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Tetralogy of fallot, pulmonary atresia, and diminutive pulmonary arteries
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries ALDO R. CASTANEDA, M.D. JOHN E. MAYER, Jr., M.D. JAMES E. LOCK, M.D. Departments of Cardiac Surgery and Cardiology The Children's Hospital and Harvard Medical School Boston, Massachusetts
The surgical management of classical tetralogy of Fallot (TOF), with right ventricular-to-pulmonary artery continuity and pulmonic stenosis, has been well established and standardized, and both early and late results are good, even in critically ill infants. In other patients with pulmonary atresia with ventricular septal defect, however, significant additional therapeutic challenges are seen, primarily because of the wide range of origin, size, and distribution of pulmonary blood supply found in this entity. The most fortunate subset of patients with tetralogy of Fallot with pulmonary atresia (TOFPA) are those with valvar pulmonary atresia, a ductus-dependent pulmonary arterial circulation and essentially normal pulmonary arteries. At the other end of anatomic complexity are those patients with TOF-PA without a patent ductus arteriosus (PDA) and with diminutive or absent central pulmonary arteries. In these patients pulmonary blood flow is supplied exclusively by aortopulmonary collateral arteries (APCAs). Because of the significant variations in pulmonary arterial structure and blood flow, no single effective treatment plan is applicable to this diverse group of patients. Generally, Address correspondenceto Aldo R. Castaneda, M.D., Department of Cardiac Surgery, The Children's Hospital, 300 LongwoodAvenue,Boston, MA 02115.
children with pulmonary arteries of adequate size are managed successfully by primary surgical repair, whereas others with diminutive or absent central pulmonary arteries and APCAs require different and more complex treatment strategies.
EMBRYOLOGICAL CONSIDERATIONS During early fetal development the vascular plexus within the lung buds connects with systemic segmental arteries originating from the dorsal aorta. 1'2 By the fortieth day of gestation, this plexus has differentiated into pulmonary segmental arteries supplying the terminal bronchopulmonary units. Within a short time thereafter, the pulmonary parenchyma receives a dual blood supply: one from the right ventricle and the pulmonary arteries originating from the sixth branchial arches and the other from systemic segmental arteries. By the fiftieth day of normal gestation, however, the systemic arterial supply undergoes involution, and blood flow to the developing lung is supplied exclusively by the pulmonary arteries. In the more complex forms of TOF-PA, this normal development is defective and some bronchopulmonary segments or lobes are supplied by true pulmonary arteries and others by APCAs. These systemic collaterals retain the histoProg Pediatr Cardiol 1992; 1(1):50-60
Copyright 9 1992by AndoverMedicalPublishers, Inc.
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
Group I and Group II In TOF-PA with well-developed pulmonary arteries, pulmonary blood flow usually is supplied mainly by a large PDA. In patients in Groups I and II, the pulmonary arteries tend to connect to all bronchopulmonary segments, and it is rare to find diminutive pulmonary arteries. Group II defines patients in whom the main pulmonary artery is entirely absent.
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FIGURE 1. The histologic features of an APCA before it enters the lung parenchyma and within the lung parenchyma are depicted here. Before entering the parenchyma APCAs retain the characteristics of muscular arteries with a well-developed muscular media and adventitia. Within the lung the median muscular layer is gradually replaced by an elastic lamina. In obstructed APCAs normal arteriolar histologic anatomy is preserved with a thin elastic layer. In unobstructed APCAs changes of pulmonary vascular obstructive disease (PVOD) are commonly due to increased blood flow and pressure.
logic characteristics of muscular arteries before they enter the lung parenchyma, whereas the median muscular layer gradually changes into an elastic lamina after the artery penetrates the lung parenchyma (Figure 1). 3
GROSS ANATOMY In TOF-PA the intracardiac lesion is similar to that of conventional TOF, except that there is complete obliteration of the distal right ventricular-pulmonary outflow tract. The therapeutic complexity of this malformation is dependent on the considerable variations in anatomy of the pulmonary circulation, especially in the origin, size, course, and final destination of the pulmonary blood supply. The four major anatomic subsets of this anomaly are shown in Figure 2.
Group III The PDA is either absent or very small in Group III patients. The pulmonary arteries are either hypoplastic or diminutive, connecting to variable numbers of bronchopulmonary segments. Usually, the more important sources of pulmonary blood flow are the APCAs. Discontinuity between the diminutive left and right pulmonary arteries occurs in approximately 30% of cases. Under those conditions one of the diminutive pulmonary arteries usually originates from a left- or a right-sided PDA, depending on the orientation of the aortic arch. Group I V
Group IV patients have no true mediastinal pulmonary arteries. All bronchopulmonary segments are supplied by APCAs, although remnants of parenchymal pulmonary arteries may be present.
ANATOMICAL CHARACTERISTICS In the presence of APCAs, both central and peripheral pulmonary arteries are usually hypoplastic. Moreover, in approximately 60% of APCAs, a significant stenosis is present, either at the origin of the artery from the aorta or at the junction of the systemic collateral artery and the pulmonary artery. 4.5 Most APCAs originate from the descending thoracic aorta, usually near the left main bronchus, with a left-sided aortic arch, or close to the carina, in patients with a right-sided aortic arch. 6'7In some cases APCAs arise from a common aortic trunk, and occasionally a large left or right APCA, distant from its aortic origin, will cross to the contralateral lung. APCAs can also originate from aortic branches such as the left and right subclavian arteries, internal mammary arteries, or even from intraabdominal branches (indirect APCAs).
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Progress in Pediatric Cardiology
TOF/PA
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FIGURE 2. TOF-PA is classified into four groups. In Groups I and II pulmonary arteries are well developed and blood flow is supplied by a large PDA. The main pulmonary artery is absent in Group II. In Group III the PDA is either absent or very small. Both left and right pulmonary arteries are hypoplastic or diminutive, connecting to variable numbers of bronchopulmonary segments; the more important sources of pulmonary blood flow are usually APCAs. In Group IV there are no mediastinal pulmonary arteries and all bronchopulmonary segments are supplied entirely by APCAs.
The APCAs either connect outside the lung with central pulmonary arteries, connect within the lung with lobar or segmental pulmonary arteries, or do not connect with any puImonary arteries, supplying the lung independently (Figure 3). Haworth, 3 who has contributed much to the understanding of the pulmonary blood supply in TOF-PA, demonstrated that central pulmonary arteries supply an average of 50% of bronchopulmonary segments, and APCAs supply 45% of the segments. In the remaining 5%, pulmonary blood supply is dual; these arteries tend to diverge toward the periphery, each accompanying a specific airway to supply a different portion of the bronchopulmonary segment. It may be that all of these findings are interdependent. In many infants with dual supply who have been restudied at later ages, some APCAs have disappeared, most likely from thrombosis. Whether from diminutive pulmonary arteries or from APCAs, the source of pulmonary blood flow affects both the anatomy and the function of the
pulmonary microcirculation. According to Haworth and coworker, 4 preacinar vessels tend to be abnormally small in TOF-PA, both absolutely small and in relationship to the size of accompanying airways. Intra-acinar arteries continue to develop after birth and during the first three years of life. It is important to note that they are fewer in number in TOF-PA, and they have a thinner media layer and a smaller external diameter. Rabinovitch and others 8 found a reduction in the number of pulmonary alveoli when pulmonary blood flow was decreased early in life. Therefore, it is likely that the increased pulmonary vascular resistance found early in life in patients with TOF-PA is caused by a decreased number of intra-acinar arteries, whereas at later ages the increase in pulmonary vascular resistance is more likely the result of pulmonary arteriolar obstructive changes from increased 9blood flow and pressure through unobstructed APC.As. Thiene and associates 5 have demonstrated Heath-Edwards Stage 4 obstructive arteriolar le-
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Puhnonary Arteries
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53
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FIGURE 3. APCAs either connect to central pulmonary arteries (PA) within the mediastinum, connect to lobar or segmental pulmonary arteries within the lung, or do notconnect with any native pulmonary arteries, supplying the lung independently.
