Systemic Collateral and Pulmonary Artery Stenosis in Patients with Congenital Pulmonary Valve Atresia and Ventricular Septal Defect MICHAEL D. MCGOON, RICHARD E. FULTON, M.D., GEORGE D. DAVIS, M.D., DONALD G. RITTER, M.D., CATHERINE A. NEILL, M.D., AND ROBERT I. WHITE, JR., M.D. SUMMARY Angiograms of 30 patients with congenital pulmonary valve atresia, ventricular septal defect, and large systemicpulmonary collateral arteries (SPCAs) were evaluated. All had aortography, 28 had SPCA arteriography, and 26 had right ventriculography. Seventeen (65%) of 26 patients had a right ventricular infundibulum, 23 (77%) had a pulmonary artery confluence, and five of the nine patients without a right ventricular infundibulum had a confluence. Sixty-six SPCAs of aortic origin were seen; 28 (42%) had
narrowing and 21 patients (70%) had one or more narrowed SPCAs. Five patients had collaterals from internal mammary, subclavian or innominate arteries. Fourteen (47%) had hilar pulmonary artery stenosis. Of these 14 patients mild peripheral stenosis was demonstrated in five. Right aortic arch was present in 15 patients (50%). Complete angiographic delineation of pulmonary vasculature is an essential procedure for preoperative detection of pulmonary and SPCA stenoses in these patients.
CONGENITAL PULMONARY VALVE ATRESIA with ventricular septal defect (VSD) associated with hypoplasia or absence of the main pulmonary artery has been referred to generally as severe tetralogy of Fallot, pseudotruncus arteriosus' or, if no hilar pulmonary arteries are seen, type IV truncus arteriosus.2 We prefer not to use these terms synonomously as some forms of pulmonary valve atresia with VSD have become increasingly amenable to correction by newer surgical techniques. Until recently, it was difficult to make the distinction between truncus type IV, an inoperable anomaly, and other forms of pulmonary valve atresia with VSD. Since it is now imperative that this distinction be made, a thorough angiographic examination of the aorta and systemic collateral circulation to the lung is essential for diagnosis and for determining operability and surgical approach. With the development and increasing application of surgical techniques in the management of patients with pulmonary artery discontinuity,3-7 attention has been directed to the importance of selective catheterization as a means of obtaining maximal radiographic information for determining correctability of the lesion.8 10 Concise detailed understanding of the pulmonary vasculature in this congenital problem has become a vital prerequisite to optimal management. Diagnostic evaluation of these patients has revealed a high incidence of central and peripheral pulmonary artery stenosis not fully documented previously. Recognizing the importance of characterizing all systemic collateral and pulmonary arteries in these patients, we have retrospectively analyzed the angiograms of 30 patients in a combined series
from The Johns Hopkins Hospital and The Mayo Clinic in an effort to evaluate primarily the presence, degree and location of stenosis and/or hypoplasia of the systemic collateral arteries to the lungs and the pulmonary arteries.
From the Division of Cardiovascular Radiology, Department of Radiology and Radiological Sciences, and the Division of Pediatric Cardiology, Department of Pediatrics, The Johns Hopkins Medical Institutions, Baltimore, Maryland; and the Division of Cardiovascular Radiology, Department of Radiology, and the Division of Pediatric Cardiology, Department of Pediatrics, The Mayo Clinic, Rochester, Minnesota. Supported in part by USPHS Training Grant No. 5 TOI HL05970-04 from the National Heart and Lung Institute, Bethesda, Maryland. Mr. McGoon is a Henry Strong Denison Scholar, 1976-77. Address for reprints: Robert I. White, Jr., M.D., Department of Radiology, Johns Hopkins Hospital, Baltimore, Maryland 21205. Received March 11, 1977; revision accepted April 25, 1977.
Materials and Methods Specifically excluded in this review were those patients with congenital pulmonary valve atresia and hypoplastic right ventricle, congenital pulmonary valve atresia with pulmonary blood flow arising entirely from a patent ductus arteriosus, acquired pulmonary valve atresia associated with surgical systemic-pulmonary artery shunts, and patients with transposed or malposed great arteries. Thirty-nine patients at The Johns Hopkins Hospital and 63 patients at The Mayo Clinic had primary diagnoses of pulmonary valve atresia, VSD, and large systemic-pulmonary collateral arteries (SPCAs). Of these 102 patients, 30 fulfilled all our criteria and had the appropriate studies available for review. All patients had aortography, 26 had right ventriculography and 28 had selective angiography of at least one SPCA. The techniques for selective catheterization of large bronchial or other collateral vessels to the lungs have been previously described9 and are similar to our techniques for selective catheterization of subclavian-pulmonary or other systemic-pulmonary artery shunts."' The use of soft, variable stiffness guidewires is often necessary to selectively advance the catheter into hilar pulmonary arteries. Depending on the size of the patient and the size of the collateral vessel to the lung, an amount and flow rate for injection of contrast material are chosen. At times, a one second test injection at the anticipated flow rate is done under fluoroscopy with video-tape monitoring. This assures that proper opacification will be obtained during the angiographic series and also assures that recoil of the catheter will not occur. Often, larger amounts of contrast material than anticipated are required for adequate opacification when there are large systemic-pulmonary collaterals from the descending thoracic aorta. Radiographic subtraction techniques are an additional useful method for enhancing the angiographic evaluation of the systemic-pulmonary artery circulation.
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TABLE 1. Stenosi.s of Systemic-Pulmonary Collateral Arteries No. of Pts.
No. of SPCAs
8
1
11 8 3
2 3 4
30
Total
SPCAs
8 22 24 12
66
Pts. with SPCAs with stenotic SPCAs stenosis
5 (63%) 12 (55%) 9 (38%) 2 (17%) 28 (42%)
5 (63%) 10 (91%) 5 (63%) 1 (33%)
TABLE 2. Pulmonary Artery Stenosis in Patient.s monary Valve Atresia and Ventricular Septal Defect No PAS Hilar PAS 9 Unilateral 4 Bilateral Peripheral PAS and Unilateral Hilar Stenosis Peripheral PAS Stenosis
with Ptl12 13
1 4
21 (70%)
Abbreviations: SPCA = systemic-pulmonary collateral arteries; Pts = patienta.
