. 56: 908, 1958. 30 Shone, J. D., Amplatz, K., Anderson, R. c., Adams, P., Jr., and Edwards, J. E.: Congenital Stenosis of Individual Pulmonary Veins, Circulation 26: 574, 1962. 31 Singshinsuk, J., Hartmann, A. F., and Elliott, L. P.: Stenosis of the Individual Pulmonary Veins, Radiology 87: 514, 1966. 32 Snellen, H. A., and Bruins, C.: Anomalies of Venous Return, in Watson, H., editor: Pediatric Cardiology, St. Louis, 1968, The C. V. Mosby Company, pp. 427-428. 33 Wagenvoort, C. A.: Vasoconstrictive Primary Pulmonary Hypertension and Pulmonary Venoocclusive Disease, Cardiovasc. Clin. 4: 97, 1972.
0/ the
literature and report 0/ a surgical case
Stenosis or atresia of the individual pulmonary veins is a rare condition that is usually fatal when untreated, even when only one side is involved. The lesion can be diagnosed at cardiac catheterization by pressure and angiographic data. The surgical approach to pulmonary vein stenosis must be flexible. The technique of repair will depend upon the local anatomy of each lesion. Those of the diaphragmatic type can be treated effectively by excision of the obstructing membrane. Increase of the vein's caliber can be achieved by patch angioplasty . When segmental stenosis or atresia is present, it may be necessary to anastomose the vein directly to the left atrium. Relief of most types of extrapulmonary venous stenosis and atresia should be possible with currently available techniques. If relief of the obstruction is not possible, undrained pulmonary tissue should be excised whenever technically feasible.
Robert M. Sade, M.D., Michael D. Freed, M.D., Edward C. Matthews, M.D., and Aldo R. Castaneda, M.D., Boston, Mass., and Portland, Maine
Stenosis or atresia of the pulmonary veins without anomalous connection is a rare cause of pulmonary artery hypertension. Of the twenty-three cases that have been reported, four have been corrected surgically,"- 19, 2(; and three of them were correctly diagnosed preoperatively.": 2(; This report describes a patient with pulmonary vein atresia whose lesion was diagnosed at cardiac catheterization and then partially corrected at operation. Case report O. E. (CHMC No. 77-75-18) was admitted to CHMC on Dec. 20, 1972, at the age of 8 months. At the age of 5 months she had been admitted to Maine Medical Center with a history of repeated pulmonary infections and failure to thrive. At that time work-up was negative with
From the Departments of Cardiovascular Surgery and Cardiology, The Children's Hospital Medical Center and Harvard Medical School, Boston, Mass. 02115, and the Maine Medical Center, Portland, Maine 04102. Received for publication Jan. 28, 1974. Address for reprints: Robert M. Sade, M.D., Department of Cardiovascular Surgery, Children's Hospital Medical Center, 300 Longwood Ave., Boston, Mass. 02115.
the exception of mild tachypnea and mild cardiomegaly on x-ray study. The electrocardiogram was normal. Because she was thought to be in mild congestive heart failure she was treated with digitalis but without improvement. Over the next 3 months she continued to have respiratory difficulties, manifested by rapid, labored breathing without fever. On readmission to Maine Medical Center at 8 months of age, she was a small, thin infant in moderate respiratory distress. A Grade 2/6 systolic murmur was audible along the left sternal border. The pulmonic second sound was normally split and mildly accentuated. An electrocardiogram showed mild right ventricular hypertrophy, and a chest x-ray film disclosed mild cardiomegaly and increased pulmonary blood flow. Cardiac catheterization was performed. There was no evidence of an intracardiac shunt. The pulmonary artery pressure was mildly elevated (50/17 mm. Hg, mean 30 rnrn. Hg), as were wedge pressures in the right and left upper pulmonary arteries (mean 22 mm. Hg). The left atrium and ventricle were not entered. Anteroposterior and lateral cineangiograms were performed by injection of contrast medium into the main pulmonary artery. There was prompt opacification of a dilated right lower pulmonary artery. The left pulmonary arteries an~ right upper and middle pulmonary arteries were quite small, less than one third the size of the right lower pul-
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A.
Upper P.V.
B.
Lt. Atria and Lower P. V. Incised
Lower P. V.
