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Tricuspid atresia
Tricuspid atresia A re-evaluation and classification Forty-five specimens of hearts with tricuspid atresia were studied and classified according to the nature of the great vessels and the ventricles. The new classification is a modification of the Edwards-Burchell classification of 1949 and takes recognition of modification by Keith and associates. According to the new classification, tricuspid atresia is divided into three types, namely, with normally related great vessels (Type 1), with transposed great vessels (Type Il], and with persistent truncus arteriosus (Type lJ/). Type lJ tricuspid atresia, characterized by transposed great vessels, is further subdivided into Subtype A, characterized by single subaortic conus, and Subtype B, characterized by both a subaortic and a subpulmonary COnus (double conus). When only a subaortic conus is present, the external relationship of the great vessels conforms to either d-transposition or l-transposition, Type 1 and each of the entities in Type lJ tricuspid atresia are further subdivided according to the presence or absence of obstruction to pulmonary blood flow. The new classification recognizes three variants, namely, l-transposition, double conus, and persistent truncus, as compared to the classification of 1949. Normally related great vessels were present in 56 per cent and transposed great vessels in 42 per cent of the cases. Anatomic features of obstruction to pulmonary blood flow were present in 60 per cent of all cases. Obstruction to pulmonary blood flow occurred in 84 per cent of specimens with normally related great vessels as compared to 32 per cent of specimens with transposed great vessels.
Rajendra Tandon, M.D., and Jesse E. Edwards, M.D., St. Paul and Minneapolis, Minn.
In a study of the anatomic features of hearts with tricuspid atresia, it became obvious that the morphologic features are more variable than has been described. The purpose of this study was to review the anatomic features of 45 specimens with tricuspid atresia available to us. As one result, the previously proposed classification of Edwards and Burchell! was modified and enlarged to include the various anatomic features of the ventricles and great vessels encountered in the present study. The study is also pertinent at this time because of the From the Departments of Pathology, United HospitalsMiller Division, St. Paul, Minn. 55102, and the University of Minnesota, Minneapolis, Minn. 55455. This study was supported by Public Health Service Research Grant 5 ROI HL05694 and Research Training Grant 5 TOI HL05570 from the National Heart and Lung Institute. Received for publication Oct. 26, 1973.
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recent attempts at corrective surgery in patients with tricuspid atresia.": " Forty-five specimens of right atrioventricular valvular atresia were available to us from the Cardiovascular Registry of the United Hospitals-Miller Division and the Department of Pathology of the University of Minnesota Hospitals. The ages of the patients ranged from 1 day to 33 years. Twenty-five specimens were from male and 18 from female patients. The exact age and sex of 2 patients was not known to us. Situs solitus of atria and viscera was present in all cases. The cardiac apex pointed toward the right in 3 cases. Definition of terms Tricuspid atresia. In the present communication, atresia of the right atrioventricular valve is termed tricuspid atresia. With
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ventricular inversion, the right atrioventricular valve may in fact be the mitral valve. However, in all our cases of ventricular inversion the patent atrioventricular valve appeared to be the mitral valve, leaving the atretic one as the tricuspid valve. Conus. The term conus is applied to a muscular cardiac segment intervening between the semilunar and the atrioventricular valves. It is characterized by lack of continuity between the mitral or tricuspid valves, on one hand, and a semilunar valve, on the other hand. Transposition of great vessels. The external relationship of the great vessels wherein the aorta is abnormally placed with respect to the pulmonary trunk is termed transposition of the great vessels. Under this broad designation, the relationship of the great vessels is variable. The aorta may be anterior and to the left of the pulmonary trunk, conforming to the relationship in corrected (or inverted) transposition of the great vessels (l-transposition) . The aorta may be anterior and to the right of the pulmonary trunk, displaying a relationship like that in complete or noninverted transposition of the great vessels (d-transposition) . Last, the aorta may lie to the right of the pulmonary trunk and either in the same frontal plane as the pulmonary trunk or slightly anterior to it. In the latter variety, the aorta and pulmonary trunk are parallel and their valves are at the same horizontal level. The first two types of relationships are also characterized by the presence of a subaortic conus, but the pulmonary valve is in continuity with the mitral valve. The latter variety has both a subaortic and a subpulmonary conus (double conus), resembling the great vessel-ventricular relationship seen in double-outlet right ventricle. .j
.j
Classification In classifying the 45 cases available to us, we made use of the fact that certain features are common to all cases of tricuspid atresia while other features result in differences between them. Those that are al-
ways present are (1) atresia of the right atrioventricular valve, (2) communication between the two atria, (3) a left atrioventricular valve, (4) a left-sided ventricle with hypertrophied walls and a large cavity, and (5) hypoplasia of the right-sided ventricle. The features which are variable are (1) the relationship of the great vessels and (2) the presence or absence of obstruction to pulmonary blood flow. Obstruction or free flow may be determined by the caliber of the communication between the two ventricles and by the state of the pulmonary valve. The new classification is an enlargement of the modification of the Edwards-Burchell classification proposed earlier." It incorporates the refinements regarding relationships between the great arteries and their relationship to the ventricular portion of the heart which we observed in our 45 specimens. According to the new classification, tricuspid atresia is divided into three main types: atresia with normally related great vessels (Type I), with transposed great vessels (Type II), and with persistent truncus arteriosus (Type III) (Table I). Type II tricuspid atresia (with transposition of the great vessels) is further subdivided into the form with a subaortic conus (Subtype A) and into that with both subaortic and subpulmonary coni (double conus) (Subtype B). When only a subaortic conus is present, it may occupy one of two positions. The conus may be normally placed, conforming in its position to that in complete (or noninverted) transposition of great vessels (d-transposition) (Group 1), or it may be inverted, conforming to that in corrected (inverted) transposition of the great vessels (I-transposition) . In each of the first two major types (Types I and II), regardless of other considerations, there may be subdivision according to the nature of the pathway leading to the pulmonary arterial system. Thus obstruction to pulmonary flow (atresia [Subgroup a] or stenosis [Subgroup b]) or absence of obstruction to pulmonary flow (Subgroup c) is an important subdivision of each entity.