Particular attention was paid to the presence or absence of right ventricular infundibulum; presence and size of the pulmonary artery confluence; presence and location of pulmonary artery stenosis; and number, origin, and stenosis of systemic-pulmonary collateral arteries. The pulmonary artery confluence was defined as any connection between the right and left main pulmonary arteries. We graded the degree of hypoplasia of the confluence as mild, moderate, or severe by subjective comparison with the aortic root and vertebral bodies. Patients without a visible pulmonary artery confluence, but with hilar pulmonary arteries, were included. In these patients, the confluence may not have been demonstrated because of failure to selectively perform angiography in one of the collateral vessels or because the confluence was fibrous in nature.
a
Results There were 18 male and 12 female patients ranging in age from one to 50 years. A clearly demonstrated right ventricular (RV) infundibulum was present in 17 (65%) of the 26 patients who had right ventriculograms available for review (fig. 1 A). Fifteen of these had a definite pulmonary artery confluence demonstrated by angiography (figs. 1-4). Of the nine individuals without a visible RV infundibulum, five had a pulmonary artery confluence. A pulmonary artery confluence was visualized in 23 (77%) of the 30 patients. Five of these were judged to have a normal-sized pulmonary artery confluence, six had mildly hypoplastic pulmonary arteries, six had moderate hypoplasia (figs. 1, 2), and six had severe hypoplasia (fig. 3B) of the pulmonary arteries. In seven patients (23%) a pulmonary artery confluence could not be demonstrated. As summarized in table 1, eight patients had a single SPCA arising from the descending aorta, 11 patients had two SPCAs, eight had three SPCAs, and three had four. In addition, of the five patients with other large systemic collaterals, one patient had a supply from the internal mammary artery and the remainder had tortuous collaterals
30 Abbreviation: PAS = pulmonary artery stenosis.
originating from the innominate or subclavian arteries and anastomosing directly to the pulmonary arteries (fig. 3). Of the 66 SPCAs originating from the descending aorta, 28 vessels (42%) among 21 patients had definite narrowing at some point in their course (table 1, fig. 4). Nine patients (30%) had no SPCA narrowing. The most common site of stenosis appeared to be at the SPCA-pulmonary artery connection. Narrowing was also frequently seen at the origin of the SPCA from the aorta. Mid-vessel narrowing was less discrete and tended to be more tubular (fig. 5). Other SPCAs without clearly visible stenoses were often tortuous and elongated, suggesting that an appreciable gradient was present along the course of the vessel. The most frequent site of pulmonary artery stenosis was in the hilar region at the point of primary branching to upper and lower lobes. Fourteen of 30 patients (47%) demonstrated hilar pulmonary artery narrowing (figs. 1 F, 2, 4). Three patients had right-sided hilar stenosis only; six had exclusively left-sided; and five had bilateral hilar stenosis. With the exception of one case, peripheral stenosis beyond the hilar region was mild and limited in scope; four patients had evidence of mild peripheral stenosis and in only one patient was there significant beading of distal vessels (table 2). There was no correlation between the presence of hilar stenosis and hypoplasia of the pulmonary artery confluence. Pulmonary artery pressures were measured in four patients via a catheter introduced selectively through a SPCA. Peak systolic pressure differences between the SPCA and pulmonary artery ranged from 45 to 90 mm Hg. Absolute values for pulmonary artery pressures are shown in table 3. An interesting feature of this group of patients is the high proportion of aortic arch anomalies. Right aortic arch was present in 15 (50%) patients; in 13 of these (87%) there was mirror-image branching, and in the remaining two patients anomalous origin of the left subclavian artery was present. One of the 15 patients with left aortic arch had an anomalous right subclavian artery. There was no correlation between arch anomalies and the status of the confluence or presence of stenotic lesions in the circulation to the lungs.
FIGURE 1. Right ventriculogram (A, B), aortogram (C, D), and selective bronchial arteriogram (E, F) from a patient with pulmonary valve atresia, large ventricular septal defect (VSD), and systemic collaterals to the lung. The right yentriculogram (A, B) demonstrates an atretic pulmonary valve with well-defined right ventricular infundibulum (arrow). Early opacification of the aorta through the VSD is noted and systemic collaterals to the lung faintly visualized. Aortogram (C, D) demonstrates at least three large diffusely narrowed systemic collateral vessels originating from the descending aorta entering the right and left pulmonary hilar regions (C). The late radiographs (D) from this series show faint opacification of a pulmonary artery confluence (arrow). Selective bronchial arteriogram (E, F) demonstrates clearly the pulmonary artery confluence. There is moderate hypoplasia of the confluence and left hilar stenoses of the pulmonary artery are demonstrated. Clear definition of the pulmonary artery confluence and distal pulmonary circulation was only possible after selective bronchial arteriography. Downloaded from http://circ.ahajournals.org/ by guest on March 8, 2015
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Discussion
Pulmonary valve atresia with VSD and systemic collaterals to the lungs is, under certain circumstances, an operable condition. Complete delineation of the vascular supply to the lungs is essential to determine preoperatively
the presence of adequate pulmonary arteries with or without a confluence. The operative procedures which have been employed include the interposition of a valved prosthetic conduit or insertion of a patchgraft from the right ventricular outflow tract to the confluence when the confluence of the pulmonary arteries is of adequte size.3 If the pulmonary artery confluence is small, systemic-pulmonary artery shunts may palliate and increase the size of the pulmonary artery confluence so that later a definitive operation may be performed.7 Accurate definition of collaterals preoperatively is also important to facilitate intraoperative procedures and to prevent postoperative cardiac overdistension or left-to-right shunt. Classification of the large systemic collateral arteries supplying the pulmonary arteries in this anomaly has not yet been established because of an incomplete understanding of the embryonic development of these vessels.12.18 Some authors state that the term "'bronchial artery" is embryologically and anatomically incorrect,18 while others continue to use the phrase "large bronchial collateral arteries" for description of these vessels.7 We have utilized the term ".systemic-pulmonary collateral artery" (SPCA) to refer to both bronchial and intercostal artery collaterals, as well as collateral vessels of less certain derivation. Assessment of other features of pulmonary artery vascular anatomy is of value in predicting the outcome of surgery. It has been suggested that a degree of collateral and/or pulmonary artery stenosis in these patients may protect more distal pulmonary vessels from arterial pressure early in life, thus enhancing the probability of favorable surgical results.1, 8, 10, 18, 19 Several previous reports suggest that bronchial and/or pulmonary artery stenosis is a frequent feature of pulmonary atresia. Chesler et al.10 described a series of 44 patients studied by selective arteriography of whom 38 had demonstrable pulmonary arteries. Nine patients had exclusively nonductal systemic arteries supplying the lungs and of these, five had stenosis of the systemic artery and two had "stenotic origins" of the left and right pulmonary arteries. In another series,8 I I of 30 patients with pulmonary valve atresia had large nonductal SPCAs supplying the lung; nine had proximal stenoses of at least one of the systemic collateral arteries. The large systemic arteries were described as entering the lungs via the hilum to become continuous with the hilar pulmonary arteries, at which point there was usually a stenosed segment. The authors observed that those patients without a stenotic segment had evidence of severe pulmonary hypertension, making them poor candidates for surgery. The present study confirms the high incidence of stenotic systemic-collateral arteries to the lungs in patients with pulmonary valve atresia. Seventy percent of TABLE 3. Pulmonary Artery Pressures in Patients with Pulmonary Valve Atresia and VSD
FIGURE 2.