sions in two infants with large APCAs, one of whom was only five months of age. Stenosis within APCAs protects the pulmonary vascular bed from damage, but the resultant decrease in pulmonary blood flow also restricts vascular and parenchymal development, which may be equally limiting in the long term.
IMPORTANT DIAGNOSTIC ASPECTS Accurate preoperative measurements of pulmonary artery size or diameter present a number of problems. The maximal capacity or compliance of the undistended pulmonary arteries cannot be assessed reliably with a diminished pulmonary blood flow. Consequently, before surgery it is difficult to predict the postoperative size of a pulmonary artery carrying a normal volume of blood. In spite of this limitation, several methods to quantitate pulmonary artery size have been used to estimate the postoperative repair outcome. The most popular evaluation formula, suggested by McGoon and associates, 9 is based on measurements of the diameter of the right and left pulmonary arteries, normal-
ized by relating them to measurements of the diameter of the descending thoracic aorta at the level of the diaphragm. With this scheme right and left pulmonary arteries are considered to be nonrestrictive to flow when the combined diameter ratio is about 2.0 or greater, whereas a combined diameter ratio of <0.8 indicates severe flow restriction within central pulmonary arteries. The technique developed by Nakata and coworkers t~ measures the diameter of the right and left pulmonary arteries just proximal to the first branch points. Magnification error is corrected either by using values preoperatively determined by cardiac catheterization or by comparing angiographic vessel sizes to the known diameter of an angiographic catheter. Pulmonary artery size is reported as the sum of the cross-sectional areas of the right and left pulmonary arteries, indexed to body surface area. The normal Nakata pulmonary artery index (PAl) is 300 + / - 30 mm2/M z. We have defined pulmonary arteries as diminutive when the PAl is less than 150 mm2/M z. These angiographic assessments have a limitation: The size of the pulmonary arteries may be
Progress in Pediatric Cardiology
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significantly larger after an increased blood flow and distending pressure produced by surgical right ventricular-to-pulmonary artery continuity. On the other hand, there is a small subset of patients in whom the central pulmonary arteries are so small-1 to 2 mm in diameter with PAI <100 ram2/ M 2 - that closure of the ventricular septal defect is clearly contraindicated. In addition to the preoperative identification of the presence and size of pulmonary arteries, it is critically important to demonstrate in detail the origin, course, and distribution of all APCAs. This usually requires selective angiographic injections into all direct and indirect APCAs to obtain the comp!ete map of the pulmonary circulation that is essential in planning optimal treatment strategies. i
;THERAPEUTIC CONSIDERATIONS Most patients with TOF-PA, and particularly those with a ductus-dependent pulmonary circulation and a PAI >150 mm2/M 2, can be successfully repaired with low operative risk and good late hemodynamic and electrophysiologic results. The therapeutic challenges are found in the subset of patients in whom the pulmonary arteries are diminutive with PAl <150 mmZ/Mzand in whom variable numbers of bronchopulmonary segments are supplied by APCAs. Hereafter, this discussion will be limited to the management of patients with TOF-PA who have diminutive pulmonary arteries. The ultimate therapeutic goal is to establish a right ventricular-dependent pulmonary circulation, ideally supplying all 20 bronchopulmonary segments. Hemodynamically, the postoperative right ventrical and left ventrical (RV/LV) systolic pressure ratio should be <0.6 with no residual left-to-right shunts and with little or no evidence of ventricular ectopic electrical activity (Lown <2). In patients with TOF-PA and diminutive pulmonary arteries, this optimal result is rarely achieved, mostly because of several surgical technical limitations, because of the complex variations of pulmonary artery anatomy, and, in our opinion, because of a delay in aggressively treating the pulmonary vascular components of this defect in early infancy. In the past, patients with TOF-PA and diminutive pulmonary arteries were often managed somewhat haphazardly, using a variety of medical or surgical
approaches. This management included primary repair or staged operations, such as preliminary systemic-to-pulmonary artery shunts, n'12 or the establishment of right ventricular-to-pulmonary artery continuity. 6n3n4 These procedures were primarily designed to provide relief of cyanosis and to stimulate enlargement of hypoplastic pulmonary arteries, with the expectation of a later, safer surgical closure of the ventricular septal defect and elimination of any remaining functionally important APCAs. A review revealed that medical management of patients with TOF-PA with diminutive pulmonary arteries was often inadequate, xs An initial high mortality (33%) was found in the few patients who had late repair, and almost all of the survivors had unsatisfactory results. Attempts at primary repair were also disappointing; seven of nine patients died, all from ventricular failure and low cardiac output. Of the two surviving patients, neither has had a satisfactory late outcome. Attempts at initial systemic-to-pulmonary artery shunts decreased the first stage operative mortality, but there were several late deaths before or during subsequent repair. By 1984 the Departments of Cardiac Surgery and Cardiology at The Children's Hospital in Boston demonstrated that hypoplastic and stenotic pulmonary arteries could be enlarged by transcatheter balloon dilation and that flow through APCAs could be interrupted by transcatheter placement of coils. ~6-~s Consequently, a new approach to the management of patients with TOF-PA and diminutive pulmonary arteries evolved in that institution, combining early surgical relief of right ventricular outflow tract obstruction without closure of the ventricular septal defect, followed by interventional catheterization to dilate peripheral pulmonary artery stenosis and to obstruct redundant aortopulmonary collaterals with coils. Thereafter, these preliminary procedures were followed by surgical repair of any residual right ventricular outflow tract obstruction and closure of the ventricular septal defect.