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Table I. Classification of tricuspid atresia: 45 cases Classification
No. of cases
I. Normally related great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Type II. Transposition of great vessels Subtype A. Single conus Group 1. Noninverted great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Group 2. Inverted great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Subtype B. Double conus Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Type III. Persistent truncus arteriosus
25
Type
Description of entities Normally related great vessels (Type I). Normally related great vessels were present in 25 of the 45 cases of tricuspid atresia (55.5 per cent). In each, there was subpulmonary conus and absence of sub aortic conus so that mitral and aortic valve continuity was maintained. Obstruction to pulmonary blood flow was present in 21 of the 25 hearts with normally related great vessels. The site of obstruction to pulmonary blood flow was at the communication between the two ventricles, at the pulmonary valve level, or both. Pulmonary atresia (I a). Only 1 specimen showed the features of Subgroup a. This was characterized by atresia at the pulmonary valve as well as an intact ventricular septum (Fig. 1, a). The right ventricle was present as an endothelium-lined, slitlike, blind cavity to the right side of the anterior wall of the left ventricle. A patent ductus arteriosus was the source of pulmonary arterial flow
I
20 4
12
16
19
I
2 9 4
2
o
3
I
2
Pulmonary stenosis (Ib). Twenty specimens exhibited normally related great vessels and pulmonary stenosis. Nineteen of these were classical examples of the type generally recognized as Type Ib, while the twentieth case showed features of tetralogy of Fallot coexisting with tricuspid atresia. CLASSICAL CONDITION. In the 19 specimens with the classical features of Type Ib, the pulmonary stenosis was in a subpulmonary position and was represented by the narrow defect between the two ventricles. In these, the ventricular septal defect was in the muscular part of the septum at variable distance below the aortic valve (Fig. 1, b). The aorta thus arose entirely from the left ventricle. Of particular interest was I case in which there had been spontaneous closure of the ventricular septal defect. As the ductus arteriosus was found to be closed, no obvious channels for pulmonary arterial flow were identified. Pulmonary valvular stenosis, in addition,
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b.
Fig. 1. Diagrammatic portrayal of tricuspid atresia with normally related great vessels (Type I). a, Type la. Pulmonary atresia associated. The mitral valve (M.) leads into the large left ventricle (L. V.). The right ventricle (RY.) is represented by an endothelium-lined, blind slit. The patent ductus arteriosus (P.D.A.) runs between the aorta (A.) and the pulmonary trunk (P.T.) and represents the essential channel for delivery of blood to the lungs. b, Type lb. Small ventricular septal defect resulting in subpulmonary stenosis. The right ventricle is hypoplastic. c, Type Ib (atypical). Features of tetralogy of Fallot are associated with tricuspid atresia. d, Type Ie. Large ventricular septal defect is the characteristic feature. R.A., Right atrium. L.A., Left atrium.
was present in 3 cases. These were among 6 with bicuspid pulmonary valves and 1 with a unicuspid unicommissural valve. A left aortic arch was present in 17 of the 19 cases. One specimen had a right aortic arch and another a double aortic
arch. In the latter case, the left arch was hypoplastic whereas the right was enlarged. No examples of juxtaposition of the atrial appendages were found in this group. ASSOCIATED TETRALOGY OF FALLOT. The twentieth case of tricuspid atresia with nor-
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Fig. 2. Tricuspid atresia with d-transposition and single conus (Type IIA 1). a, Type IIA l a, Pulmonary valvular atresia associated. The subaortic conus (C.) represents the hypoplastic right ventricle communicating with the left ventricle through a ventricular septal defect. A., Ascending aorta. b, Type IIA lb. Subpulmonary stenosis associated. Pulmonary (P. V.) and mitral valvular continuity is present. c, Type IIA Ic, Absence of obstruction to pulmonary blood flow. For other abbreviations, see Fig. I.
mally related great vessels and subpulmonary stenosis also exhibited the features of tetralogy of Fallot. In this specimen, a wide subaortic ventricular septal defect was present and the aorta overrode the ventricular septum (Fig. 1, c). The right ventricle, though small, was of adequate size. The obstruction to pulmonary flow was the result of a narrow right ventricular outflow tract, as seen in tetralogy of Fallot, as well as a narrow dysplastic pulmonary valve. The aortic arch was on the left side and the atrial appendages were normally positioned. Absence of' obstruction to pulmonary flow (Ie). Each of the 4 cases belonging to Subgroup c had two ventricles communicating through a large ventricular septal defect. The sinus portion of the right ventricle was hypoplastic, while the outflow region was normal in size. The pulmonary trunk was wider than the aorta in 3 cases and the same width as the aorta in 1 case. The aorta arose entirely from the left ventri-
cle in each, and the aortic and mitral valves exhibited continuity (Fig. 1, d). In 1 of the specimens, left-sided juxtaposition of atrial appendages (both atrial appendages to the left of the great arteries) was present. Although the thoracic roentgenogram in this case showed the heart to be in the left hemithorax, the apex pointed toward the right. Transposition of great vessels (Type II). By definition, each of the 19 specimens belonging to Type II was characterized by abnormal relationship of the great vessels (transposition). These were subdivided according to the character of the outflow of the ventricular portion of the heart. There were 16 specimens with a single conus, which was subaortic in each instance, and 3 specimens with both subaortic and subpulmonary coni (double conus). Single (subaortic) conus (llA). In each of the 16 cases of transposition of the great vessels and a single (subaortic) conus, the ascending aorta and pulmonary trunk
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Table II. Obstructive anomalies in the 9 cases of tricuspid atresia with d-transposition of great vessels and absence of obstruction to pulmonary blood flow Systemic arterial obstructive anomalies
Cases 1 2 3 4 5
6 7 8
9 Legend:
Age 6 1 4 5
da. mo. da. da. 7 mo. Ph yr. 24 da. 6 yr. 4 da. + = present; 0
Coarctation oj aorta + + + +
0 0 0 0 0
Tubular hypoplasia of aortic arch + + + + +
0 0 0 0
lnterHypoplastic ruption of ascending aortic arch aorta 0 0 0 0 0 0
Valvular aortic stenosis
Subaortic stenosis
0 0 0
0 0 0
0
+
+ +
+ +
0 0 0 0
0 0
0 0
+
+
0 0
0 0
+
0
+
0
= absent.