Fig. 1. A, The atretic left upper and lower pulmonary veins (P.v.) and the right upper pulmonary vein are depicted with the corresponding hypoplastic pulmonary arteries (P.A .). B, The narrowed segment of the left lower vein was opened and atresia was found; the vein was ligated and opened proximally. Then an opening was created in the adjacent left atrium. C and D, A side-to-side anastomosis of vein to left atrium was carried out.
monary artery. During the levophase, the right lower pulmonary vein drained normally into the left atrium. The other pulmonary veins were poorly visualized. The left atrium was of normal size, and the atrial appendage was in its usual position. The left ventricle was of normal size and filled promptly from the left atrium. On the basis of elevated wedge pressures, pulmonary artery hypertension, and the cineangiograms, the physicians believed that the child had obstruction to pulmonary venous return of the right upper, left upper, and left lower veins. They could not determine whether this was due to partial cor triatriatum or to obstruction of the individual pulmonary veins. Because of recurrent episodes of labored, gasping respirations associated with cyanosis, thought to be due to acute pulmonary edema, the child was transferred to Children's Hospital Medical Center for surgical intervention.
Findings on admission were unchanged. An echocardiogram disclosed a normal-sized left atrium and left ventricle and a mobile mitral valve. On Dec. 22, 1972, the patient was taken to the operating room. With the child under deep hypothermia and circulatory arrest, the left atrium was opened. The four pulmonary vein orifices were normally placed, but upper vein openings were atretic, represented by a dimple in the posterior left atrial wall. The heart was retracted anteriorly, and the left lower pulmonary vein was found to be dilated proximal to its junction with the left atrium. Incision of the vessel revealed an atretic segment about 5 mm. long immediately proximal to its junction with the left atrium. A small incision was made in the left atrium just above the inferior vein orifice, and a side-to-side anastomosis of the proximal pulmonary vein to the left atrium was carried out (Fig. I). Explora-
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Fig. 2. Radionuclide angiocardiography after injection of 991lltechnicium as sodium pertechnetate into the inferior vena cava . 1, One second after inferior vena caval injection, radionuclide has appeared in the right atrium and ventricle a nd is beginning to appear in the pulmonary artery. 2, The pulmonary artery is now clearly seen, with good visualization of the right pulmonary artery and right lower lung field; there is slight visualization of the left lower lung field. 3, Radionuclide is heavily concentrated in right lower lung field, moderately so in the left lower lung field, and is .barely detectable in the upper lung fields. 4, Returning radionuclide fills the left heart and the ascending aorta. 5, The descending aorta is now apparent , with early filling of abdom inal viscera; the upper lung fields are filling mostly from bronchial flow, especially on the right. 6, Emptying of the left heart and aorta into the systemic circulation is seen. tion of the left superior pulmonary vein revealed an atretic cord extending into the pulmonary parenchyma. Exploration of the right superior pulmona ry vein revealed severe stenosi s of the vein at its emergence from the pulmonary parenchyma, as well as a segment of complete atresia about I ern, long near the atrium. The right lower pulmonary vein was inspected and found to be normal in caliber. The right upper lobe artery was ligated. Cardiopulmonary bypass was reinstituted and the patient rewarmed. Postoperatively, the patient required intensive pulmonary care and remained intubated until the fourth postoperative day . On the second day after extubation a chest x-ray film showed edema and atelectasis of the left upper lobe. The patient was treated aggre ssively with diuretic and pulmonary therapy, and the lung was completely clear 2 day s later. Throughout the postoperative per iod chest films showed a vascular pattern of pulmonary venous congestion in both the left upper and left lower lobe areas. Pulmon ary blood flow was clearly increased to the right lower lobe. At the time of discharge the right lower lobe was somewhat increased in volume and the right upper lobe somewhat diminished in volume. uHIllT ech netium pulmonary scan showed absence of flow to the right upper lung field, severe reduction of flow to the
left upper lung field, and moderate reduction of flow to the left lower lung field. The right lower lung field received a major portion of the pulmonary blood flow ( Fig. 2) . The patient was discharged on the eighteenth postoperative day. Her only medication was digoxin. The child returned to the remote community in which she lived . About 1 month after discharge she was admitted to a local hospital with pneumonia and congestive heart failure . She was treated with diuretics and digitalis. After initial improvement she apparently developed an influenza-like illness and died within a few days. No autopsy was obtained.