Intraoperative Control of APCAs The origin and course of all APCAs must be clearly outlined before surgery. In the majority of patients, the APCAs emerge from the posterior mediastihum, anterior to the left or right bronchus, to enter the appropriate hila. These vessels may be identified from a sternotomy approach and are looped
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
55
DAP c o l l a t e r a l s , L. t h o r a c o t o m y
FIGURE 4. An aortic or pulmonary artery valved homografl was interposed between the right ventricular outflow tract and the diminutive pulmonary arteries. A pericardial patch was used to augment the proximal anastomosis (insert). Most APCAs can be temporarily looped through a midline sternotomy. In a few instances (insert) if the origin of the APCAs is either from the distal descending thoracic aorta or if it courses behind the left or right bronchus, a lateral thoracotomy is necessary to temporarily or permanently interrupt these vessels.
before beginning cardiopulmonary bypass. We find it useful to dissect the area between the ascending aorta and the right superior vena cava, since the more important APCAs can be found in this area passing anteriorly to the right bronchus. In a few instances in which the origin of the APCAs is either from the distal descending thoracic aorta and/or the APCA courses behind the left or right bronchus, a preliminary thoracotomy is necessary to temporarily or permanently interrupt these vessels (Figure 4). Unifocalization procedures in 6 of 20 patients at The Children's Hospital were carried out after the first stage conduit interposition operation. By first interposing a conduit between the right ventricle and the pulmonary arteries, enlargement of these vessels is stimulated and access is provided for balloon dilation of peripheral pulmonary stenosis and for more accurate angiographic delineation of bronchopulmonary segmental distribution, an important guide to further unifocalization proce-
dures. Whenever an APCA is the end-artery to a significant area of the lung parenchyma, it should be detached from the aorta and anastomosed in an end-to-side fashion to the corresponding pulmonary artery, using a continuous 7-0 PDS suture (Figure 5). Of the six patients who had unifocalization surgery, postoperative catheterizations demonstrated patent anastomoses in all but one. In this patient, a direct anastomosis was not possible because of the distance between arteries, and this patient died after thrombosis of a Gore-Tex graft, placed in an attempt to bridge the distance.
TOF-PA with Either Discontinuous Diminutive Left and Right Pulmonary Arteries or Absent Mediastinal Pulmonary Arteries
In a few patients diminutive pulmonary arteries are present but discontinuous; even fewer patients have no mediastinal pulmonary arteries at all. In many of these patients a coalescence of vessels suit-
56
Progress in Pediatric Cardiology
VSD / "
TOF/PA, MAPC (PAl 50 mm21M 2)
RV-PA homograft and bilateral unifocalization
VSD closure (14 months)
FIGURE 5. Diminutive pulmonary arteries supplied only the right middle lobe, the left lingula, and the left upper lobe. APCAs supplied the fight upper lobe, the fight lower lobe, and the left lower lobe. During initial right ventficular-topulmonary artery (RV-PA) homograft interposition, the fight upper lobe and fight lower APCAs (MAPC) were detached from the aorta and connected endto-side to the fight pulmonary artery; the left lower lobe APCA was connected to the left pulmonary artery. Within 14 months the native pulmonary artery and the unifocalized collateral arteries had enlarged sufficiently to allow for successful closure of the ventricular septal defect.
able for anastomosis can be found at the hilum. First, a right thoracotomy is performed and a 4 mm Gore-Tex graft is interposed between the right subclavian artery and the hilar vascular confluence. In a second operation, usually during the same hospitalization, this procedure is repeated on the left side. The objectives are to unify left- and right-sided pulmonary blood supply through a controlled graft. Within 4-6 months, and after demonstrating an enlargement of the intraparenchymal branches, a larger 10-12 mm Gore-Tex graft is interposed between the right and left hilar pulmonary arteries (Figure 6). Then, through a midline sternotomy and on cardiopulmonary bypass, a valved-homograft is placed between this central Gore-Tex graft and the right ventricle. At the beginning of cardiopulmonary bypass, the left and right modified BlalockTaussig shunts are removed. The ventricular septal
defect is closed only if the peripheral pulmonary arteries have enlarged sufficiently. Otherwise, the ventricular septal defect is left open and closed during a third operation.
RESULTS From 1984 through August 1988, The Children's Hospital has treated 20 patients with TOF-PA and diminutive pulmonary arteries (PAI 10 mm2/M 2 to 150 mm2/M2)J s All patients were managed according to the strategies outlined here. Seven patients were younger than 9 months of age and four were neonates. In all 20 patients aortic or pulmonary cryopreserved valved homografts were placed "between the right ventricle and the junction of the right and left diminutive pulmonary arteries. Cardiopulmonary bypass and a short period of circula-
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Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
TOF/PA
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FIGURE 6. In this patient there were no mediastinal pulmonary arteries. A t 2 weeks of age a 4 mm Gore-Tex shunt was placed between the right subclavian artery and the right hilum through a right thoracotomy. At 4 months of age the same operation was repeated on the left. After the intraparenchymal pulmonary branches became larger, both shunts were removed at II months; a I2 mm conduit was used to connect the right and left hilar pulmonary arteries, and an aortic valved homograft was placed between this central conduit and the right ventricular outflow tract. A t 18 months of age the ventricular septal defect was successfully closed.
tory arrest were used to achieve a bloodless and motionless field, ideal for constructing a necessarily meticulous distal anastomosis. During rewarming, anastomosis between the proximal homograft and the right ventricular anastomosis was accomplished using a glutaraldehyde pretreated pericardial patch to avoid proximal kinking of the homograft. Four of the twenty patients required a separate right lateral thoracotomy to control APCAs before beginning cardiopulmonary bypass. Six (35%) of the twenty patients died. Three patients (15%) died shortly after surgery, two died within 6 months of the operation, and one patient died one year later from a pulmonary artery aneurysm produced by balloon dilation. Of the re-
maining 14 patients, 12 have undergone closure of the ventricular septal defect with two deaths. Of the 10 survivors, seven patients have good hemodynamic results (proved by cardiac catheterization), one patient has residual right ventricular hypertension, and two patients have not yet been catheterized. The 10 survivors were alive at an average of 23 months after surgery. Seven of the ten surviving repaired patients had coil ernbolization of residual systemic collaterals and also underwent successful pulmonary artery dilation procedures. Of the two remaining unrepaired patients, one is not being considered for repair because of inadequate distal pulmonary arteries; the other patient awaits unifocalization surgery. Successful pulmonary artery
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Progress in Pediatric Cardiology
growth was demonstrated in these patients, even in one with an initial PAI of 10 m m ' / M 2. The Children's Hospital has limited experience with the subset of TOF-PA patients with discontinuous and diminutive or absent mediastinal pulmonary arteries. Of five patients with absent mediastinal pulmonary arteries, four have survived, and in two of them the ventricular septal defect has been closed during a third operation.