ran parallel to each other with the aorta lying more anteriorly than the pulmonary trunk. This category was further divided according to whether the aorta lay to the right (noninverted, d-transposition-Group I) or to the left (inverted, I-transposition -Group II) of the pulmonary trunk. d-Transposition was present in 12 cases and I-transposition in 4. In each group, except when pulmonary atresia was present, there was continuity between the pulmonary and mitral valves. d-TRANSPOSITION (IIA 1). Among the 12 cases of d-transposition, there was variation in the nature of the tract that leads to the pulmonary trunk. In 1 case (Type IIA la), there was pulmonary atresia at the valve level (Fig. 2, a). A patent ductus provided a route for the flow of blood to the lungs. Pulmonary stenosis (Type IIA 1b) was present in two cases. In 1 instance, the pulmonary valve was tricuspid with a small annulus; in addition, there was muscular subpulmonary stenosis. In the other case, the pulmonary valve was dome-shaped and stenotic (Fig. 2, b). The former case showed left-sided juxtaposition of atrial appendages and the latter showed a cleft anterior leaflet of the mitral valve with evidence for mitral regurgitation. Lack of pulmonary stenosis (Type IIA lc) was exhibited by the remaining 9 of
the 12 specimens with d-transposition (Fig. 2, c). Seven of the 9 specimens had obstructive anomalies of the aorta or subaortic stenosis in various combinations (Table II). In 1 specimen there was interruption of the aortic arch, and in 4 others tubular hypoplasia and coarctation of the aorta were found. In another specimen, a segment of the aortic arch was atretic. Two specimens showed obstruction at the aortic valve. In 1 there was valvular stenosis, and in the other we found a narrow valvular ring associated with a hypoplastic ascending aorta. Four specimens exhibited subaortic stenosis. In 3 of these it was the result of a small ventricular septal defect, and in the fourth it resulted from a narrow tract connecting the left ventricle with the hypoplastic right ventricle. A nonstenotic bicuspid aortic valve was present in 1 of these specimens. In 7 of the 9 cases without pulmonary stenosis, the ductus arteriosus was patent. In each of the 6 in which this vessel was widely patent, one or more of the described obstructive anomalies of the aortic arch was present. The aortic arch was on the left side in 8 cases and on the right side in 1 case. Three specimens exhibited left-sided juxtaposition of atrial appendages, one being the heart with the right aortic arch.
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c. Fig. 3. Tricuspid atresia with I-transposition and single conus (Type IIA 2). a, Type IIA .2a. With pulmonary atresia. The aorta is anterior and to the left of the pulmonary trunk. The aorta arises from a conus of the left ventricle. The subaortic conus separates the mitral valve from the aortic valve (isolated bulbar inversion associated with I-transposition). The hypoplastic right ventricle lies below the atretic pulmonary valve. The cardiac apex points toward the right. In the I case observed, there was a right aortic arch with mirror-image branching. A patent ductus was present. b, Type IIA 2b. The stenotic pulmonary valve lies posterior to the aortic valve and is continuous with the mitral valve. The sub aortic conus represents the hypoplastic right ventricle, and its communication with the left ventricle is considered to be a muscular ventricular septal defect. c, Type IIA 2c. Absence of obstruction to pulmonary blood flow. Except for absence of obstruction to pulmonary flow and the presence of a right-sided apex in this case, the features are like those in b. d, Type IIA 2c. Absence of obstruction to pulmonary blood flow. The pulmonary trunk overrides the ventricular septum which separates the hypoplastic right ventricle from the left ventricle. The only inlet for the right ventricle is through the subpulmonary ventricular septal defect. The anatomic features indicate isolated bulbar inversion associated with I-transposition. Juxtaposition of the atrial appendages was present in this case. For abbreviations, see Fig. I.
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1-TRANSPOSITION (IIA 2). The external relationship of the great vessels in each of the 4 cases of I-transposition was as seen in corrected (inverted) transposition of the great vessels. The ascending aorta lay anterior and to the left of the pulmonary trunk. The right atrioventricular valve was atretic in each. The left atrioventricular valve exhibited the features of a mitral valve in each and opened into a large ventricular chamber. The sinus part of the chamber had the morphologic characteristics of a left ventricle. This ventricle occupied a leftsided position in the ventricular mass. The left atrioventricular valve was in continuity with the pulmonary valve in 3 cases. In the remaining case, the presence or absence of continuity could not be discerned because of pulmonary valvular atresia. With regard to the nature of the pulmonary arterial tract, 1 of the 4 specimens with I-transposition showed pulmonary atresia (Type IIA 2a), and another, pulmonary stenosis (Type IIA 2b). In two cases, no pulmonary arterial obstruction was present (Type IIA 2c). Since there were complexities with regard to the relationships between the great vessels and the ventricles in I-transposition, the specimens will be described in detail according to the subject of pulmonary stenosis. PULMONARY ATRESIA (IIA 2a). In the single case of pulmonary atresia and I-transposition, the obstruction was at the level of the pulmonary valve (Fig. 3, a). The cardiac apex pointed toward the right. The right and left atria were in situs solitus position and received the systemic and pulmonary veins normally. The right atrioventricular valve was atretic and the left showed the characteristics of a mitral valve. Whereas the inflow portion of the left-sided ventricular cavity showed the morphologic features of a left ventricle, the outflow region was like that of the morphologic right ventricle, and there was absence of left atrioventricular valve-aortic valve continuity. A small endothelium-lined, blind slit below the pulmonary valve was
considered to represent the right ventricle. The aortic arch was right sided. The right coronary artery arose from the right and the left coronary artery from the posterior aortic sinus. The anatomic diagnosis in this case was situs solitus of the viscera and of the atrial and ventricular sinuses, tricuspid atresia with isolated bulbar inversion, 1transposition of the great vessels, pulmonary atresia, and right aortic arch. PULMONARY STENOSIS (IIA 2b). In the 1 specimen of I-transposition with pulmonary stenosis, the right atrioventricular valve was atretic. The left atrioventricular valve showed the morphologic characteristics of a mitral valve, and the left-sided ventricular cavity exhibited the morphologic characteristics of a left ventricle. The base of the left ventricle was divided by a muscular ridge into a left anterior and a right posterior compartment. The aorta arose from the left anterior compartment and the pulmonary trunk from the right posterior compartment. Mitral and pulmonary valvular continuity was present, whereas the aortic valve was discontinuous with the mitral valve (Fig. 3, b). The right ventricle was represented by the subaortic conus. The ascending aorta swept to the left of the pulmonary trunk before continuing as the left aortic arch. The anatomic diagnosis in this case was tricuspid atresia, valvular pulmonary stenosis, isolated bulbar inversion, and l-transposition of the great vessels. ABSENCE OF PULMONARY STENOSIS (IIA 2c). There were 2 specimens with absence of obstruction to pulmonary blood flow and I-transposition. The atria were in situs solitus position, and the morphologic right and left ventricles were normally placed. The right atrioventricular valve was atretic, and the left exhibited the morphologic features of a mitral valve. The left ventricular cavity into which the mitral valve opened showed the features of a left ventricle. Mitral valve-pulmonary valve continuity was present in both. In 1 of the specimens, the pulmonary trunk arose from the left ventricle and the aorta from a conus of the
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Fig. 4. Tricuspid atresia with transposition and double conus (Type lIB). G, Type lIB b. Double conus and subpulmonary stenosis. Both great vessels arise from the left ventricle. The mitral valve is not in continuity with either of the semilunar valves. The latter lie at the same level. The right ventricle connects with the left through two muscular septal defects. b, Type lIB c. The aorta arises from the hypoplastic right ventricle while the pulmonary trunk arises from the left ventricle but is separated from the mitral valve by conal musculature. For abbreviations, see Fig. 1.