Selective bronchial arteriogram (panelA, AP ;panel B,
lateral) demonstrating moderate hypoplasia of pulmonary artery confluence and severe peripheral pulmonary artery stenoses involving the left hilar branches. An additional SPCA supplied the right upper lobe (not shown).
Pt
PA pressure
SPCA stenosis
PA stenosis
1 2 3 4
15/11 (13) 60/46 (50) 30/20 (25) 10/3 (6)
3/3 2/3 1/1 1/2
Left hilar None None Bilateral hilar
Abbreviations: PA pulmonary artery; SPCA = systemic-pulmonary collateral artery; VSD = ventricular septal defect.
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STENOSES OF COLLATERALS IN PULMONARY ATRESIA/McGoon et al.
477
l
I
FIGURE 3. Early (A), mid (B) and late (C) AP radiographs from selective right internal mammary artery (IMA) arteriogram. A large proximal IMA is noted (arrow) and arising from it is a large collateral artery (double arrow) which anastomoses directly to a severely hypoplastic pulmonary artery confluence. The continuation of the normal sized IMA extends retrosternally (D). Five of the 30 patients in this series had innominate or subclavian collaterals anastomosing directly with pulmonary artery confluences.
patients had some stenosis of at least one SPCA, while 30% had stenosis of all SPCAs. The hemodynamic characteristics of eight patients with pulmonary valve atresia and VSD were studied by selective pressure measurements via collateral arteries by Macartney et al.19 They found systolic pressure differences across the stenoses of 28-81 mm Hg to be invariably present regardless of the type of aortopulmonary connection (SPCA, patent ductus arteriosus, or surgical shunt) and reasoned that the stenoses at the aortopulmonary collateral/pulmonary artery junction generally protected the distal pulmonary
vascular bed from the adverse effect of systemic pressures. In the present study, the four patients in whom selective pressures were measured had a significant pressure difference across the SPCA. Thus, despite the systemic origin of the pulmonary blood flow in these patients, anatomic and hemodynamic observations suggest that in most of these patients the distal vasculature is to some extent protected from systemic pressures. Nearly half (47%) of the patfients studied had angiographically demonstrable hilar stenosis of the pulmonary artery, either immediately distal to the SPCA-pulmonary
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AORTIC ARCH -
Right- 50%
-
Left- 50%
PA STENOSIS
17%
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OON FWENCE 77%
65%
FIGURE 4. Schematic representation of the characteristics of 30 patients with pulmonary valve atresia and systemic-pulmonary collateral arteries. Figures refer to percentage of patients demonstrating each feature, unless otherwise noted. SPCA = systemic-pulmonary collateral artery; PA = pulmonary artery; R V - right ventricle.
artery junction or at the level of primary branching of the pulmonary artery. Since these stenotic sites are distal to the point of surgical anastomosis of the conduit, they may produce high pulmonary artery pressure postoperatively in some patients, thus accounting for an inadequate surgical result. There appears to be a slight tendency for SPCA stenosis to occur in conjunction with hilar stenosis so that the prognostic advantages of the former may be counterbalanced by the potential disadvantages of the latter. Individuals with SPCA stenosis and no hilar stenosis would be predicted to derive the most benefits from surgery, provided there is a suitable pulmonary artery confluence or adequate vessel for anastomosis of the conduit. This remains
theoretical and requires postoperative follow-up of a number of patients for verification. Three surgical series4 6 I report postoperatively elevated RV systolic pressures in a number of patients and generally less markedly elevated systolic pulmonary artery pressures. No correlation of results with the presence of pulmonary or SPCA stenosis was attempted, though degree of pulmonary artery hypoplasia was well recognized as limiting surgical results. In one report, two week postoperative pressure measurements distal to the allograft valve in a bifurcating dacron conduit were 75/10 and published preoperative angiograms suggested a degree of peripheral pulmonary artery stenosis in this patient.4 In Chesler's series of 44 patients with pulmonary valve atresia and VSD, each of the nine patients with only nonductal systemic artery supply to the pulmonary arteries had a right ventricular infundibulum.'0 Conversely, in the entire series, four patients had absent right ventricular infundibulum and in these, no pulmonary arteries could be demonstrated. The conclusion was drawn that "when an infundibulum is identified, the condition is likely to be pseudotruncus arteriosus. t In the absence of an identifiable infundibulum, the malformation is probably truncus arteriosus type IV where the chances of finding collateral vessels anatomically and hemodynamically suitable for surgical correction are very much less." The present study fails to support that conclusion. We found that of the nine individuals without an identifiable infundibulum, five had a pulmonary artery confluence demonstrated by either aortography or selective SPCA injection and three of the confluences were of normal size or mildly hypoplastic. The existence of a confluence without radiographic evidence of a right ventricular outflow tract may thus not be as rare as previously thought. Failure to visualize an infundibulum should not preclude a thorough search for evidence of confluent pulmonary arteries by selective angiography of the collateral arteries. Establishing a firm diagnosis in this
I1
~ i ~
~
~~~~~~~-_j
I
'Am~S "I w
FIGURE 5. Aortogram (A) and selective bronchial arteriogram (B) demonstrating a systemic-pulmonary collateral artery (SPCA ) with mid-vessel t ubular narrowing that supplies a left p ulmonary artery. No stenosis was seen in the SPCA
to the right lung, and no confluence filled in later films of this series. Downloaded from http://circ.ahajournals.org/ by guest on March 8, 2015