DISCUSSION In patients with conventional TOF and ventricular-tq-pulmonary artery continuity, diminutive pulm6nary arteries are rare. The incidence of this complicating anatomy is <0.5%. However, in patients ilwith TOF-PA in whom pulmonary blood flow is mostly or exclusively dependent on aortopulmonary collaterals, diminutive pulmonary arteries are common. This most complex form of TOF-PA presents serious therapeutic challenges. Operative mortality and postoperative morbidity is high, and in the past, few of the surgical survivors have had adequate hemodynamic results. 19 Initial medical management without surgery has frequently been associated with the development of advanced pulmonary vascular obstructive disease (PVOD) in bronchopulmonary segments exposed to unobstructed APCA blood flow and with evidence of progressive narrowing of stenotic lesions within APCAs which were impossible to correct surgically and were resistant to balloon dilation. Moreover, there is also evidence that decreased pulmonary blood flow inhibits the development of pulmonary arterioles. Because of these secondary anatomic factors, most operations performed after 5 or 6 years of age have been disappointing. In this relatively older age group of TOF-PA patients, closure of the ventricular septal defect has commonly been associated with residual right ventricular and pulmonary arterial hypertension. Small pulmonary arteries can be enlarged by systemic-to-pulmonary artery shunts. 12 However, we have frequently observed significant iatrogenic damage to these small branch pulmonary arteries after a classical or modified Blalock-Taussig shunt has been created, and even more often after a Waterston shunt. These diminutive pulmonary arteries become easily kinked with shunt surgery, reducing or completely obstructing ipsilateral or contralat-
eral pulmonary blood flow. The surgical creation of continuity between the right ventricle and the pulmonary artery at an early age, leaving the ventricular septal defect open, provides for an antegrade and more balanced blood flow to both right and left pulmonary arteries. The use of cryopreserved valved homografts offer significant advantages over prosthetic grafts with the anatomosis to these small pulmonary arteries. This technique has led to important vessel expansion, even in neonates with initial arteries of only 1.5 mm in diameter. An additional advantage to establishing right ventricular-to-pulmonary artery continuity in early life is to provide access for catheter diagnostic and balloon dilation procedures. Balloon dilation of peripheral pulmonary stenoses is often necessary in these patients, and the precise identification of native pulmonary artery segmental distribution is best accomplished by selective angiographic injections directly into the distal pulmonary arteries. This staged and collaborative approach between cardiac surgeon and pediatric cardiologist also allows for a more rational selection of TOF-PA patients for final repair, based on more precise and complete physiologic and anatomic data. Any patient who develops a significant left-to-right ventricular septal defect shunt after the first stage operation must have sufficient antegrade flow through mediastinal pulmonary arteries to allow closure of the ventricular septal defect. In this circumstance preoperative measurements or calibrations of pulmonary artery size are much less important. The staged treatment plan presented here is based on three premises. 1. Increased blood flow increases the size of hypoplastic pulmonary arteries and stimulates development of distal pulmonary arteries. 2. These enhancing changes occur mostly in early life. 3. APCAs are unreliable sources of pulmonary blood flow resulting in pulmonary vascular obstructive disease, if they are unobstructed, and in unrepairable obstructions, if they are stenotic. 9 The combined, staged approach presented here is in an early phase of development in our institution. Several important questions remain.
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
1 . When are pulmonary arteries too small to allow for primary repair/ 2. Are valved conduits necessary; is a nonvalved conduit, permitting both systolic and diastolic flow, more effective in promoting enlargement of small pulmonary arteries/ 3. Is it possible to construct a conduit that will enlarge with time; will incorporation of a segment of autogenous vessel wall, as proved in experimental animals by Sawatari and associates, 2~ allow enlargement of conduits in humans7 4. How can protection of both the myocardium and the CNS be improved during these lengthy operations/ In the past we have been concerned about perioperative central nervous system complications in these patients, especially with the acute and chronic choreoathetosis seen in a few patients with large APCAs which were not controlled during surgery. We do not know the exact cause of these neurologic complications, but it is possible that they are the result of a cerebrovascular steal during cardiopulmonary bypass, depriving the most sensitive areas of the brain, such as the basal ganglia, of adequate blood flow. Awareness of this complication has led us to control all significant APCAs before starting cardiopulmonary bypass, even if this requires a separate thoracotomy. More effective dilation of stenotic or hypoplastic pulmonary arteries has improved with more experience and with new technical advances. Earlier complications of arterial rupture or aneurysms from balloon dilation are mostly preventable now, and the availability of balloon expandable stainless steel stents has extended the applicability of these techniques. 21 The authors are not ready to form final conclusions from their experience with this approach to the treatment of TOF-PA with diminutive pulmonary arteries. Only a small number of patients have had the staged and combined approach presented here, and the surgically important anatomic and physiologic variations of this defect are numerous. But there is encouragement from the establishment of a right ventricle-to-pulmonary artery continuity with a valved homograft in early infancy with subsequent pulmonary artery dilations and APCA embolizations that has led to successful second-stage
59
repairs in a number of patients. Providing central blood flow to diminutive pulmonary arteries produces a more predictable cross-sectional arterial enlargement and is not associated with lumenal distortion of the arteries. The conduit also provides a more reliable palliation, as judged by higher postoperative systemic oxygen saturations, probably because of an overall increase in pulmonary blood flow and a more effective and balanced distribution of blood flow into both lungs, minimizing unbalanced ventilation and perfusion. If this staged approach to treatment is begun in neonates or young infants, a more physiological development of pulmonary vascular and parenchyreal structures is possible. Ultimately, this should allow for more successful hemodynamic repair in a larger number of patients.
REFERENCES 1. BoydenEA: The time lag in the developmentof bronchial arteries. Anat Rec 1970; 166:611-614. 2. BoydenEA: The developing bronchial arteries in a fetus of the twelfth week. A m ]Anat 1970; 129:357368. 3. Haworth SG, Macartney FJ: Growth and development of pulmonary circulation in pulmonary atresia with ventricular septal defect and major aortopulmonary collateral arteries. Br Heart ] 1980; 44:1424. 4. Haworth SG, Reid L: Quantitative structural study of pulmonary circulation in the newborn with pulmonary atresia. Thorax 1977; 32:129-133. 5. Thiene G, Frescura C, Bini RM, et al: Histology of pulmonary arterial supply in pulmonary atresla with ventricular septal defect. Circulation 1979; 60:10661073. 6. PiehlerJM, Danielson GK, McGoon DC, et al: Management of pulmonary atresia with ventricular septal defect and hypoplastic pulmonary arteries by right ventricular outflow construction. ] Thorac Cardiovasc Surg 1980; 80:552-567. 7. Macartney FJ, Scott L, Deverall PB: Haemodynamic 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 1974; 36:1049-1061. 8. Rabinovitch M, Herrera-deLeon V, Castaneda AR, et al: Growth and development of the pulmonary vascular bed in patients with tetralogy of Fallot with or without pulmonary atresia. Circulation 1981; 64: 1234-1249.