left ventricle, as in the specimen with l-transposition and pulmonary stenosis (Fig. 3, c). The cardiac apex pointed toward the right in this case. In the other specimen, the sinus portion of the right ventricle was well formed, though small. The pulmonary trunk overrode the ventricular septum, with the pulmonary valve forming the roof of a ventricular septal defect; the defect provided the only inlet for the right ventricle. The aorta arose from a conus of the left ventricle. The pulmonary and mitral valves were continuous (Fig. 3, d). Both atrial appendages lay to the left of the great vessels in this case. The anatomic diagnosis in the first case was tricuspid atresia, isolated bulbar inversion, and I-transposition of the great vessels. In the second case, the diagnosis was
tricuspid atresia, isolated bulbar inversion, l-transposition of the great vessels, biventricular pulmonary trunk, and left-sided juxtaposition of atrial appendages. Double (subaortic and subpulmonary) coni (lIB). The characteristic abnormality of the 3 specimens in this subgroup was the presence of a subaortic as well as a subpulmonary conus. In I case, both coni arose from the left ventricle while, in the other 2, each ventricle possessed a conus. In each, the aorta lay to the right of the pulmonary trunk. The aorta was in the same frontal plane as the pulmonary trunk in 1 specimen and slightly anterior to it in the other 2. The aortic and pulmonary valves were in the same horizontal plane. The right atrioventricular valve was atretic and the left showed the morphologic features of a mitral valve. There was no
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continuity between either semilunar valve and the left atrioventricular valve. The right ventricle was hypoplastic in all instances. One of the cases showed pulmonary stenosis, whereas 2 exhibited no obstruction to pulmonary flow. No examples of pulmonary atresia were present among the 3 specimens with double conus (lIB a). PULMONARY STENOSIS (lIB b). In the single specimen with pulmonary stenosis (lIB b), the pulmonary trunk and aorta each arose from a respective conus of the left ventricle (Fig. 4, a). There were two large muscular ventricular septal defects connecting the hypoplastic right ventricle with the left ventricle. The membranous ventricular septum was well formed and hung over the higher ventricular septal defect as a curtain. The basis for pulmonary stenosis was a combination of dysplasia of the tricuspid pulmonary valve and a membranous ring in the subpulmonary area. Both coronary arteries arose from the anterior aortic sinus. The anatomic diagnosis in this case was tricuspid atresia with double-outlet left ventricle, two muscular ventricular septal defects, and valvular and subvalvular pulmonary stenosis. ABSENCE OF PULMONARY STENOSIS (lIB c). In each of the 2 cases of double conus without pulmonary stenosis (lIB c), the aorta and the pulmonary trunk each arose from a conus-the aorta from the right ventricle and the pulmonary trunk from the left. The left atrioventricular valve showed the morphologic characteristics of a mitral valve and was not in continuity with either the aortic or the pulmonary valve (Fig. 4, b). A large ventricular septal defect provided communication between the two ventricles. The ventricular septal defect was subaortic in both cases. It was relatively narrow in I specimen and resulted in subaortic stenosis. There was an accessory orifice in the anterior leaflet of the mitral valve in this case. Jet lesions on the left atrial wall were associated. The anatomic diagnosis in both cases was tricuspid atresia with transposition of the great vessels and double conus.
Fig. 5. Tricuspid atresia with persistent truncus arteriosus. Both pulmonary arteries (R .P.A., L.P.A.) arise separately from the truncus arteriosus (T.A.) The truncus valve forms the roof of a ventricular septal defect, providing the only inlet for the right ventricle.
Persistent truncus arteriosus (Type III). Among the 45 cases of tricuspid atresia, I was associated with persistent truncus arteriosus. The right atrioventricular valve was atretic and the left showed the characteristics of a mitral valve. The mitral valve led into a large morphologic left ventricle. A ventricular septal defect was present in the outflow tract occupying the site of membranous and the anterior smooth septum. The roof of the ventricular septal defect was formed by the truncus valve which arose from both ventricles. The truncus valve with three cusps was in continuity with the mitral valve (Fig. 5). The right ventricle was present as a small cavity and communicated with the left ventricle through the ventricular septal defect. The first set of branches from the truncus was represented by the two coronary arteries. These were followed by the two pulmonary arteries arising separately, one above the other. The right pulmonary artery arose 8
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mm. and the left pulmonary artery 14 mm. above the truncus valve. Thus, the truncus arteriosus was of Type II according to the classification of Collett and Edwards." Associated anomalies. The foregoing material reviewed some of the anomalies that are associated with tricuspid atresia, excluding variations in ventricular structure and relations with great vessels. Associated anomalies and others not mentioned are summarized for convenience. Anomalies of the aortic arch system. RIGHT AORTIC ARCH WITH MIRROR-IMAGE BRANCHING. A right aortic arch with mirrorimage branching was present in 3 of the 45 cases. In 1 case each, the great vessels showed normal relationship (Ib ), d-transposition (IIA lc) , and l-transposition (IIA 2a). DOUBLE AORTIC ARCH. Double aortic arch was found in 1 case. This showed normally related great vessels (Ib). OBSTRUCTIVE ANOMALIES OF THE ARCH. Tubular hypoplasia of the aortic arch, coarctation, interruption, and atresia of the arch were present only in the group with dtransposition of the great vessels and have been covered in the main body of the paper (Table II). Pulmonary atresia. Pulmonary atresia of some type was observed in 4 cases. In 3 of these, the atresia was at the level of the pulmonary valve. It occurred once among each of the following types of tricuspid atresia: with normally related great vessels, with d-.. transposition, and with l-transposition. A patent ductus arteriosus provided the pulmonary blood flow in each case. In the fourth case, the "pulmonary atresia" was unusual in type. It resulted from spontaneous closure of the ventricular septal defect. The consequence was complete obstruction to pulmonary blood flow. The great vessels were normally related in this case (Ib) and the ductus arteriosus had closed spontaneously. Unusual communications between the atria. In 43 of the 45 specimens the communication between the two atria was at the fossa ovalis. In some of these, the com-
munication was represented by a valvular competent patent foramen ovale, while in others an atrial septal defect resulted from valvular incompetence of the foramen ovale. In 1 of the 2 remaining specimens, an ostium primum type of atrial septal defect was present, and in the other the atrial septum was intact. In the latter case, the coronary sinus communicated with both atria and was the only route through which the right atrial blood could reach the left atrium." Juxtaposition of atrial appendages. Juxtaposition of atrial appendages was observed in 6 cases. In each, both atrial appendages lay to the left of the great vessels. The great vessels were normally related in 1 case, exhibited d-transposition in 4, and I-transposition in the sixth. Comments In 1906, Kuhne 7 classified tricuspid atresia into those cases associated with transposition of great vessels and those without associated transposition of great vessels. Based on Kuhne's observations, a clinicopathological classification was proposed in 1949 by Edwards and Burchell' and later modified by Edwards." It included the recognition of two types of great vessel relationships-normal or transposed-and of the basic clinical patterns resulting from the presence or absence of obstruction to pulmonary blood flow. Keith, Rowe, and Vlad" reviewed 143 specimens of tricuspid atresia of which 92 were from the literature. They modified the classification of Edwards and Burchell to include l-transposition (inverted transposition) of the great vessels, a condition seen in 4 of the 143 specimens they reviewed. Those authors referred to this form as Type III tricuspid atresia and restricted d-transposi tion (noninverted) to Type II. In the classification here presented, we adhere basically to that of Edwards and Burchell, while accepting the modification of Keith and associates in dividing transposition into d- and 1- types. This classification adds the recognition of double conus and persistent truncus arteriosus in association with tricuspid atresia.