STENOSES OF COLLATERALS IN PULMONARY ATRESIA/McGoon et al4 regard is of fundamental importance in determining the operability of the lesion. Nearly half (48%) of the 23 patients with a pulmonary artery confluence had moderate or severe hypoplasia, though there was no correlation between either SPCA or hilar stenosis and degree of hypoplasia. Even severe hypoplasia does not preclude surgical correction, in view of our personal experience and recent reports that pulmonary arteries in such patients may increase in diameter in response to a palliative aortopulmonary shunt procedure, thus making them suitable for definitive correction at a later date.7 If flow through the surgical shunt provides a new and substantial stimulus to growth, the best responses may eventually be found to occur in those pulmonary arteries previously protected from systemic pressures by stenotic collaterals. The high incidence of a right aortic arch in pulmonary valve atresia is well recognized, as it is in various other congenital anomalies. Eight of 30 patients with pulmonary valve atresia studied by Jefferson et al.16 had a right aortic arch and six (40%) of these were in the subgroup of 15 patients with large systemic collaterals, i.e., the group most analogous to the population we have studied. To our knowledge, the 50% incidence we observed represents the highest association of right aortic arch with any congenital cardiac anomaly. The high incidence of SPCA and hilar pulmonary artery narrowing in patients with pulmonary valve atresia and ventricular septal defect will require careful postoperative evaluation after total correction to appreciate the effects of these anatomical stenoses on the ultimate course of these patients. Careful preoperative evaluation of all systemic collaterals by selective angiography is considered necessary to visualize stenotic hilar pulmonary arteries and to determine the presence or absence of a pulmonary artery confluence in each patient.
Acknowledgment The authors gratefully acknowledge the assistance of Mrs. Olga Carr in the preparation of this manuscript.
479
References 1. Taussig HB: Congenital Malformations of the Heart. Cambridge, Harvard University Press, 1947 2. Collett RW, Edwards JE: Persistent truncus arteriosus: A classification according to anatomic types. Surg Clin North Am: 1245, 1949 3. McGoon DC, Rastelli GC, Wallace RB: Discontinuity between right ventricle and pulmonary artery: Surgical treatment. Ann Surg 172: 680, 1970 4. Kouchoukos NT, Barcia A, Bargeron LM, Kirklin JW: Surgical treatment of congenital pulmonary atresia with ventricular septal defect. J Thorac Cardiovasc Surg 61: 60, 1971 5. Doty DB, Kouchoukos NT, Kirklin JW, Barcia A, Bargeron LM: Surgery for pseudotruncus arteriosus with pulmonary blood flow originating from upper descending thoracic aorta. Circulation 45 (suppl 1): 1-121, 1972 6. Pacifico AD, Kirklin JW, Bargeron LM, Sota B: Surgical treatment of common arterial trunk with pseudotruncus arteriosus. Circulation 50 (suppl II): 11-20, 1974 7. McGoon DC, Baird DK, Davis GD: Surgical management of large bronchial collateral arteries with pulmonary stenosis or atresia. Circulation 52: 109, 1975 8. Chesler E, Beck W, Schrire V: Selective catheterization of pulmonary or bronchial arteries in the preoperative assessment of pseudotruncus arteriosus and truncus arteriosus type IV. Am J Cardiol 26: 20, 1970 9. Levin DC, Baltaxe HA, Goldberg HP, Engle MA, Ebert PA, Sos TA, Levin AR: The importance of selective angiography of systemic arterial supply to the lungs in planning surgical correction of pseudotruncus arteriosus. Am J Roentgenol 121: 606, 1974 10. Chesler E, Matisonn R, Beck W: The assessment of the arterial supply to the lungs in pseudotruncus arteriosus and truncus arteriosus type IV in relation to surgical repair. Am Heart J 88: 542, 1974 11. White RI Jr: Technique and preliminary results of selective catheterization of patients with Blalock-Taussig shunts. Radiology 105: 703, 1972 12. Marchand P, Gilroy JC, Wilson VH: An anatomical study of the bronchial vascular system and its variation in disease. Thorax 5: 207, 1950 13. Tobin CE: The bronchial arteries and their connections with other vessels in the human lung. Surg Gynecol Obstet 75: 741, 1952 14. Gunteroth WG, Arcasoy MM, Phillips LA, Figley MM: Demonstration of collateral circulation to the lungs with angiocardiographic studies in congenital heart disease. Am Heart J 64: 293, 1962 15. Boyden EA: The time lag in the development of bronchial arteries. Anat Record 166: 611, 1970 16. Jefferson K, Rees S, Somerville J: Systemic arterial supply to the lungs in pulmonary atresia and its relation to pulmonary artery development. Br Heart J 34: 418, 1972 17. Stuckey D, Bowdler JD, Reye RDK: Absent sixth aortic arch: A form of pulmonary atresia. Br Heart J 30: 258, 1968 18. Tynan MJ, Gleeson JA: Pulmonary atresia with bronchial arteries arising from the subclavian arteries. Br Heart J 28: 573, 1966 19. Macartney FJ, Scott 0, Deverall PB: Hemodynamic and anatomical characteristics of pulmonary blood supply in pulmonary atresia with ventricular septal defect, including a case of persistent fifth aortic arch. Br Heart J 36: 1049, 1974
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Systemic collateral and pulmonary artery stenosis in patients with congenital pulmonary valve atresia and ventricular septal defect. M D McGoon, R E Fulton, G D Davis, D G Ritter, C A Neill and R I White, Jr Circulation. 1977;56:473-479 doi: 10.1161/01.CIR.56.3.473 Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1977 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7322. Online ISSN: 1524-4539
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narrowing and 21 patients (70%) had one or more narrowed SPCAs. Five patients had collaterals from internal mammary, subclavian or innominate arteries. Fourteen (47%) had hilar pulmonary artery stenosis. Of these 14 patients mild peripheral stenosis was demonstrated in five. Right aortic arch was present in 15 patients (50%). Complete angiographic delineation of pulmonary vasculature is an essential procedure for preoperative detection of pulmonary and SPCA stenoses in these patients.