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9. McGoon DC, Baird DK, Davis GD: Surgical management of large bronchial collateral arteries with pulmonary stenosis or atresia. Circulation 1975; 52: 109-118. 10. Nakata S, Imai Y, Takanashi Y, et al: A new method for the quantitative standardization of crosssectional areas of the pulmonary arteries in congenital heart diseases with decreased pulmonary blood flow. ] Thorac Cardiovasc Surg 1984; 88:610-619. 11. Gill CC, Moodie DS, McGoon DC: Staged surgical management of pulmonary atresia with diminutive pulmonary arteries. ] Thorac Cardiovasc Surg 1977; 73:436-442. 12. Kirklin JW, Bargeron LM Jr, Pacifico AD: The enlargement of small pulmonary arteries by preh mmary palhatlve operations. Circulation 1977; 56: 612-617. 13. Millikan JS, Puga FJ, Danielson GK, et al: Staged surgical repair of pulmonary a tresia, ventricular septal defect; and hypoplastic, confluent pulmonary arteries. ] Thorac Cardiovasc Surg 1986; 91:818-825. 14. Olin CL, Ritter DG, McGoon DC, et al: Pulmonary atresia: Surgical considerations and results in 103 patients undergoing definitive repair. Circulation 1976; 54(suppl 1II):35-40. 15. Rome JJ, Mayer JE, Castaneda AR, et al: Tetralogy .t
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of Fallot with pulmonary atresia: Rehabilitation of diminutive pulmonary arteries. Circulation, in press. Lock JE, Castaneda-Zuniga WR, Fuhrman BP, et al: Balloon dilation angioplasty of hypoplastic and stenotic pulmonary arteries. Circulation 1983; 67:962967. Ring JC, Bass JL, Marvin W, et al: Management of congenital stenosis of a branch pulmonary artery with balloon dilation angioplasty: Report of 52 procedures. ] Thorac Cardiovasc Surg 1985; 90:35-44. Perry SB, Radtke W, Fellows KE, et ah Coil embolization to occlude aortopulmonary collateral vessels and shunts in patients with congenital heart disease. J Am Coll Cardiol 1989; 13:100-108. Kirklin JW, Blackstone EH, Shimazaki Y: Survival, functional status, and reoperations after repair of tetralogy of Fallot with pulmonary atresia. ] Thorac Cardiovasc Surg 1988; 96:102-116. Sawatari K, Kawata H, Armiger LC, et al: Growth of composite conduits utilizing longitudinal arterial autograft. J Thorac Cardiovasc Surg, in press. O'Laughlin MP, Perry SB, Lock JE, et al: Implantation of balloon-expandable intravascular stents in patients with congenital heart disease. Circulation 1990; 82(suppl III):658-660.
The surgical management of classical tetralogy of Fallot (TOF), with right ventricular-to-pulmonary artery continuity and pulmonic stenosis, has been well established and standardized, and both early and late results are good, even in critically ill infants. In other patients with pulmonary atresia with ventricular septal defect, however, significant additional therapeutic challenges are seen, primarily because of the wide range of origin, size, and distribution of pulmonary blood supply found in this entity. The most fortunate subset of patients with tetralogy of Fallot with pulmonary atresia (TOFPA) are those with valvar pulmonary atresia, a ductus-dependent pulmonary arterial circulation and essentially normal pulmonary arteries. At the other end of anatomic complexity are those patients with TOF-PA without a patent ductus arteriosus (PDA) and with diminutive or absent central pulmonary arteries. In these patients pulmonary blood flow is supplied exclusively by aortopulmonary collateral arteries (APCAs). Because of the significant variations in pulmonary arterial structure and blood flow, no single effective treatment plan is applicable to this diverse group of patients. Generally, Address correspondenceto Aldo R. Castaneda, M.D., Department of Cardiac Surgery, The Children's Hospital, 300 LongwoodAvenue,Boston, MA 02115.
children with pulmonary arteries of adequate size are managed successfully by primary surgical repair, whereas others with diminutive or absent central pulmonary arteries and APCAs require different and more complex treatment strategies.
EMBRYOLOGICAL CONSIDERATIONS During early fetal development the vascular plexus within the lung buds connects with systemic segmental arteries originating from the dorsal aorta. 1'2 By the fortieth day of gestation, this plexus has differentiated into pulmonary segmental arteries supplying the terminal bronchopulmonary units. Within a short time thereafter, the pulmonary parenchyma receives a dual blood supply: one from the right ventricle and the pulmonary arteries originating from the sixth branchial arches and the other from systemic segmental arteries. By the fiftieth day of normal gestation, however, the systemic arterial supply undergoes involution, and blood flow to the developing lung is supplied exclusively by the pulmonary arteries. In the more complex forms of TOF-PA, this normal development is defective and some bronchopulmonary segments or lobes are supplied by true pulmonary arteries and others by APCAs. These systemic collaterals retain the histoProg Pediatr Cardiol 1992; 1(1):50-60
Copyright 9 1992by AndoverMedicalPublishers, Inc.
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
Group I and Group II In TOF-PA with well-developed pulmonary arteries, pulmonary blood flow usually is supplied mainly by a large PDA. In patients in Groups I and II, the pulmonary arteries tend to connect to all bronchopulmonary segments, and it is rare to find diminutive pulmonary arteries. Group II defines patients in whom the main pulmonary artery is entirely absent.
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T"
e astic layer
FIGURE 1. The histologic features of an APCA before it enters the lung parenchyma and within the lung parenchyma are depicted here. Before entering the parenchyma APCAs retain the characteristics of muscular arteries with a well-developed muscular media and adventitia. Within the lung the median muscular layer is gradually replaced by an elastic lamina. In obstructed APCAs normal arteriolar histologic anatomy is preserved with a thin elastic layer. In unobstructed APCAs changes of pulmonary vascular obstructive disease (PVOD) are commonly due to increased blood flow and pressure.
logic characteristics of muscular arteries before they enter the lung parenchyma, whereas the median muscular layer gradually changes into an elastic lamina after the artery penetrates the lung parenchyma (Figure 1). 3
GROSS ANATOMY In TOF-PA the intracardiac lesion is similar to that of conventional TOF, except that there is complete obliteration of the distal right ventricular-pulmonary outflow tract. The therapeutic complexity of this malformation is dependent on the considerable variations in anatomy of the pulmonary circulation, especially in the origin, size, course, and final destination of the pulmonary blood supply. The four major anatomic subsets of this anomaly are shown in Figure 2.
Group III The PDA is either absent or very small in Group III patients. The pulmonary arteries are either hypoplastic or diminutive, connecting to variable numbers of bronchopulmonary segments. Usually, the more important sources of pulmonary blood flow are the APCAs. Discontinuity between the diminutive left and right pulmonary arteries occurs in approximately 30% of cases. Under those conditions one of the diminutive pulmonary arteries usually originates from a left- or a right-sided PDA, depending on the orientation of the aortic arch. Group I V
Group IV patients have no true mediastinal pulmonary arteries. All bronchopulmonary segments are supplied by APCAs, although remnants of parenchymal pulmonary arteries may be present.
ANATOMICAL CHARACTERISTICS In the presence of APCAs, both central and peripheral pulmonary arteries are usually hypoplastic. Moreover, in approximately 60% of APCAs, a significant stenosis is present, either at the origin of the artery from the aorta or at the junction of the systemic collateral artery and the pulmonary artery. 4.5 Most APCAs originate from the descending thoracic aorta, usually near the left main bronchus, with a left-sided aortic arch, or close to the carina, in patients with a right-sided aortic arch. 6'7In some cases APCAs arise from a common aortic trunk, and occasionally a large left or right APCA, distant from its aortic origin, will cross to the contralateral lung. APCAs can also originate from aortic branches such as the left and right subclavian arteries, internal mammary arteries, or even from intraabdominal branches (indirect APCAs).
52
Progress in Pediatric Cardiology
TOF/PA
I
I!
Iii
IY
FIGURE 2. TOF-PA is classified into four groups. In Groups I and II pulmonary arteries are well developed and blood flow is supplied by a large PDA. The main pulmonary artery is absent in Group II. In Group III the PDA is either absent or very small. Both left and right pulmonary arteries are hypoplastic or diminutive, connecting to variable numbers of bronchopulmonary segments; the more important sources of pulmonary blood flow are usually APCAs. In Group IV there are no mediastinal pulmonary arteries and all bronchopulmonary segments are supplied entirely by APCAs.