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The incidence of transposition in our series was somewhat higher than that in the series reviewed by Keith (42 per cent in this series; 30 per cent in Keith's). To our knowledge, no other case of persistent truncus arteriosus with tricuspid atresia, as seen in 1 of our cases, has previously been reported. When transposition was associated with a single conus, the more common type was d-transposition, the less common, l-transposition (ratio 3:1). Our studies indicate that, in tricuspid atresia with obstruction to pulmonary blood flow, normally related great vessels are more common than transposition, whereas, in the absence of obstruction to pulmonary blood flow, some type of transposition of the great vessels is more frequent than normally related great vessels. Among our various groups of tricuspid atresia, 27 of 45 cases (60 per cent) showed obstruction to pulmonary blood flow, whereas in 18 specimens (40 per cent) there was no obstruction to pulmonary blood flow. Of the 27 specimens with obstruction to pulmonary blood flow, 21 cases (78 per cent) showed normally related great vessels, while 6 cases (22 per cent) exhibited transposition of the great vessels. On the other hand, of the 18 specimens without obstruction to pulmonary blood flow, 13 (72 per cent) showed transposition of the great vessels, 4 (22 per cent) exhibited normally related great vessels, and 1 specimen (6 per cent) had persistent truncus. When the great vessels were normally related, obstruction to pulmonary flow was common (21 of 25 cases; 84 per cent). When they were transposed, obstruction to pulmonary flow was less common (6 of 19 cases; 32 per cent). In instances of single conus and transposition, obstruction to pulmonary flow was less common in d-transposition (3 of 12 cases; 25 per cent) than in l-transposition (2 of 4 cases; 50 per cent). Although in our series the number of cases of double conus is small, obstruction to pulmonary flow was less common than
54 1
absence of this condition (l case of pulmonary stenosis among 3). Obstruction to systemic arterial flow was seen in 7 of the 45 cases of tricuspid atresia. Each was associated with transposed great vessels. The obstruction was more frequently extracardiac (aortic) than intracardiac, but in some cases both were present together. We did not observe aortic obstruction in any of our cases in which the great vessels were normally related. We are, however, aware of 1 reported case of tricuspid atresia and normally related great vessels in which coarctation of the aorta was present." Pulmonary stenosis was absent in that case. Of particular interest, from a developmental viewpoint, are our 4 cases of l-transposition. For discussion, these cases might be considered to be examples of "corrected transposition with mitral atresia." If this were so, the main ventricle would be expected to be the anatomic right ventricle and the atretic valve a right-sided mitral valve; yet the internal features of the hearts did not support such a concept, as the main ventricle showed the characteristics of a left ventricle and the intact valve those of a mitral valve. These cases, therefore, are considered to be examples of bulbar inversion without inversion of the ventricular sinuses." Theoretically, further variability in the group represented by the only case of persistent truncus arteriosus is possible. In our specimen, the truncus arteriosus was of Type II according to the classification of Collett and Edwards. G In a study of the literature, we did not find any reported cases of persistent truncus arteriosus associated with tricuspid atresia.
Addendum Since the completion of this study, 2 cases have been added to our collection. Since both provide additional features of interest, we would like to summarize them. In I case reported by MarinGarcia and associates.t- the tricuspid atresia was associated with normally related great vessels, intact ventricular septum, patent ductus arteriosus, and absence of the pulmonary valve. The other
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case was characterized by tricuspid atresia, normally related great vessels, pulmonary stenosis, and absence of the atrial septum (common atrium). REFERENCES
2 3
4
5
6
Edwards, 1. E., and Burchell, H. B.: Congenital Tricuspid Atresia: A Classification, Med. Clin. North Am. 33: 1177, 1949. Fontan, F., and Baudet, E.: Surgical Repairs of Tricuspid Atresia, Thorax 26: 240, 1971. Stanford, W., Armstrong, R. G., Cline, R. E., and King, T. D.: Right Atrium-Pulmonary Artery Allograft for Correction of Tricuspid Atresia, I. THORAC. CARDIOVASC. SURG. 66: 105, 1973. Van Praagh, R., and Vlad, P.: Transposition of the great arteries, in Keith, I. D., Rowe, R. D., and Vlad, P., editors: Heart Disease in Infancy and Childhood, ed. 2, New York, 1967, Macmillan Publishing Co., Inc. Edwards, I. E.: Congenital Malformations of the Heart and Great Vessels. C. Malformation of the Valves, in Gould, S. E., editor: Pathology of the Heart and Blood Vessels, ed. 3, Springfield, III., 1968, Charles C Thomas, Publisher, p. 313. Collett, R. W., and Edwards, I. E.: Persistent
7 8
9
10 11
12
Truncus Arteriosus: A Classification According to Anatomic Types, Surg. Clin. North Am. 33: 1245, 1949. KUhne, M.: Uber zwei Faile kongenitaler Atresie des Ostium venosum dextrum, 1ahrb. Kinderh. 63: 235, 1906. Keith, 1. D., Rowe, R. D., and Vlad, P.: Tricuspid Atresia, in Keith, I. D., Rowe, R. D., and Vlad, P., editors: Heart Disease in Infancy and Childhood, ed. 2, New York, 1967, Macmillan Publishing Co., Inc., p. 644. Chiche, P.: Etude anatomique et clinique des atresies tricuspidiennes, Arch. Mal. Coeur 44: 981, 1952. Raghib, G., Anderson, R. c., and Edwards, 1. E.: Isolated Bulbar Inversion in Corrected Transposition, Am. 1. Cardiol. 17: 407, 1966. Rose, A. G., Beckman, C. B., and Edwards, 1. E.: Communication Between the Coronary Sinus and the Left Atrium, Br. Heart 1. In press. Marin-Garcia, I., Roca, 1., Blieden, L. c., Lucus, R. V., Ir., and Edwards, I. E.: Congenital Absence of the Pulmonary Valve Associated With Tricuspid' Atresia and Intact Ventricular Septum, Chest 64: 658, 1973.