Discussion
There have been 23 case reports of localized pulmonary vein stenosis; ours is the twenty-fourth. The age range of these patients has been from the neonatal period to 15 years, but most were under the age of 6 years. Other data i are summarized in Table 1. ' In 7 cases, all four veins were obstructed. In 11 cases, obstruction was unilateral, and in 2 of them , only one vein was obstructed.
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Table I Author (date) Reye (1951) Emslie-Smith et al. 1 4 (1955) Ferencz and Dammann!" (1957) Andrews! (1957) Sherman et al. 2 9 (1958) 27
Patient's age
I
I
Veins involved
8 yr. 13 yr. 2 yr. 3 yr. 8\12 mo.
RUY, RLY, LUY, and LLY RUY and RLY LUY and LLY LUY and LLY RUY, RLY, and LLY
6 yr.
RUY, RLY, LUY, and LLY
1 yr.
Symptoms Congestive heart failure Cyanosis Cyanosis; dyspnea; failure to thrive Recurrent respiratory infections; failure to thrive Hemoptysis
Bernstein et al.! (1959) Edwards"! (1960) Case 5 Case 6 Case 7 Shone et al. 3 0 (1962) Lucas et al. 2 1 (1963) Jue et al.!S (1965) Singshinsuk et al. 3 1 (1966) MoHer et al. 2 :J (1966) Contis et al.v (1967)
1Y2 yr. 10 yr. 7 mo. 6 yr. 8 wk. 6 yr. 6 mo. 12 yr.
RUY, LCY RCY RUY, RUY, LUY RUY, RUY, RUY,
l\;lakib et al. 24 (1967)
6 wk.
LLY
Nakib et al. 2 4 (1967) Snellen and Bruins"> (1968) Becker et al." (1970)
2 yr. 13 yr. Stillborn
LCY RCY RUY, RLY, LUY, and LLY
None related to vein obstruction Cyanosis
Kawashima et al.l!' (1971)
15 yr.
RUY and LCY
Binet et al.a (1972) Park et al. 2 r> (1973) Park et al. 2<> (1973) Sade et al. (1974)
5 yr. 1 yr. 12 yr. 10 mo.
RUY RUY RUY, RUY,
Cyanosis; frequent respiratory infections Hemoptysis; recurrent cough
RLY, LUY, and LLY
RLY, LUY, and LLY RLY, LUY, and LLY LUY, and LLY RLY, and LLY LUY, and LL Y
and RLY and RLY RLY, LUY, and LLY LUY, and LLY
Cyanosis; failure to thrive Cyanosis and cyanotic spells Recurrent respiratory distress None Congestive heart failure; recurrent pneumonia
Recurrent respiratory infections
Legend: RUV, Right upper vein. RLV, Right lower vein. ReV, Right common vein. LUV, Left upper vein. LLV, Left lower vein, Ventricular septal defect. A-V, Atrioventricular. PFO. Patent foramen ovale.
In 6 cases, including the present one, all veins but one were stenotic or atretic. The anatomy of the obstruction is variable. There are a number of possibilities: a complete diaphragm at the venoatrial junction or in the vein proximal to the atrium; a partially obstructing diaphragm; a stenotic localized segment of vein; or atresia of the entire extra pulmonary vessel. Many individual patients have had different types of obstructions in different veins. Further obstruction of a stenotic vein may be produced by local thrombus." " Histologically, thickening of the intima by avascular cellular fibrous tissue often is the cause of obstruction 11; in some cases the vein is reduced to a fibrotic atretic cord. t
An obstructing diaphragm may contain scattered muscle bundles surrounded by connective tissue, in addition to intimal fibrosis." Usually, no inflammatory cells are present. In 14 cases from this group of patients, other cardiac anomalies were associated. These are summarized in Table I. Etiology
Pulmonary venous obstruction can be congenital or acquired. In acquired disease, the interior of the pulmonary veins may be obstructed by left atrial mural thrombus, myxoma," or pulmonary veno-occlusive disease'"'; on the other hand, the veins may be compressed extrinsically by neoplasms,
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Associated cardiac lesions
Surgery
Outcome
None PDA None Tricuspid atresia; TGA None
Death Death Death Death Death
None
Death
Small ASD Mitral atresia; ASD; VSD Persistent common A-V canal Large ASD Tetralogy of Fallot Pulmonary artery sling None ASD None
Death Death Death Death Postop, death Postop. death Alive and asymptomatic Death Death
Atresia of aortic and mitral valves; coarctation of aorta Coarctation of aorta with hypoplastic arch VSD Corrected TGA; Ebstein-like left A-V valve; muscular VSD; premature closure of PFO ASD; VSD None VSD None
Repai r of tetralogy of Fallot Exploratory right thoracotomy
Death Repair of VSD
Death Not stated Death
Relief of RUV and LeV stenoses
Alive 2 yr. postop.