The APCAs either connect outside the lung with central pulmonary arteries, connect within the lung with lobar or segmental pulmonary arteries, or do not connect with any puImonary arteries, supplying the lung independently (Figure 3). Haworth, 3 who has contributed much to the understanding of the pulmonary blood supply in TOF-PA, demonstrated that central pulmonary arteries supply an average of 50% of bronchopulmonary segments, and APCAs supply 45% of the segments. In the remaining 5%, pulmonary blood supply is dual; these arteries tend to diverge toward the periphery, each accompanying a specific airway to supply a different portion of the bronchopulmonary segment. It may be that all of these findings are interdependent. In many infants with dual supply who have been restudied at later ages, some APCAs have disappeared, most likely from thrombosis. Whether from diminutive pulmonary arteries or from APCAs, the source of pulmonary blood flow affects both the anatomy and the function of the
pulmonary microcirculation. According to Haworth and coworker, 4 preacinar vessels tend to be abnormally small in TOF-PA, both absolutely small and in relationship to the size of accompanying airways. Intra-acinar arteries continue to develop after birth and during the first three years of life. It is important to note that they are fewer in number in TOF-PA, and they have a thinner media layer and a smaller external diameter. Rabinovitch and others 8 found a reduction in the number of pulmonary alveoli when pulmonary blood flow was decreased early in life. Therefore, it is likely that the increased pulmonary vascular resistance found early in life in patients with TOF-PA is caused by a decreased number of intra-acinar arteries, whereas at later ages the increase in pulmonary vascular resistance is more likely the result of pulmonary arteriolar obstructive changes from increased 9blood flow and pressure through unobstructed APC.As. Thiene and associates 5 have demonstrated Heath-Edwards Stage 4 obstructive arteriolar le-
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Puhnonary Arteries
A
B
]'"" APCA to Central PA
53
C
'1'"" APCA to Lobar PA
APCA without connection to PA
FIGURE 3. APCAs either connect to central pulmonary arteries (PA) within the mediastinum, connect to lobar or segmental pulmonary arteries within the lung, or do notconnect with any native pulmonary arteries, supplying the lung independently.
sions in two infants with large APCAs, one of whom was only five months of age. Stenosis within APCAs protects the pulmonary vascular bed from damage, but the resultant decrease in pulmonary blood flow also restricts vascular and parenchymal development, which may be equally limiting in the long term.
IMPORTANT DIAGNOSTIC ASPECTS Accurate preoperative measurements of pulmonary artery size or diameter present a number of problems. The maximal capacity or compliance of the undistended pulmonary arteries cannot be assessed reliably with a diminished pulmonary blood flow. Consequently, before surgery it is difficult to predict the postoperative size of a pulmonary artery carrying a normal volume of blood. In spite of this limitation, several methods to quantitate pulmonary artery size have been used to estimate the postoperative repair outcome. The most popular evaluation formula, suggested by McGoon and associates, 9 is based on measurements of the diameter of the right and left pulmonary arteries, normal-
ized by relating them to measurements of the diameter of the descending thoracic aorta at the level of the diaphragm. With this scheme right and left pulmonary arteries are considered to be nonrestrictive to flow when the combined diameter ratio is about 2.0 or greater, whereas a combined diameter ratio of <0.8 indicates severe flow restriction within central pulmonary arteries. The technique developed by Nakata and coworkers t~ measures the diameter of the right and left pulmonary arteries just proximal to the first branch points. Magnification error is corrected either by using values preoperatively determined by cardiac catheterization or by comparing angiographic vessel sizes to the known diameter of an angiographic catheter. Pulmonary artery size is reported as the sum of the cross-sectional areas of the right and left pulmonary arteries, indexed to body surface area. The normal Nakata pulmonary artery index (PAl) is 300 + / - 30 mm2/M z. We have defined pulmonary arteries as diminutive when the PAl is less than 150 mm2/M z. These angiographic assessments have a limitation: The size of the pulmonary arteries may be
Progress in Pediatric Cardiology
54
significantly larger after an increased blood flow and distending pressure produced by surgical right ventricular-to-pulmonary artery continuity. On the other hand, there is a small subset of patients in whom the central pulmonary arteries are so small-1 to 2 mm in diameter with PAI <100 ram2/ M 2 - that closure of the ventricular septal defect is clearly contraindicated. In addition to the preoperative identification of the presence and size of pulmonary arteries, it is critically important to demonstrate in detail the origin, course, and distribution of all APCAs. This usually requires selective angiographic injections into all direct and indirect APCAs to obtain the comp!ete map of the pulmonary circulation that is essential in planning optimal treatment strategies. i
;THERAPEUTIC CONSIDERATIONS Most patients with TOF-PA, and particularly those with a ductus-dependent pulmonary circulation and a PAI >150 mm2/M 2, can be successfully repaired with low operative risk and good late hemodynamic and electrophysiologic results. The therapeutic challenges are found in the subset of patients in whom the pulmonary arteries are diminutive with PAl <150 mmZ/Mzand in whom variable numbers of bronchopulmonary segments are supplied by APCAs. Hereafter, this discussion will be limited to the management of patients with TOF-PA who have diminutive pulmonary arteries. The ultimate therapeutic goal is to establish a right ventricular-dependent pulmonary circulation, ideally supplying all 20 bronchopulmonary segments. Hemodynamically, the postoperative right ventrical and left ventrical (RV/LV) systolic pressure ratio should be <0.6 with no residual left-to-right shunts and with little or no evidence of ventricular ectopic electrical activity (Lown <2). In patients with TOF-PA and diminutive pulmonary arteries, this optimal result is rarely achieved, mostly because of several surgical technical limitations, because of the complex variations of pulmonary artery anatomy, and, in our opinion, because of a delay in aggressively treating the pulmonary vascular components of this defect in early infancy. In the past, patients with TOF-PA and diminutive pulmonary arteries were often managed somewhat haphazardly, using a variety of medical or surgical
approaches. This management included primary repair or staged operations, such as preliminary systemic-to-pulmonary artery shunts, n'12 or the establishment of right ventricular-to-pulmonary artery continuity. 6n3n4 These procedures were primarily designed to provide relief of cyanosis and to stimulate enlargement of hypoplastic pulmonary arteries, with the expectation of a later, safer surgical closure of the ventricular septal defect and elimination of any remaining functionally important APCAs. A review revealed that medical management of patients with TOF-PA with diminutive pulmonary arteries was often inadequate, xs An initial high mortality (33%) was found in the few patients who had late repair, and almost all of the survivors had unsatisfactory results. Attempts at primary repair were also disappointing; seven of nine patients died, all from ventricular failure and low cardiac output. Of the two surviving patients, neither has had a satisfactory late outcome. Attempts at initial systemic-to-pulmonary artery shunts decreased the first stage operative mortality, but there were several late deaths before or during subsequent repair. By 1984 the Departments of Cardiac Surgery and Cardiology at The Children's Hospital in Boston demonstrated that hypoplastic and stenotic pulmonary arteries could be enlarged by transcatheter balloon dilation and that flow through APCAs could be interrupted by transcatheter placement of coils. ~6-~s Consequently, a new approach to the management of patients with TOF-PA and diminutive pulmonary arteries evolved in that institution, combining early surgical relief of right ventricular outflow tract obstruction without closure of the ventricular septal defect, followed by interventional catheterization to dilate peripheral pulmonary artery stenosis and to obstruct redundant aortopulmonary collaterals with coils. Thereafter, these preliminary procedures were followed by surgical repair of any residual right ventricular outflow tract obstruction and closure of the ventricular septal defect.