Rajendra Tandon, M.D., and Jesse E. Edwards, M.D., St. Paul and Minneapolis, Minn.
In a study of the anatomic features of hearts with tricuspid atresia, it became obvious that the morphologic features are more variable than has been described. The purpose of this study was to review the anatomic features of 45 specimens with tricuspid atresia available to us. As one result, the previously proposed classification of Edwards and Burchell! was modified and enlarged to include the various anatomic features of the ventricles and great vessels encountered in the present study. The study is also pertinent at this time because of the From the Departments of Pathology, United HospitalsMiller Division, St. Paul, Minn. 55102, and the University of Minnesota, Minneapolis, Minn. 55455. This study was supported by Public Health Service Research Grant 5 ROI HL05694 and Research Training Grant 5 TOI HL05570 from the National Heart and Lung Institute. Received for publication Oct. 26, 1973.
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recent attempts at corrective surgery in patients with tricuspid atresia.": " Forty-five specimens of right atrioventricular valvular atresia were available to us from the Cardiovascular Registry of the United Hospitals-Miller Division and the Department of Pathology of the University of Minnesota Hospitals. The ages of the patients ranged from 1 day to 33 years. Twenty-five specimens were from male and 18 from female patients. The exact age and sex of 2 patients was not known to us. Situs solitus of atria and viscera was present in all cases. The cardiac apex pointed toward the right in 3 cases. Definition of terms Tricuspid atresia. In the present communication, atresia of the right atrioventricular valve is termed tricuspid atresia. With
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ventricular inversion, the right atrioventricular valve may in fact be the mitral valve. However, in all our cases of ventricular inversion the patent atrioventricular valve appeared to be the mitral valve, leaving the atretic one as the tricuspid valve. Conus. The term conus is applied to a muscular cardiac segment intervening between the semilunar and the atrioventricular valves. It is characterized by lack of continuity between the mitral or tricuspid valves, on one hand, and a semilunar valve, on the other hand. Transposition of great vessels. The external relationship of the great vessels wherein the aorta is abnormally placed with respect to the pulmonary trunk is termed transposition of the great vessels. Under this broad designation, the relationship of the great vessels is variable. The aorta may be anterior and to the left of the pulmonary trunk, conforming to the relationship in corrected (or inverted) transposition of the great vessels (l-transposition) . The aorta may be anterior and to the right of the pulmonary trunk, displaying a relationship like that in complete or noninverted transposition of the great vessels (d-transposition) . Last, the aorta may lie to the right of the pulmonary trunk and either in the same frontal plane as the pulmonary trunk or slightly anterior to it. In the latter variety, the aorta and pulmonary trunk are parallel and their valves are at the same horizontal level. The first two types of relationships are also characterized by the presence of a subaortic conus, but the pulmonary valve is in continuity with the mitral valve. The latter variety has both a subaortic and a subpulmonary conus (double conus), resembling the great vessel-ventricular relationship seen in double-outlet right ventricle. .j
.j
Classification In classifying the 45 cases available to us, we made use of the fact that certain features are common to all cases of tricuspid atresia while other features result in differences between them. Those that are al-
ways present are (1) atresia of the right atrioventricular valve, (2) communication between the two atria, (3) a left atrioventricular valve, (4) a left-sided ventricle with hypertrophied walls and a large cavity, and (5) hypoplasia of the right-sided ventricle. The features which are variable are (1) the relationship of the great vessels and (2) the presence or absence of obstruction to pulmonary blood flow. Obstruction or free flow may be determined by the caliber of the communication between the two ventricles and by the state of the pulmonary valve. The new classification is an enlargement of the modification of the Edwards-Burchell classification proposed earlier." It incorporates the refinements regarding relationships between the great arteries and their relationship to the ventricular portion of the heart which we observed in our 45 specimens. According to the new classification, tricuspid atresia is divided into three main types: atresia with normally related great vessels (Type I), with transposed great vessels (Type II), and with persistent truncus arteriosus (Type III) (Table I). Type II tricuspid atresia (with transposition of the great vessels) is further subdivided into the form with a subaortic conus (Subtype A) and into that with both subaortic and subpulmonary coni (double conus) (Subtype B). When only a subaortic conus is present, it may occupy one of two positions. The conus may be normally placed, conforming in its position to that in complete (or noninverted) transposition of great vessels (d-transposition) (Group 1), or it may be inverted, conforming to that in corrected (inverted) transposition of the great vessels (I-transposition) . In each of the first two major types (Types I and II), regardless of other considerations, there may be subdivision according to the nature of the pathway leading to the pulmonary arterial system. Thus obstruction to pulmonary flow (atresia [Subgroup a] or stenosis [Subgroup b]) or absence of obstruction to pulmonary flow (Subgroup c) is an important subdivision of each entity.
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Table I. Classification of tricuspid atresia: 45 cases Classification
No. of cases
I. Normally related great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Type II. Transposition of great vessels Subtype A. Single conus Group 1. Noninverted great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Group 2. Inverted great vessels Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Subtype B. Double conus Subgroup a. With pulmonary atresia Subgroup b. With pulmonary or subpulmonary stenosis Subgroup c. Absence of pulmonary or subpulmonary stenosis Type III. Persistent truncus arteriosus
25
Type
Description of entities Normally related great vessels (Type I). Normally related great vessels were present in 25 of the 45 cases of tricuspid atresia (55.5 per cent). In each, there was subpulmonary conus and absence of sub aortic conus so that mitral and aortic valve continuity was maintained. Obstruction to pulmonary blood flow was present in 21 of the 25 hearts with normally related great vessels. The site of obstruction to pulmonary blood flow was at the communication between the two ventricles, at the pulmonary valve level, or both. Pulmonary atresia (I a). Only 1 specimen showed the features of Subgroup a. This was characterized by atresia at the pulmonary valve as well as an intact ventricular septum (Fig. 1, a). The right ventricle was present as an endothelium-lined, slitlike, blind cavity to the right side of the anterior wall of the left ventricle. A patent ductus arteriosus was the source of pulmonary arterial flow
I
20 4
12
16
19
I
2 9 4
2
o
3
I
2
Pulmonary stenosis (Ib). Twenty specimens exhibited normally related great vessels and pulmonary stenosis. Nineteen of these were classical examples of the type generally recognized as Type Ib, while the twentieth case showed features of tetralogy of Fallot coexisting with tricuspid atresia. CLASSICAL CONDITION. In the 19 specimens with the classical features of Type Ib, the pulmonary stenosis was in a subpulmonary position and was represented by the narrow defect between the two ventricles. In these, the ventricular septal defect was in the muscular part of the septum at variable distance below the aortic valve (Fig. 1, b). The aorta thus arose entirely from the left ventricle. Of particular interest was I case in which there had been spontaneous closure of the ventricular septal defect. As the ductus arteriosus was found to be closed, no obvious channels for pulmonary arterial flow were identified. Pulmonary valvular stenosis, in addition,
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b.