CONGENITAL PULMONARY VALVE ATRESIA with ventricular septal defect (VSD) associated with hypoplasia or absence of the main pulmonary artery has been referred to generally as severe tetralogy of Fallot, pseudotruncus arteriosus' or, if no hilar pulmonary arteries are seen, type IV truncus arteriosus.2 We prefer not to use these terms synonomously as some forms of pulmonary valve atresia with VSD have become increasingly amenable to correction by newer surgical techniques. Until recently, it was difficult to make the distinction between truncus type IV, an inoperable anomaly, and other forms of pulmonary valve atresia with VSD. Since it is now imperative that this distinction be made, a thorough angiographic examination of the aorta and systemic collateral circulation to the lung is essential for diagnosis and for determining operability and surgical approach. With the development and increasing application of surgical techniques in the management of patients with pulmonary artery discontinuity,3-7 attention has been directed to the importance of selective catheterization as a means of obtaining maximal radiographic information for determining correctability of the lesion.8 10 Concise detailed understanding of the pulmonary vasculature in this congenital problem has become a vital prerequisite to optimal management. Diagnostic evaluation of these patients has revealed a high incidence of central and peripheral pulmonary artery stenosis not fully documented previously. Recognizing the importance of characterizing all systemic collateral and pulmonary arteries in these patients, we have retrospectively analyzed the angiograms of 30 patients in a combined series
from The Johns Hopkins Hospital and The Mayo Clinic in an effort to evaluate primarily the presence, degree and location of stenosis and/or hypoplasia of the systemic collateral arteries to the lungs and the pulmonary arteries.
From the Division of Cardiovascular Radiology, Department of Radiology and Radiological Sciences, and the Division of Pediatric Cardiology, Department of Pediatrics, The Johns Hopkins Medical Institutions, Baltimore, Maryland; and the Division of Cardiovascular Radiology, Department of Radiology, and the Division of Pediatric Cardiology, Department of Pediatrics, The Mayo Clinic, Rochester, Minnesota. Supported in part by USPHS Training Grant No. 5 TOI HL05970-04 from the National Heart and Lung Institute, Bethesda, Maryland. Mr. McGoon is a Henry Strong Denison Scholar, 1976-77. Address for reprints: Robert I. White, Jr., M.D., Department of Radiology, Johns Hopkins Hospital, Baltimore, Maryland 21205. Received March 11, 1977; revision accepted April 25, 1977.
Materials and Methods Specifically excluded in this review were those patients with congenital pulmonary valve atresia and hypoplastic right ventricle, congenital pulmonary valve atresia with pulmonary blood flow arising entirely from a patent ductus arteriosus, acquired pulmonary valve atresia associated with surgical systemic-pulmonary artery shunts, and patients with transposed or malposed great arteries. Thirty-nine patients at The Johns Hopkins Hospital and 63 patients at The Mayo Clinic had primary diagnoses of pulmonary valve atresia, VSD, and large systemic-pulmonary collateral arteries (SPCAs). Of these 102 patients, 30 fulfilled all our criteria and had the appropriate studies available for review. All patients had aortography, 26 had right ventriculography and 28 had selective angiography of at least one SPCA. The techniques for selective catheterization of large bronchial or other collateral vessels to the lungs have been previously described9 and are similar to our techniques for selective catheterization of subclavian-pulmonary or other systemic-pulmonary artery shunts."' The use of soft, variable stiffness guidewires is often necessary to selectively advance the catheter into hilar pulmonary arteries. Depending on the size of the patient and the size of the collateral vessel to the lung, an amount and flow rate for injection of contrast material are chosen. At times, a one second test injection at the anticipated flow rate is done under fluoroscopy with video-tape monitoring. This assures that proper opacification will be obtained during the angiographic series and also assures that recoil of the catheter will not occur. Often, larger amounts of contrast material than anticipated are required for adequate opacification when there are large systemic-pulmonary collaterals from the descending thoracic aorta. Radiographic subtraction techniques are an additional useful method for enhancing the angiographic evaluation of the systemic-pulmonary artery circulation.
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TABLE 1. Stenosi.s of Systemic-Pulmonary Collateral Arteries No. of Pts.
No. of SPCAs
8
1
11 8 3
2 3 4
30
Total
SPCAs
8 22 24 12
66
Pts. with SPCAs with stenotic SPCAs stenosis
5 (63%) 12 (55%) 9 (38%) 2 (17%) 28 (42%)
5 (63%) 10 (91%) 5 (63%) 1 (33%)
TABLE 2. Pulmonary Artery Stenosis in Patient.s monary Valve Atresia and Ventricular Septal Defect No PAS Hilar PAS 9 Unilateral 4 Bilateral Peripheral PAS and Unilateral Hilar Stenosis Peripheral PAS Stenosis
with Ptl12 13
1 4
21 (70%)
Abbreviations: SPCA = systemic-pulmonary collateral arteries; Pts = patienta.