Relief Patch Patch Relief
Alive 6 mo. postop, Postop. death Alive Postop. death
of RUV and RLV stenoses angioplasty of both involved veins angioplasty of all veins (age 12 yr.) of LLV stenosis only
_CV, Left common vein. PDA, Patent ductus arteriosus. TGA, Transposition of the great arteries. ASD, Atrial septal defect. VSD,
mediastinal fibrous masses,'> or by fibrosis resulting from chronic pulmonary infections.") It is occasionally difficult to determine whether specific stenoses are congenital or acquired since evidence may be adduced to support both possibilities in an individual case:' However, most cases of pulmonary venous stenosis and atresia are probably congenital. The evidence for this was summarized by Shone": (1) Clinical evidence of the lesion usually begins at a young age; (2) other congenital anomalies are frequently associated; (3) there is usually little or no evidence of active inflammation; and (4) the obstructive lesion occurring in normally connecting veins is similar to that seen in
veins connecting with structures other than the left atrium. Additional evidence of congenital origin was suggested by Kawashima's") case, in which the configuration of the stenosis was diaphragmatic; there were scattered muscle bundles and no inflammatory infiltrates in the resected tissue. In one of his cases (Case 5), Edwards 11 noted that the elastic configuration of the pulmonary artery was like that of the aorta, which indicated that pulmonary artery hypertension had been present since birth. Definite proof that pulmonary venous stenosis can be congenital was, provided by Becker's" case. Becker described a stillborn fetus with multiple anomalies of the heart,
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including severe stenosis of all pulmonary veins. The involved veins had marked intimal thickening similar to that which has been described in many of the other reported cases. A variant of congenital pulmonary vein obstruction is one in which there is stenosis or atresia of the veins throughout both their intrapulmonary and extrapulmonary courses." We are concerned here with the more frequent localized type in which only the extrapulmonary veins are involved, since this is the only lesion that can at present be approached surgically. Embryology
The foregut lies next to the dorsal aorta in a 3 mm. embryo and passes through the posterior aspect of a mass of mesenchymal cells. Surrounding the foregut is an abundant supply of capillaries, the splanchnic plexus, which has numerous connections with the dorsal aorta. At the 3 mm. stage of the embryo, the lung makes its first appearance as a bud growing outward from the caudal end of the laryngotracheal groove on the ventr \1 surface of the foregut, adjacent to the liver bud. Both buds carry with them a network of capillaries from the splanchnic plexus.!" At the 4 mm. stage, the lung bud divides into two primary bronchi. When the embryo is 7 mm. long, the lobe buds have appeared, two on the left and three on the right. Growth of the lung continues in a ventral and caudal direction; during this process it loses connections with the splanchnic plexus and the aorta. Pulmonary arteries and veins are formed in situ around the developing lung, and only later do the arteries connect with the sixth aortic arch to form the pulmonary arterial circulation.:' By the 3 mm. stage a diverticulum has formed in the future left atrial portion of the sinoatrial region." The diverticulum, or common pulmonary vein," grows toward the developing lungs and ultimately connects with the pulmonary veins, which are already well formed. When this drainage pathway is established, the early connections between the splanchnic plexus and the umbilicovi-
telline (abdominal visceral) and cardinal (somatic) venous systems become of secondary importance and are largely lost. Small connections may persist normally as bronchial venous channels, or major connections may persist abnormally as in total anomalous pulmonary venous connection and various forms of bronchopulmonary sequestration. H As the left atrium grows rapidly, the common pulmonary vein is absorbed into its posterior wall and the pulmonary veins enter the left atrium individually. The veins on one side occasionally form a single channel before entering the atrium. A wide variety of obstructive lesions of the pulmonary venous drainage may occur, depending upon the stage at which normal embryogenesis is interrupted. ' ! If atresia of the common pulmonary vein occurs very early, a major drainage route can be established via either the umbilicovitelline or cardinal venous systems (total anomalous pulmonary venous connection with infra- or supracardiac drainage). If stenosis occurs later, the result may be stenosis of the common pulmonary vein (cor triatriatum with or without anomalous connection to the right atrium). If stenosis occurs very late, after absorption of the common pulmonary vein into the left atrium, the result is stenosis or atresia of individual pulmonary veins. Pathophysiology
The functional pathology of pulmonary venous obstruction-" and of pulmonary edema" has been reviewed recently. Any lesion that elevates the pulmonary venous pressure produces medial hypertrophy in the pulmonary veins. The elevated pressure is transmitted to the pulmonary capillary beds; when hydrostatic pressure exceeds oncotic pressure, fluid leaves the vascular compartment and is removed from the interstitial spaces by pulmonary lymphatics. When the amount of fluid leaving the capillaries exceeds the lung's capacity for lymph flow, pulmonary edema ensues. Four mechanisms are available to compensate for the effects of venous hypertension: (1) increase of pul-