Fig. 1. Diagrammatic portrayal of tricuspid atresia with normally related great vessels (Type I). a, Type la. Pulmonary atresia associated. The mitral valve (M.) leads into the large left ventricle (L. V.). The right ventricle (RY.) is represented by an endothelium-lined, blind slit. The patent ductus arteriosus (P.D.A.) runs between the aorta (A.) and the pulmonary trunk (P.T.) and represents the essential channel for delivery of blood to the lungs. b, Type lb. Small ventricular septal defect resulting in subpulmonary stenosis. The right ventricle is hypoplastic. c, Type Ib (atypical). Features of tetralogy of Fallot are associated with tricuspid atresia. d, Type Ie. Large ventricular septal defect is the characteristic feature. R.A., Right atrium. L.A., Left atrium.
was present in 3 cases. These were among 6 with bicuspid pulmonary valves and 1 with a unicuspid unicommissural valve. A left aortic arch was present in 17 of the 19 cases. One specimen had a right aortic arch and another a double aortic
arch. In the latter case, the left arch was hypoplastic whereas the right was enlarged. No examples of juxtaposition of the atrial appendages were found in this group. ASSOCIATED TETRALOGY OF FALLOT. The twentieth case of tricuspid atresia with nor-
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Fig. 2. Tricuspid atresia with d-transposition and single conus (Type IIA 1). a, Type IIA l a, Pulmonary valvular atresia associated. The subaortic conus (C.) represents the hypoplastic right ventricle communicating with the left ventricle through a ventricular septal defect. A., Ascending aorta. b, Type IIA lb. Subpulmonary stenosis associated. Pulmonary (P. V.) and mitral valvular continuity is present. c, Type IIA Ic, Absence of obstruction to pulmonary blood flow. For other abbreviations, see Fig. I.
mally related great vessels and subpulmonary stenosis also exhibited the features of tetralogy of Fallot. In this specimen, a wide subaortic ventricular septal defect was present and the aorta overrode the ventricular septum (Fig. 1, c). The right ventricle, though small, was of adequate size. The obstruction to pulmonary flow was the result of a narrow right ventricular outflow tract, as seen in tetralogy of Fallot, as well as a narrow dysplastic pulmonary valve. The aortic arch was on the left side and the atrial appendages were normally positioned. Absence of' obstruction to pulmonary flow (Ie). Each of the 4 cases belonging to Subgroup c had two ventricles communicating through a large ventricular septal defect. The sinus portion of the right ventricle was hypoplastic, while the outflow region was normal in size. The pulmonary trunk was wider than the aorta in 3 cases and the same width as the aorta in 1 case. The aorta arose entirely from the left ventri-
cle in each, and the aortic and mitral valves exhibited continuity (Fig. 1, d). In 1 of the specimens, left-sided juxtaposition of atrial appendages (both atrial appendages to the left of the great arteries) was present. Although the thoracic roentgenogram in this case showed the heart to be in the left hemithorax, the apex pointed toward the right. Transposition of great vessels (Type II). By definition, each of the 19 specimens belonging to Type II was characterized by abnormal relationship of the great vessels (transposition). These were subdivided according to the character of the outflow of the ventricular portion of the heart. There were 16 specimens with a single conus, which was subaortic in each instance, and 3 specimens with both subaortic and subpulmonary coni (double conus). Single (subaortic) conus (llA). In each of the 16 cases of transposition of the great vessels and a single (subaortic) conus, the ascending aorta and pulmonary trunk
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Table II. Obstructive anomalies in the 9 cases of tricuspid atresia with d-transposition of great vessels and absence of obstruction to pulmonary blood flow Systemic arterial obstructive anomalies
Cases 1 2 3 4 5
6 7 8
9 Legend:
Age 6 1 4 5
da. mo. da. da. 7 mo. Ph yr. 24 da. 6 yr. 4 da. + = present; 0
Coarctation oj aorta + + + +
0 0 0 0 0
Tubular hypoplasia of aortic arch + + + + +
0 0 0 0
lnterHypoplastic ruption of ascending aortic arch aorta 0 0 0 0 0 0
Valvular aortic stenosis
Subaortic stenosis
0 0 0
0 0 0
0
+
+ +
+ +
0 0 0 0
0 0
0 0
+
+
0 0
0 0
+
0
+
0
= absent.
ran parallel to each other with the aorta lying more anteriorly than the pulmonary trunk. This category was further divided according to whether the aorta lay to the right (noninverted, d-transposition-Group I) or to the left (inverted, I-transposition -Group II) of the pulmonary trunk. d-Transposition was present in 12 cases and I-transposition in 4. In each group, except when pulmonary atresia was present, there was continuity between the pulmonary and mitral valves. d-TRANSPOSITION (IIA 1). Among the 12 cases of d-transposition, there was variation in the nature of the tract that leads to the pulmonary trunk. In 1 case (Type IIA la), there was pulmonary atresia at the valve level (Fig. 2, a). A patent ductus provided a route for the flow of blood to the lungs. Pulmonary stenosis (Type IIA 1b) was present in two cases. In 1 instance, the pulmonary valve was tricuspid with a small annulus; in addition, there was muscular subpulmonary stenosis. In the other case, the pulmonary valve was dome-shaped and stenotic (Fig. 2, b). The former case showed left-sided juxtaposition of atrial appendages and the latter showed a cleft anterior leaflet of the mitral valve with evidence for mitral regurgitation. Lack of pulmonary stenosis (Type IIA lc) was exhibited by the remaining 9 of
the 12 specimens with d-transposition (Fig. 2, c). Seven of the 9 specimens had obstructive anomalies of the aorta or subaortic stenosis in various combinations (Table II). In 1 specimen there was interruption of the aortic arch, and in 4 others tubular hypoplasia and coarctation of the aorta were found. In another specimen, a segment of the aortic arch was atretic. Two specimens showed obstruction at the aortic valve. In 1 there was valvular stenosis, and in the other we found a narrow valvular ring associated with a hypoplastic ascending aorta. Four specimens exhibited subaortic stenosis. In 3 of these it was the result of a small ventricular septal defect, and in the fourth it resulted from a narrow tract connecting the left ventricle with the hypoplastic right ventricle. A nonstenotic bicuspid aortic valve was present in 1 of these specimens. In 7 of the 9 cases without pulmonary stenosis, the ductus arteriosus was patent. In each of the 6 in which this vessel was widely patent, one or more of the described obstructive anomalies of the aortic arch was present. The aortic arch was on the left side in 8 cases and on the right side in 1 case. Three specimens exhibited left-sided juxtaposition of atrial appendages, one being the heart with the right aortic arch.