Intraoperative Control of APCAs The origin and course of all APCAs must be clearly outlined before surgery. In the majority of patients, the APCAs emerge from the posterior mediastihum, anterior to the left or right bronchus, to enter the appropriate hila. These vessels may be identified from a sternotomy approach and are looped
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
55
DAP c o l l a t e r a l s , L. t h o r a c o t o m y
FIGURE 4. An aortic or pulmonary artery valved homografl was interposed between the right ventricular outflow tract and the diminutive pulmonary arteries. A pericardial patch was used to augment the proximal anastomosis (insert). Most APCAs can be temporarily looped through a midline sternotomy. In a few instances (insert) if the origin of the APCAs is either from the distal descending thoracic aorta or if it courses behind the left or right bronchus, a lateral thoracotomy is necessary to temporarily or permanently interrupt these vessels.
before beginning cardiopulmonary bypass. We find it useful to dissect the area between the ascending aorta and the right superior vena cava, since the more important APCAs can be found in this area passing anteriorly to the right bronchus. In a few instances in which the origin of the APCAs is either from the distal descending thoracic aorta and/or the APCA courses behind the left or right bronchus, a preliminary thoracotomy is necessary to temporarily or permanently interrupt these vessels (Figure 4). Unifocalization procedures in 6 of 20 patients at The Children's Hospital were carried out after the first stage conduit interposition operation. By first interposing a conduit between the right ventricle and the pulmonary arteries, enlargement of these vessels is stimulated and access is provided for balloon dilation of peripheral pulmonary stenosis and for more accurate angiographic delineation of bronchopulmonary segmental distribution, an important guide to further unifocalization proce-
dures. Whenever an APCA is the end-artery to a significant area of the lung parenchyma, it should be detached from the aorta and anastomosed in an end-to-side fashion to the corresponding pulmonary artery, using a continuous 7-0 PDS suture (Figure 5). Of the six patients who had unifocalization surgery, postoperative catheterizations demonstrated patent anastomoses in all but one. In this patient, a direct anastomosis was not possible because of the distance between arteries, and this patient died after thrombosis of a Gore-Tex graft, placed in an attempt to bridge the distance.
TOF-PA with Either Discontinuous Diminutive Left and Right Pulmonary Arteries or Absent Mediastinal Pulmonary Arteries
In a few patients diminutive pulmonary arteries are present but discontinuous; even fewer patients have no mediastinal pulmonary arteries at all. In many of these patients a coalescence of vessels suit-
56
Progress in Pediatric Cardiology
VSD / "
TOF/PA, MAPC (PAl 50 mm21M 2)
RV-PA homograft and bilateral unifocalization
VSD closure (14 months)
FIGURE 5. Diminutive pulmonary arteries supplied only the right middle lobe, the left lingula, and the left upper lobe. APCAs supplied the fight upper lobe, the fight lower lobe, and the left lower lobe. During initial right ventficular-topulmonary artery (RV-PA) homograft interposition, the fight upper lobe and fight lower APCAs (MAPC) were detached from the aorta and connected endto-side to the fight pulmonary artery; the left lower lobe APCA was connected to the left pulmonary artery. Within 14 months the native pulmonary artery and the unifocalized collateral arteries had enlarged sufficiently to allow for successful closure of the ventricular septal defect.
able for anastomosis can be found at the hilum. First, a right thoracotomy is performed and a 4 mm Gore-Tex graft is interposed between the right subclavian artery and the hilar vascular confluence. In a second operation, usually during the same hospitalization, this procedure is repeated on the left side. The objectives are to unify left- and right-sided pulmonary blood supply through a controlled graft. Within 4-6 months, and after demonstrating an enlargement of the intraparenchymal branches, a larger 10-12 mm Gore-Tex graft is interposed between the right and left hilar pulmonary arteries (Figure 6). Then, through a midline sternotomy and on cardiopulmonary bypass, a valved-homograft is placed between this central Gore-Tex graft and the right ventricle. At the beginning of cardiopulmonary bypass, the left and right modified BlalockTaussig shunts are removed. The ventricular septal
defect is closed only if the peripheral pulmonary arteries have enlarged sufficiently. Otherwise, the ventricular septal defect is left open and closed during a third operation.
RESULTS From 1984 through August 1988, The Children's Hospital has treated 20 patients with TOF-PA and diminutive pulmonary arteries (PAI 10 mm2/M 2 to 150 mm2/M2)J s All patients were managed according to the strategies outlined here. Seven patients were younger than 9 months of age and four were neonates. In all 20 patients aortic or pulmonary cryopreserved valved homografts were placed "between the right ventricle and the junction of the right and left diminutive pulmonary arteries. Cardiopulmonary bypass and a short period of circula-
57
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
TOF/PA
_J
!
2 weeks
a
L 4 months
- 1 1 months ! VSD closure 1 8 months
FIGURE 6. In this patient there were no mediastinal pulmonary arteries. A t 2 weeks of age a 4 mm Gore-Tex shunt was placed between the right subclavian artery and the right hilum through a right thoracotomy. At 4 months of age the same operation was repeated on the left. After the intraparenchymal pulmonary branches became larger, both shunts were removed at II months; a I2 mm conduit was used to connect the right and left hilar pulmonary arteries, and an aortic valved homograft was placed between this central conduit and the right ventricular outflow tract. A t 18 months of age the ventricular septal defect was successfully closed.
tory arrest were used to achieve a bloodless and motionless field, ideal for constructing a necessarily meticulous distal anastomosis. During rewarming, anastomosis between the proximal homograft and the right ventricular anastomosis was accomplished using a glutaraldehyde pretreated pericardial patch to avoid proximal kinking of the homograft. Four of the twenty patients required a separate right lateral thoracotomy to control APCAs before beginning cardiopulmonary bypass. Six (35%) of the twenty patients died. Three patients (15%) died shortly after surgery, two died within 6 months of the operation, and one patient died one year later from a pulmonary artery aneurysm produced by balloon dilation. Of the re-
maining 14 patients, 12 have undergone closure of the ventricular septal defect with two deaths. Of the 10 survivors, seven patients have good hemodynamic results (proved by cardiac catheterization), one patient has residual right ventricular hypertension, and two patients have not yet been catheterized. The 10 survivors were alive at an average of 23 months after surgery. Seven of the ten surviving repaired patients had coil ernbolization of residual systemic collaterals and also underwent successful pulmonary artery dilation procedures. Of the two remaining unrepaired patients, one is not being considered for repair because of inadequate distal pulmonary arteries; the other patient awaits unifocalization surgery. Successful pulmonary artery
58
Progress in Pediatric Cardiology
growth was demonstrated in these patients, even in one with an initial PAI of 10 m m ' / M 2. The Children's Hospital has limited experience with the subset of TOF-PA patients with discontinuous and diminutive or absent mediastinal pulmonary arteries. Of five patients with absent mediastinal pulmonary arteries, four have survived, and in two of them the ventricular septal defect has been closed during a third operation.