Particular attention was paid to the presence or absence of right ventricular infundibulum; presence and size of the pulmonary artery confluence; presence and location of pulmonary artery stenosis; and number, origin, and stenosis of systemic-pulmonary collateral arteries. The pulmonary artery confluence was defined as any connection between the right and left main pulmonary arteries. We graded the degree of hypoplasia of the confluence as mild, moderate, or severe by subjective comparison with the aortic root and vertebral bodies. Patients without a visible pulmonary artery confluence, but with hilar pulmonary arteries, were included. In these patients, the confluence may not have been demonstrated because of failure to selectively perform angiography in one of the collateral vessels or because the confluence was fibrous in nature.
a
Results There were 18 male and 12 female patients ranging in age from one to 50 years. A clearly demonstrated right ventricular (RV) infundibulum was present in 17 (65%) of the 26 patients who had right ventriculograms available for review (fig. 1 A). Fifteen of these had a definite pulmonary artery confluence demonstrated by angiography (figs. 1-4). Of the nine individuals without a visible RV infundibulum, five had a pulmonary artery confluence. A pulmonary artery confluence was visualized in 23 (77%) of the 30 patients. Five of these were judged to have a normal-sized pulmonary artery confluence, six had mildly hypoplastic pulmonary arteries, six had moderate hypoplasia (figs. 1, 2), and six had severe hypoplasia (fig. 3B) of the pulmonary arteries. In seven patients (23%) a pulmonary artery confluence could not be demonstrated. As summarized in table 1, eight patients had a single SPCA arising from the descending aorta, 11 patients had two SPCAs, eight had three SPCAs, and three had four. In addition, of the five patients with other large systemic collaterals, one patient had a supply from the internal mammary artery and the remainder had tortuous collaterals
30 Abbreviation: PAS = pulmonary artery stenosis.
originating from the innominate or subclavian arteries and anastomosing directly to the pulmonary arteries (fig. 3). Of the 66 SPCAs originating from the descending aorta, 28 vessels (42%) among 21 patients had definite narrowing at some point in their course (table 1, fig. 4). Nine patients (30%) had no SPCA narrowing. The most common site of stenosis appeared to be at the SPCA-pulmonary artery connection. Narrowing was also frequently seen at the origin of the SPCA from the aorta. Mid-vessel narrowing was less discrete and tended to be more tubular (fig. 5). Other SPCAs without clearly visible stenoses were often tortuous and elongated, suggesting that an appreciable gradient was present along the course of the vessel. The most frequent site of pulmonary artery stenosis was in the hilar region at the point of primary branching to upper and lower lobes. Fourteen of 30 patients (47%) demonstrated hilar pulmonary artery narrowing (figs. 1 F, 2, 4). Three patients had right-sided hilar stenosis only; six had exclusively left-sided; and five had bilateral hilar stenosis. With the exception of one case, peripheral stenosis beyond the hilar region was mild and limited in scope; four patients had evidence of mild peripheral stenosis and in only one patient was there significant beading of distal vessels (table 2). There was no correlation between the presence of hilar stenosis and hypoplasia of the pulmonary artery confluence. Pulmonary artery pressures were measured in four patients via a catheter introduced selectively through a SPCA. Peak systolic pressure differences between the SPCA and pulmonary artery ranged from 45 to 90 mm Hg. Absolute values for pulmonary artery pressures are shown in table 3. An interesting feature of this group of patients is the high proportion of aortic arch anomalies. Right aortic arch was present in 15 (50%) patients; in 13 of these (87%) there was mirror-image branching, and in the remaining two patients anomalous origin of the left subclavian artery was present. One of the 15 patients with left aortic arch had an anomalous right subclavian artery. There was no correlation between arch anomalies and the status of the confluence or presence of stenotic lesions in the circulation to the lungs.
FIGURE 1. Right ventriculogram (A, B), aortogram (C, D), and selective bronchial arteriogram (E, F) from a patient with pulmonary valve atresia, large ventricular septal defect (VSD), and systemic collaterals to the lung. The right yentriculogram (A, B) demonstrates an atretic pulmonary valve with well-defined right ventricular infundibulum (arrow). Early opacification of the aorta through the VSD is noted and systemic collaterals to the lung faintly visualized. Aortogram (C, D) demonstrates at least three large diffusely narrowed systemic collateral vessels originating from the descending aorta entering the right and left pulmonary hilar regions (C). The late radiographs (D) from this series show faint opacification of a pulmonary artery confluence (arrow). Selective bronchial arteriogram (E, F) demonstrates clearly the pulmonary artery confluence. There is moderate hypoplasia of the confluence and left hilar stenoses of the pulmonary artery are demonstrated. Clear definition of the pulmonary artery confluence and distal pulmonary circulation was only possible after selective bronchial arteriography. Downloaded from http://circ.ahajournals.org/ by guest on March 8, 2015
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Discussion
Pulmonary valve atresia with VSD and systemic collaterals to the lungs is, under certain circumstances, an operable condition. Complete delineation of the vascular supply to the lungs is essential to determine preoperatively
the presence of adequate pulmonary arteries with or without a confluence. The operative procedures which have been employed include the interposition of a valved prosthetic conduit or insertion of a patchgraft from the right ventricular outflow tract to the confluence when the confluence of the pulmonary arteries is of adequte size.3 If the pulmonary artery confluence is small, systemic-pulmonary artery shunts may palliate and increase the size of the pulmonary artery confluence so that later a definitive operation may be performed.7 Accurate definition of collaterals preoperatively is also important to facilitate intraoperative procedures and to prevent postoperative cardiac overdistension or left-to-right shunt. Classification of the large systemic collateral arteries supplying the pulmonary arteries in this anomaly has not yet been established because of an incomplete understanding of the embryonic development of these vessels.12.18 Some authors state that the term "'bronchial artery" is embryologically and anatomically incorrect,18 while others continue to use the phrase "large bronchial collateral arteries" for description of these vessels.7 We have utilized the term ".systemic-pulmonary collateral artery" (SPCA) to refer to both bronchial and intercostal artery collaterals, as well as collateral vessels of less certain derivation. Assessment of other features of pulmonary artery vascular anatomy is of value in predicting the outcome of surgery. It has been suggested that a degree of collateral and/or pulmonary artery stenosis in these patients may protect more distal pulmonary vessels from arterial pressure early in life, thus enhancing the probability of favorable surgical results.1, 8, 10, 18, 19 Several previous reports suggest that bronchial and/or pulmonary artery stenosis is a frequent feature of pulmonary atresia. Chesler et al.10 described a series of 44 patients studied by selective arteriography of whom 38 had demonstrable pulmonary arteries. Nine patients had exclusively nonductal systemic arteries supplying the lungs and of these, five had stenosis of the systemic artery and two had "stenotic origins" of the left and right pulmonary arteries. In another series,8 I I of 30 patients with pulmonary valve atresia had large nonductal SPCAs supplying the lung; nine had proximal stenoses of at least one of the systemic collateral arteries. The large systemic arteries were described as entering the lungs via the hilum to become continuous with the hilar pulmonary arteries, at which point there was usually a stenosed segment. The authors observed that those patients without a stenotic segment had evidence of severe pulmonary hypertension, making them poor candidates for surgery. The present study confirms the high incidence of stenotic systemic-collateral arteries to the lungs in patients with pulmonary valve atresia. Seventy percent of TABLE 3. Pulmonary Artery Pressures in Patients with Pulmonary Valve Atresia and VSD
FIGURE 2.