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monary lymphatic flow; (2) development of collateral communications with the bronchial venous system; (3) alteration of pulmonary capillary permeability; and (4) decrease in pulmonary blood flow to areas with venous obstruction, produced by increased arteriolar resistance. This last mechanism may result in increased pressure in the pulmonary artery. Pulmonary artery hypertension can be due to muscular medial hypertrophy of the pulmonary arterioles or, when those anatomic changes are absent, to increased periarterial tissue pressure from local edema or increased arterial tone. Ferencz':' was the first to note that the pulmonary arterial changes are bilateral even when venous stenosis is unilateral. The precise mechanism that mediates this phenomenon is not known.' It has been demonstrated experimentally that distention of only one pulmonary vein produces marked pulmonary arteriolar constriction by reflex reaction, despite the fact that there is no change in pulmonary venous pressure." Ligation of one pulmonary vein results in pulmonary artery hypertension with muscular hypertrophy of small pulmonary arteries in both lungs. These anatomic changes occur within 3 weeks of vein ligation. "', The effect of pulmonary artery hypertension on proximal structures includes dilatation of the entire pulmonary arterial tree, hypertrophy of the pulmonary arterial wall, and hypertrophy of the right ventricle. Right ventricular failure and right atrial enlargement may also occur.
Clinical picture The clinical picture of pulmonary vein obstruction resembles that seen with any lesion which produces pulmonary venous hypertension. Symptoms usually reflect respiratory involvement, such as recurrent respiratory infections, progressive dyspnea, cyanosis, and hemoptysis. About two thirds of these patients have associated malformations of the heart (see Table I); symptoms of associated lesions may predominate. One patient had surgical correction of tetralogy
of Fallot and died postoperatively because of unrecognized pulmonary vein stenosis. n Signs of pulmonary artery hypertension and right ventricular hypertrophy, such as systolic ejection click and loud pulmonary component of the second heart sound, are often present. The electrocardiogram usually shows evidence of right ventricular hypertrophy, sometimes associated with right atrial enlargement, but pulmonary venous stenosis alone does not produce left atrial enlargement or left ventricular hypertrophy. The plain chest film shows a normal or slightly enlarged heart, with increased pulmonary venous markings. Huge tortuous pulmonary veins may be present." The left atrium and ventricle are not enlarged, although the right ventricle and right atrium may be. The main pulmonary artery is prominent. The lung fields may have a finely reticulated vascular pattern; occasionally, there is the appearance of pulmonary edema. Kerley B lines are sometimes present. The possibility of diagnosing this lesion by cardiac catheterization and angiocardiography was suggested by Shone.:" A diagnosis was achieved in 4 of the reported cases" "n,:n as well as in our case. When pulmonary venous obstruction is present, cardiac catheterization should demonstrate pulmonary arterial hypertension, a high pulmonary capillary wedge pressure, and a normal left atrial pressure. Selective angiography of the main pulmonary artery should show no filling or delay of flow from one or more pulmonary veins. It may be possible to visualize the obstructing lesion itself. Selective angiography of the pulmonary veins can demonstrate obstructing lesions." Our patient had both pulmonary artery hypertension and a high pulmonary wedge pressure. Angiocardiography with injection of the main pulmonary artery provided early and distinct visualization of the right inferior pulmonary vein but poor visualization of the others. No evidence of a bichambered left atrium could be seen. I Al}other successfully diagnbsed case, that of Binet,' also involved pulmonary artery
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hypertension with elevated pulmonary capillary wedge pressure. Selective angiography of the two branch pulmonary arteries revealed normal left vasculature; however, on the right there was to-and-fro motion of the contrast material in the right pulmonary artery with reflux into the main pulmonary trunk. Opacification of the small blood vessels gave a "dead tree appearance." The diagnosis was made at catheterization in 2 other patients by recording pressures in each pulmonary vein simultaneously with wedge pressures in corresponding pulmonary arteries. Stenosis at the venoatrial junction was angiographically demonstrated with selective pulmonary vein injections.:" In an unoperated patient," pulmonary artery hypertension was noted but wedge pressures were not measured. Later review of the angiogram distinctly showed focal stenoses in major intrapulmonary branches of both upper veins, as well as severe stenosis of the left lower vein at its junction with the left atrium.