DISCUSSION In patients with conventional TOF and ventricular-tq-pulmonary artery continuity, diminutive pulm6nary arteries are rare. The incidence of this complicating anatomy is <0.5%. However, in patients ilwith TOF-PA in whom pulmonary blood flow is mostly or exclusively dependent on aortopulmonary collaterals, diminutive pulmonary arteries are common. This most complex form of TOF-PA presents serious therapeutic challenges. Operative mortality and postoperative morbidity is high, and in the past, few of the surgical survivors have had adequate hemodynamic results. 19 Initial medical management without surgery has frequently been associated with the development of advanced pulmonary vascular obstructive disease (PVOD) in bronchopulmonary segments exposed to unobstructed APCA blood flow and with evidence of progressive narrowing of stenotic lesions within APCAs which were impossible to correct surgically and were resistant to balloon dilation. Moreover, there is also evidence that decreased pulmonary blood flow inhibits the development of pulmonary arterioles. Because of these secondary anatomic factors, most operations performed after 5 or 6 years of age have been disappointing. In this relatively older age group of TOF-PA patients, closure of the ventricular septal defect has commonly been associated with residual right ventricular and pulmonary arterial hypertension. Small pulmonary arteries can be enlarged by systemic-to-pulmonary artery shunts. 12 However, we have frequently observed significant iatrogenic damage to these small branch pulmonary arteries after a classical or modified Blalock-Taussig shunt has been created, and even more often after a Waterston shunt. These diminutive pulmonary arteries become easily kinked with shunt surgery, reducing or completely obstructing ipsilateral or contralat-
eral pulmonary blood flow. The surgical creation of continuity between the right ventricle and the pulmonary artery at an early age, leaving the ventricular septal defect open, provides for an antegrade and more balanced blood flow to both right and left pulmonary arteries. The use of cryopreserved valved homografts offer significant advantages over prosthetic grafts with the anatomosis to these small pulmonary arteries. This technique has led to important vessel expansion, even in neonates with initial arteries of only 1.5 mm in diameter. An additional advantage to establishing right ventricular-to-pulmonary artery continuity in early life is to provide access for catheter diagnostic and balloon dilation procedures. Balloon dilation of peripheral pulmonary stenoses is often necessary in these patients, and the precise identification of native pulmonary artery segmental distribution is best accomplished by selective angiographic injections directly into the distal pulmonary arteries. This staged and collaborative approach between cardiac surgeon and pediatric cardiologist also allows for a more rational selection of TOF-PA patients for final repair, based on more precise and complete physiologic and anatomic data. Any patient who develops a significant left-to-right ventricular septal defect shunt after the first stage operation must have sufficient antegrade flow through mediastinal pulmonary arteries to allow closure of the ventricular septal defect. In this circumstance preoperative measurements or calibrations of pulmonary artery size are much less important. The staged treatment plan presented here is based on three premises. 1. Increased blood flow increases the size of hypoplastic pulmonary arteries and stimulates development of distal pulmonary arteries. 2. These enhancing changes occur mostly in early life. 3. APCAs are unreliable sources of pulmonary blood flow resulting in pulmonary vascular obstructive disease, if they are unobstructed, and in unrepairable obstructions, if they are stenotic. 9 The combined, staged approach presented here is in an early phase of development in our institution. Several important questions remain.
Tetralogy of Fallot, Pulmonary Atresia, and Diminutive Pulmonary Arteries
1 . When are pulmonary arteries too small to allow for primary repair/ 2. Are valved conduits necessary; is a nonvalved conduit, permitting both systolic and diastolic flow, more effective in promoting enlargement of small pulmonary arteries/ 3. Is it possible to construct a conduit that will enlarge with time; will incorporation of a segment of autogenous vessel wall, as proved in experimental animals by Sawatari and associates, 2~ allow enlargement of conduits in humans7 4. How can protection of both the myocardium and the CNS be improved during these lengthy operations/ In the past we have been concerned about perioperative central nervous system complications in these patients, especially with the acute and chronic choreoathetosis seen in a few patients with large APCAs which were not controlled during surgery. We do not know the exact cause of these neurologic complications, but it is possible that they are the result of a cerebrovascular steal during cardiopulmonary bypass, depriving the most sensitive areas of the brain, such as the basal ganglia, of adequate blood flow. Awareness of this complication has led us to control all significant APCAs before starting cardiopulmonary bypass, even if this requires a separate thoracotomy. More effective dilation of stenotic or hypoplastic pulmonary arteries has improved with more experience and with new technical advances. Earlier complications of arterial rupture or aneurysms from balloon dilation are mostly preventable now, and the availability of balloon expandable stainless steel stents has extended the applicability of these techniques. 21 The authors are not ready to form final conclusions from their experience with this approach to the treatment of TOF-PA with diminutive pulmonary arteries. Only a small number of patients have had the staged and combined approach presented here, and the surgically important anatomic and physiologic variations of this defect are numerous. But there is encouragement from the establishment of a right ventricle-to-pulmonary artery continuity with a valved homograft in early infancy with subsequent pulmonary artery dilations and APCA embolizations that has led to successful second-stage
59
repairs in a number of patients. Providing central blood flow to diminutive pulmonary arteries produces a more predictable cross-sectional arterial enlargement and is not associated with lumenal distortion of the arteries. The conduit also provides a more reliable palliation, as judged by higher postoperative systemic oxygen saturations, probably because of an overall increase in pulmonary blood flow and a more effective and balanced distribution of blood flow into both lungs, minimizing unbalanced ventilation and perfusion. If this staged approach to treatment is begun in neonates or young infants, a more physiological development of pulmonary vascular and parenchyreal structures is possible. Ultimately, this should allow for more successful hemodynamic repair in a larger number of patients.
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9. McGoon DC, Baird DK, Davis GD: Surgical management of large bronchial collateral arteries with pulmonary stenosis or atresia. Circulation 1975; 52: 109-118. 10. Nakata S, Imai Y, Takanashi Y, et al: A new method for the quantitative standardization of crosssectional areas of the pulmonary arteries in congenital heart diseases with decreased pulmonary blood flow. ] Thorac Cardiovasc Surg 1984; 88:610-619. 11. Gill CC, Moodie DS, McGoon DC: Staged surgical management of pulmonary atresia with diminutive pulmonary arteries. ] Thorac Cardiovasc Surg 1977; 73:436-442. 12. Kirklin JW, Bargeron LM Jr, Pacifico AD: The enlargement of small pulmonary arteries by preh mmary palhatlve operations. Circulation 1977; 56: 612-617. 13. Millikan JS, Puga FJ, Danielson GK, et al: Staged surgical repair of pulmonary a tresia, ventricular septal defect; and hypoplastic, confluent pulmonary arteries. ] Thorac Cardiovasc Surg 1986; 91:818-825. 14. Olin CL, Ritter DG, McGoon DC, et al: Pulmonary atresia: Surgical considerations and results in 103 patients undergoing definitive repair. Circulation 1976; 54(suppl 1II):35-40. 15. Rome JJ, Mayer JE, Castaneda AR, et al: Tetralogy .t
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