Selective bronchial arteriogram (panelA, AP ;panel B,
lateral) demonstrating moderate hypoplasia of pulmonary artery confluence and severe peripheral pulmonary artery stenoses involving the left hilar branches. An additional SPCA supplied the right upper lobe (not shown).
Pt
PA pressure
SPCA stenosis
PA stenosis
1 2 3 4
15/11 (13) 60/46 (50) 30/20 (25) 10/3 (6)
3/3 2/3 1/1 1/2
Left hilar None None Bilateral hilar
Abbreviations: PA pulmonary artery; SPCA = systemic-pulmonary collateral artery; VSD = ventricular septal defect.
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STENOSES OF COLLATERALS IN PULMONARY ATRESIA/McGoon et al.
477
l
I
FIGURE 3. Early (A), mid (B) and late (C) AP radiographs from selective right internal mammary artery (IMA) arteriogram. A large proximal IMA is noted (arrow) and arising from it is a large collateral artery (double arrow) which anastomoses directly to a severely hypoplastic pulmonary artery confluence. The continuation of the normal sized IMA extends retrosternally (D). Five of the 30 patients in this series had innominate or subclavian collaterals anastomosing directly with pulmonary artery confluences.
patients had some stenosis of at least one SPCA, while 30% had stenosis of all SPCAs. The hemodynamic characteristics of eight patients with pulmonary valve atresia and VSD were studied by selective pressure measurements via collateral arteries by Macartney et al.19 They found systolic pressure differences across the stenoses of 28-81 mm Hg to be invariably present regardless of the type of aortopulmonary connection (SPCA, patent ductus arteriosus, or surgical shunt) and reasoned that the stenoses at the aortopulmonary collateral/pulmonary artery junction generally protected the distal pulmonary
vascular bed from the adverse effect of systemic pressures. In the present study, the four patients in whom selective pressures were measured had a significant pressure difference across the SPCA. Thus, despite the systemic origin of the pulmonary blood flow in these patients, anatomic and hemodynamic observations suggest that in most of these patients the distal vasculature is to some extent protected from systemic pressures. Nearly half (47%) of the patfients studied had angiographically demonstrable hilar stenosis of the pulmonary artery, either immediately distal to the SPCA-pulmonary
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AORTIC ARCH -
Right- 50%
-
Left- 50%
PA STENOSIS
17%
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CIRCULATION
478
OON FWENCE 77%
65%
FIGURE 4. Schematic representation of the characteristics of 30 patients with pulmonary valve atresia and systemic-pulmonary collateral arteries. Figures refer to percentage of patients demonstrating each feature, unless otherwise noted. SPCA = systemic-pulmonary collateral artery; PA = pulmonary artery; R V - right ventricle.
artery junction or at the level of primary branching of the pulmonary artery. Since these stenotic sites are distal to the point of surgical anastomosis of the conduit, they may produce high pulmonary artery pressure postoperatively in some patients, thus accounting for an inadequate surgical result. There appears to be a slight tendency for SPCA stenosis to occur in conjunction with hilar stenosis so that the prognostic advantages of the former may be counterbalanced by the potential disadvantages of the latter. Individuals with SPCA stenosis and no hilar stenosis would be predicted to derive the most benefits from surgery, provided there is a suitable pulmonary artery confluence or adequate vessel for anastomosis of the conduit. This remains
theoretical and requires postoperative follow-up of a number of patients for verification. Three surgical series4 6 I report postoperatively elevated RV systolic pressures in a number of patients and generally less markedly elevated systolic pulmonary artery pressures. No correlation of results with the presence of pulmonary or SPCA stenosis was attempted, though degree of pulmonary artery hypoplasia was well recognized as limiting surgical results. In one report, two week postoperative pressure measurements distal to the allograft valve in a bifurcating dacron conduit were 75/10 and published preoperative angiograms suggested a degree of peripheral pulmonary artery stenosis in this patient.4 In Chesler's series of 44 patients with pulmonary valve atresia and VSD, each of the nine patients with only nonductal systemic artery supply to the pulmonary arteries had a right ventricular infundibulum.'0 Conversely, in the entire series, four patients had absent right ventricular infundibulum and in these, no pulmonary arteries could be demonstrated. The conclusion was drawn that "when an infundibulum is identified, the condition is likely to be pseudotruncus arteriosus. t In the absence of an identifiable infundibulum, the malformation is probably truncus arteriosus type IV where the chances of finding collateral vessels anatomically and hemodynamically suitable for surgical correction are very much less." The present study fails to support that conclusion. We found that of the nine individuals without an identifiable infundibulum, five had a pulmonary artery confluence demonstrated by either aortography or selective SPCA injection and three of the confluences were of normal size or mildly hypoplastic. The existence of a confluence without radiographic evidence of a right ventricular outflow tract may thus not be as rare as previously thought. Failure to visualize an infundibulum should not preclude a thorough search for evidence of confluent pulmonary arteries by selective angiography of the collateral arteries. Establishing a firm diagnosis in this
I1
~ i ~
~
~~~~~~~-_j
I
'Am~S "I w
FIGURE 5. Aortogram (A) and selective bronchial arteriogram (B) demonstrating a systemic-pulmonary collateral artery (SPCA ) with mid-vessel t ubular narrowing that supplies a left p ulmonary artery. No stenosis was seen in the SPCA