Surgery The possibility of surgical repair of venous stenosis was suggested as early as 1958."" The first successful repair was that of Kawashima, n who reported the case of a 15-year-old boy with a history of repeated respiratory infections during childhood, a heart murmur starting at the age of 5 years, and cyanosis starting at the age of 10 years. The diagnosis at cardiac catheterization was atrial septal defect. At operation, a large atrial septal defect was found, through which a diaphragmatic obstruction of the right upper pulmonary vein was seen. An obstructing localized thickening was also present at the entry of a common left venous trunk into the left atrium. The right upper vein diaphragm was excised and the thickening at the left vein orifice was incised. The atrial septal defect was closed. A large ventricular septal defect was discovered and repaired with a patch. The patient had done well for 2 years after operation at the time of that report, except for one episode of hemoptysis 4 months postoperatively. A late
postoperative lung scan showed slightly diminished flow in the left upper lung but no difference between the right upper and right lower lung fields. The second successful repair, reported by Binet, ii was performed in a 5-year-old child who had a history of repeated hemoptysis and respiratory infections. The findings at cardiac catheterization and angiocardiography have been described above. The diagnosis of stenosis of the right pulmonary veins was made, and the patient was operated upon. The upper and lower pulmonary veins joined to form a common vein which entered the left atrium. Two diaphragmatic obstructions were found, one in each vein immediately before the common vein was formed. The diaphragms were excised and the veins were patched open with a single piece of pericardium. Cardiopulmonary bypass was available but was not necessary. Despite pulmonary complications in the first few postoperative days, the child was doing well 6 months after operation. The 2 patients reported by Park'" underwent patch angioplasty of localized stenoses. One patient, a l-year-old infant, had both right pulmonary veins repaired but died postoperatively. At autopsy, thrombosis at the operative site was found. The second patient had repair of a ventricular septal defect at the age of 21 months; but postoperatively, the child continued to have pulmonary artery hypertension. When he was 12 years old, obstruction of the pulmonary veins was found and was relieved by patch angioplasty. Signs of pulmonary hypertension subsided postoperatively. Our patient is the fifth to have had surgical repair of pulmonary vein stenosis. It is unfortunate that an autopsy could not be obtained. It would be of great interest to know whether the left lower vein was still patent at the time of death. Her death was probably related directly to the fact that the atresia of both upper veins could not be relieved by operation. There is no clear-cut answer to the problem of dealing with uncorrectable obstructive lesions. The three alternative solutions are as follows: (1) to
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leave the involved lung undisturbed; (2) to ligate the pulmonary artery to the involved lung; or (3) to excise all pulmonary tissue with impaired venous drainage. Leaving residual stenosis without other intervention seems unwise for two reasons: First, any severe stenosis or atresia of a pulmonary vein appears to be lethal, since in most reported cases death has occurred during childhood, even when only one or two veins were involved; second, experimental evidence, cited above, suggests that obstruction of only one pulmonary vein is enough to lead to severe bilateral pulmonary vascular obstructive disease. One intervention that might reduce venous hypertension is ligation of the pulmonary arterial inflow. This procedure seemed to offer some protection to the right upper lobe in our patient; in the early postoperative period, she experienced transient severe edema and atelectasis in only the left upper lobe, which had an intact pulmonary artery. However, pulmonary artery ligation does not interrupt the bronchial artery flow, and it is possible that pulmonary venous hypertension could continue despite pulmonary artery ligation. Experimental data suggest that obstruction of both pulmonary arterial and venous supplies results in a high incidence of pulmonary infarction, whether the bronchial arteries are open or ligated." Therefore, we suggest that the procedure offering the best chance for long-term survival is excision of any lobe or lung from which free venous drainage cannot be established.