to the right lung, and no confluence filled in later films of this series. Downloaded from http://circ.ahajournals.org/ by guest on March 8, 2015
STENOSES OF COLLATERALS IN PULMONARY ATRESIA/McGoon et al4 regard is of fundamental importance in determining the operability of the lesion. Nearly half (48%) of the 23 patients with a pulmonary artery confluence had moderate or severe hypoplasia, though there was no correlation between either SPCA or hilar stenosis and degree of hypoplasia. Even severe hypoplasia does not preclude surgical correction, in view of our personal experience and recent reports that pulmonary arteries in such patients may increase in diameter in response to a palliative aortopulmonary shunt procedure, thus making them suitable for definitive correction at a later date.7 If flow through the surgical shunt provides a new and substantial stimulus to growth, the best responses may eventually be found to occur in those pulmonary arteries previously protected from systemic pressures by stenotic collaterals. The high incidence of a right aortic arch in pulmonary valve atresia is well recognized, as it is in various other congenital anomalies. Eight of 30 patients with pulmonary valve atresia studied by Jefferson et al.16 had a right aortic arch and six (40%) of these were in the subgroup of 15 patients with large systemic collaterals, i.e., the group most analogous to the population we have studied. To our knowledge, the 50% incidence we observed represents the highest association of right aortic arch with any congenital cardiac anomaly. The high incidence of SPCA and hilar pulmonary artery narrowing in patients with pulmonary valve atresia and ventricular septal defect will require careful postoperative evaluation after total correction to appreciate the effects of these anatomical stenoses on the ultimate course of these patients. Careful preoperative evaluation of all systemic collaterals by selective angiography is considered necessary to visualize stenotic hilar pulmonary arteries and to determine the presence or absence of a pulmonary artery confluence in each patient.
Acknowledgment The authors gratefully acknowledge the assistance of Mrs. Olga Carr in the preparation of this manuscript.
479
References 1. Taussig HB: Congenital Malformations of the Heart. Cambridge, Harvard University Press, 1947 2. Collett RW, Edwards JE: Persistent truncus arteriosus: A classification according to anatomic types. Surg Clin North Am: 1245, 1949 3. McGoon DC, Rastelli GC, Wallace RB: Discontinuity between right ventricle and pulmonary artery: Surgical treatment. Ann Surg 172: 680, 1970 4. Kouchoukos NT, Barcia A, Bargeron LM, Kirklin JW: Surgical treatment of congenital pulmonary atresia with ventricular septal defect. J Thorac Cardiovasc Surg 61: 60, 1971 5. Doty DB, Kouchoukos NT, Kirklin JW, Barcia A, Bargeron LM: Surgery for pseudotruncus arteriosus with pulmonary blood flow originating from upper descending thoracic aorta. Circulation 45 (suppl 1): 1-121, 1972 6. Pacifico AD, Kirklin JW, Bargeron LM, Sota B: Surgical treatment of common arterial trunk with pseudotruncus arteriosus. Circulation 50 (suppl II): 11-20, 1974 7. McGoon DC, Baird DK, Davis GD: Surgical management of large bronchial collateral arteries with pulmonary stenosis or atresia. Circulation 52: 109, 1975 8. Chesler E, Beck W, Schrire V: Selective catheterization of pulmonary or bronchial arteries in the preoperative assessment of pseudotruncus arteriosus and truncus arteriosus type IV. Am J Cardiol 26: 20, 1970 9. Levin DC, Baltaxe HA, Goldberg HP, Engle MA, Ebert PA, Sos TA, Levin AR: The importance of selective angiography of systemic arterial supply to the lungs in planning surgical correction of pseudotruncus arteriosus. Am J Roentgenol 121: 606, 1974 10. Chesler E, Matisonn R, Beck W: The assessment of the arterial supply to the lungs in pseudotruncus arteriosus and truncus arteriosus type IV in relation to surgical repair. Am Heart J 88: 542, 1974 11. White RI Jr: Technique and preliminary results of selective catheterization of patients with Blalock-Taussig shunts. Radiology 105: 703, 1972 12. Marchand P, Gilroy JC, Wilson VH: An anatomical study of the bronchial vascular system and its variation in disease. Thorax 5: 207, 1950 13. Tobin CE: The bronchial arteries and their connections with other vessels in the human lung. Surg Gynecol Obstet 75: 741, 1952 14. Gunteroth WG, Arcasoy MM, Phillips LA, Figley MM: Demonstration of collateral circulation to the lungs with angiocardiographic studies in congenital heart disease. Am Heart J 64: 293, 1962 15. Boyden EA: The time lag in the development of bronchial arteries. Anat Record 166: 611, 1970 16. Jefferson K, Rees S, Somerville J: Systemic arterial supply to the lungs in pulmonary atresia and its relation to pulmonary artery development. Br Heart J 34: 418, 1972 17. Stuckey D, Bowdler JD, Reye RDK: Absent sixth aortic arch: A form of pulmonary atresia. Br Heart J 30: 258, 1968 18. Tynan MJ, Gleeson JA: Pulmonary atresia with bronchial arteries arising from the subclavian arteries. Br Heart J 28: 573, 1966 19. Macartney FJ, Scott 0, Deverall PB: Hemodynamic and anatomical characteristics of pulmonary blood supply in pulmonary atresia with ventricular septal defect, including a case of persistent fifth aortic arch. Br Heart J 36: 1049, 1974
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Systemic collateral and pulmonary artery stenosis in patients with congenital pulmonary valve atresia and ventricular septal defect. M D McGoon, R E Fulton, G D Davis, D G Ritter, C A Neill and R I White, Jr Circulation. 1977;56:473-479 doi: 10.1161/01.CIR.56.3.473 Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1977 American Heart Association, Inc. All rights reserved. Print ISSN: 0009-7322. Online ISSN: 1524-4539
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