Occasionally, selective angiography of a pulmonary vein can demonstrate the lesion. The surgical approach to pulmonary vein stenosis must be flexible. The technique of repair will depend upon the local anatomy of each lesion. Those of the diaphragmatic type can be treated effectively by excision of the obstructing membrane. Increase of the vein's caliber can be effectively achieved by patch angioplasty. When segmental stenosis or atresia is present, it may be necessary to anastomose the vein directly to the left atrium. Relief of most types of extrapulmonary venous stenosis and atresia should be possible with currently available techniques. If relief of the obstruction is not possible, undrained pulmonary tissue should be excised whenever technically feasible. We gratefully acknowledge the contribution of Salvatore Treves, M.D., in performing and interpreting the radionuclide angiocardiogram. REFERENCES
2 3
4 5
Summary
Stenosis or atresia of individual pulmonary veins is a rare condition that is usually fatal when untreated, even when only one side is involved. The lesion can be diagnosed at cardiac catheterization by the findings of ( 1) pulmonary artery hypertension, (2) elevated pulmonary capillary wedge pressure, (3) normal left atrial pressure, and (4) angiography of the main pulmonary artery showing either no filling or delay of emptying of one or more pulmonary veins.
6
7
8
9
Andrews, E. C., Jr.: Five Cases of an Undescribed Form of Pulmonary Interstitial Fibrosis Caused by Obstruction of the Pulmonary Veins, Johns Hopkins Med. J. 100: 28, 1957. Auer, J.: The Development of the Human Pulmonary Vein and Its Major Variations, Anat. Rec. 101: 581, 1948. Becker, A. R., Becker, M. J., and Edwards, J. E.: Occlusion of the Pulmonary Veins, "Mitral" Insufficiency, and Ventricular Septal Defect: Functional Resemblance to Ventricular Aneurysm, Am. J. Dis. Child. 120: 557, 1970. Bernstein, J., Nolke, A. C., and Reed, J. 0.: Extrapulmonic Stenosis of the Pulmonary Veins, Circulation 19: 891, 1959. Binet, 1. P., Bouchard, F., Langlois, 1., Cheto· chine, F., Conso, J. F., and Pottemain, M.: Unilateral Congenital Stenosis of the Pulmonary Veins: A Very Rare Cause of Pulmonary Hypertension, 1. THORAc. CARDIOVASC. SURG. 63: 397, 1972. Blesovsky, A.: Pulmonary Sequestration: A Report of an Unusual Case and a Review of the Literature, Thorax 22: 351, 1967. Braun, K., and Stern, S.: Functional Significance of the Pulmonary Venous System, Am. J. Cardio!. 20: 56, 1967. Bremer, J. L.: An Acknowledgment of Federow's Work on ·the Pulmonary Arteries, Anat, Rec. 6: 491, 1912. Contis, G., Fung, R. H., Vawter, G. F., and
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13
14
15
16
17
18
19
20
Sade et al.
Nadas, A. S.: Stenosis and Obstruction of the Pulmonary Vein Associated With Pulmonary Artery Hypertension, Am. J. Cardio!. 20: 718, 1967. Diamond, I.: The Hamman-Rich Syndrome in Childhood: Report of a Case With Unilateral Pulmonary Arterial and Venous Stenosis and Arteriovenous Occlusion, Pediatrics 22: 279, 1958. Edwards, J. E.: Congenital Stenosis of Pulmonary Veins, Lab. Invest. 9: 46, 1960. Edwards, J. E., and Burchell, H. B.: Multilobar Pulmonary Venous Obstruction With Pulmonary Hypertension: "Protective" Arterial Lesions in the Involved Lobes, Arch. Intern. Med. 87: 372, 1951. Ellis, F. H., Grindlay, J. H., and Edwards, J. E.: The Bronchial Arteries: II. Their Role in Pulmonary Embolism and Infarction, Surgery 31: 167, 1952. Emslie-Smith, D., Hill, I. G. W., and Lowe, K. G.: Unilateral Membranous Pulmonary Venous Occlusion, Pulmonary Hypertension and Patent Ductus Arteriosus, Br. Heart J. 17: 79, 1955. Ferencz, C., and Dammann, J. F., Jr.: Significance of the Pulmonary Vascular Bed in Congenital Heart Disease: V. Lesion of the Left Side of the Heart Causing Obstruction of the Pulmonary Venous Return, Circulation 16: 1046, 1957. Huntington, G. S.: The Morphology of the Pulmonary Artery in the Mammalia, Anat. Rec. 6: 491, 1919. Hyman, A. L., and Sanchez, G.: Alterations in Pulmonary Vasculature and Urine Produced by Acute Distention of a Single Pulmonary Vein in Intact Dogs, Circulation 30: 98, 1964 (Supp!. III). Jue, K. L., Raghib, G., Amplatz, K., Adams, P., Jr., and Edwards, J. E.: Anomalous Origin of the Left Pulmonary Artery From the Right Pulmonary Artery, Am. J. Roentgeno!. Radium Ther. Nuc!. Med. 95: 598, 1965. Kawashima, Y., Ueda, T., Naito, Y, Morikawa, E., and Manabe, H.: Stenosis of Pulmonary Veins: Report of a Patient Surgically Corrected, Ann. Thor. Surg. 12: 196, 1971. Lucas, R. V., Jr.: Congenital Causes of Pulmonary Venous Obstruction, Cardiovasc. Clin. 4: 79, 1972.
The Journal of Thoracic and Cardiovascular Surgery
21 Lucas, R. V., Jr., Anderson, R. c., Amplatz, K., Adams, P., Jr., and Edwards, J. E.: Congenital Causes of Pulmonary Venous Obstruction, Pediatr. Clin. North Am. 10: 781, 1963. 22 Lucas, R. V., Jr., Woolfrey, B. P., Anderson, R. C., Lester, R. G., and Edwards, J. E.: Atresia of the Common Pulmonary Veins, Pediatrics 29: 729, 1962. 23 Moller, J. H., Noren, G. R., David, P. R., Amplatz, K., Kanjuh, V. I., and Edwards, J. E.: Congenital Stenosis of the Individual Pulmonary Veins, Am. Heart J. 72: 530, 1966. 24 Nakib, A., Moller, J. H., Kanjuh, V. I., and Edwards, J. E.: Anomalies of the Pulmonary Veins, Am. J. Cardio!. 20: 77, 1967. 25 Narkiewicz, M., Chadzypangiotis, D., Wrzolkowa, T., and Kabasik, A.: Sequelae of Lung Lobar Vein Ligation in Cat, Pol. Med. J. 11: 1252, 1972. 26 Park, S. C., Neches, W. H., Lenox, C. c., Zuberbuhler, J. R., Siewers, R. W., and Bahnson, H. T.: Successful Preoperative Diagnosis and Surgical Repair of Pulmonary Vein Stenosis, Circulation 48: 33, 1973 (Suppl, IV). 27 Reye, R. D. K.: Congenital Stenosis of Pulmonary Veins in Their Extrapulmonary Course, Med. J. Aust. 1: 801, 1951. 28 Robin, E. D., Cross, C. E., and Zelis, R.: Pulmonary Edema (Second of Two Parts) N. Engl. J. Med. 288: 292, 1973. 29 Sherman, F. E., Stengel, W. F., and Bauersfeld, S. R.: Congenital Stenosis of Pulmonary Veins at Their Atrial Junctions, Am. Heart J. 56: 908, 1958. 30 Shone, J. D., Amplatz, K., Anderson, R. c., Adams, P., Jr., and Edwards, J. E.: Congenital Stenosis of Individual Pulmonary Veins, Circulation 26: 574, 1962. 31 Singshinsuk, J., Hartmann, A. F., and Elliott, L. P.: Stenosis of the Individual Pulmonary Veins, Radiology 87: 514, 1966. 32 Snellen, H. A., and Bruins, C.: Anomalies of Venous Return, in Watson, H., editor: Pediatric Cardiology, St. Louis, 1968, The C. V. Mosby Company, pp. 427-428. 33 Wagenvoort, C. A.: Vasoconstrictive Primary Pulmonary Hypertension and Pulmonary Venoocclusive Disease, Cardiovasc. Clin. 4: 97, 1972.