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c. Fig. 3. Tricuspid atresia with I-transposition and single conus (Type IIA 2). a, Type IIA .2a. With pulmonary atresia. The aorta is anterior and to the left of the pulmonary trunk. The aorta arises from a conus of the left ventricle. The subaortic conus separates the mitral valve from the aortic valve (isolated bulbar inversion associated with I-transposition). The hypoplastic right ventricle lies below the atretic pulmonary valve. The cardiac apex points toward the right. In the I case observed, there was a right aortic arch with mirror-image branching. A patent ductus was present. b, Type IIA 2b. The stenotic pulmonary valve lies posterior to the aortic valve and is continuous with the mitral valve. The sub aortic conus represents the hypoplastic right ventricle, and its communication with the left ventricle is considered to be a muscular ventricular septal defect. c, Type IIA 2c. Absence of obstruction to pulmonary blood flow. Except for absence of obstruction to pulmonary flow and the presence of a right-sided apex in this case, the features are like those in b. d, Type IIA 2c. Absence of obstruction to pulmonary blood flow. The pulmonary trunk overrides the ventricular septum which separates the hypoplastic right ventricle from the left ventricle. The only inlet for the right ventricle is through the subpulmonary ventricular septal defect. The anatomic features indicate isolated bulbar inversion associated with I-transposition. Juxtaposition of the atrial appendages was present in this case. For abbreviations, see Fig. I.
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1-TRANSPOSITION (IIA 2). The external relationship of the great vessels in each of the 4 cases of I-transposition was as seen in corrected (inverted) transposition of the great vessels. The ascending aorta lay anterior and to the left of the pulmonary trunk. The right atrioventricular valve was atretic in each. The left atrioventricular valve exhibited the features of a mitral valve in each and opened into a large ventricular chamber. The sinus part of the chamber had the morphologic characteristics of a left ventricle. This ventricle occupied a leftsided position in the ventricular mass. The left atrioventricular valve was in continuity with the pulmonary valve in 3 cases. In the remaining case, the presence or absence of continuity could not be discerned because of pulmonary valvular atresia. With regard to the nature of the pulmonary arterial tract, 1 of the 4 specimens with I-transposition showed pulmonary atresia (Type IIA 2a), and another, pulmonary stenosis (Type IIA 2b). In two cases, no pulmonary arterial obstruction was present (Type IIA 2c). Since there were complexities with regard to the relationships between the great vessels and the ventricles in I-transposition, the specimens will be described in detail according to the subject of pulmonary stenosis. PULMONARY ATRESIA (IIA 2a). In the single case of pulmonary atresia and I-transposition, the obstruction was at the level of the pulmonary valve (Fig. 3, a). The cardiac apex pointed toward the right. The right and left atria were in situs solitus position and received the systemic and pulmonary veins normally. The right atrioventricular valve was atretic and the left showed the characteristics of a mitral valve. Whereas the inflow portion of the left-sided ventricular cavity showed the morphologic features of a left ventricle, the outflow region was like that of the morphologic right ventricle, and there was absence of left atrioventricular valve-aortic valve continuity. A small endothelium-lined, blind slit below the pulmonary valve was
considered to represent the right ventricle. The aortic arch was right sided. The right coronary artery arose from the right and the left coronary artery from the posterior aortic sinus. The anatomic diagnosis in this case was situs solitus of the viscera and of the atrial and ventricular sinuses, tricuspid atresia with isolated bulbar inversion, 1transposition of the great vessels, pulmonary atresia, and right aortic arch. PULMONARY STENOSIS (IIA 2b). In the 1 specimen of I-transposition with pulmonary stenosis, the right atrioventricular valve was atretic. The left atrioventricular valve showed the morphologic characteristics of a mitral valve, and the left-sided ventricular cavity exhibited the morphologic characteristics of a left ventricle. The base of the left ventricle was divided by a muscular ridge into a left anterior and a right posterior compartment. The aorta arose from the left anterior compartment and the pulmonary trunk from the right posterior compartment. Mitral and pulmonary valvular continuity was present, whereas the aortic valve was discontinuous with the mitral valve (Fig. 3, b). The right ventricle was represented by the subaortic conus. The ascending aorta swept to the left of the pulmonary trunk before continuing as the left aortic arch. The anatomic diagnosis in this case was tricuspid atresia, valvular pulmonary stenosis, isolated bulbar inversion, and l-transposition of the great vessels. ABSENCE OF PULMONARY STENOSIS (IIA 2c). There were 2 specimens with absence of obstruction to pulmonary blood flow and I-transposition. The atria were in situs solitus position, and the morphologic right and left ventricles were normally placed. The right atrioventricular valve was atretic, and the left exhibited the morphologic features of a mitral valve. The left ventricular cavity into which the mitral valve opened showed the features of a left ventricle. Mitral valve-pulmonary valve continuity was present in both. In 1 of the specimens, the pulmonary trunk arose from the left ventricle and the aorta from a conus of the
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Fig. 4. Tricuspid atresia with transposition and double conus (Type lIB). G, Type lIB b. Double conus and subpulmonary stenosis. Both great vessels arise from the left ventricle. The mitral valve is not in continuity with either of the semilunar valves. The latter lie at the same level. The right ventricle connects with the left through two muscular septal defects. b, Type lIB c. The aorta arises from the hypoplastic right ventricle while the pulmonary trunk arises from the left ventricle but is separated from the mitral valve by conal musculature. For abbreviations, see Fig. 1.
left ventricle, as in the specimen with l-transposition and pulmonary stenosis (Fig. 3, c). The cardiac apex pointed toward the right in this case. In the other specimen, the sinus portion of the right ventricle was well formed, though small. The pulmonary trunk overrode the ventricular septum, with the pulmonary valve forming the roof of a ventricular septal defect; the defect provided the only inlet for the right ventricle. The aorta arose from a conus of the left ventricle. The pulmonary and mitral valves were continuous (Fig. 3, d). Both atrial appendages lay to the left of the great vessels in this case. The anatomic diagnosis in the first case was tricuspid atresia, isolated bulbar inversion, and I-transposition of the great vessels. In the second case, the diagnosis was
tricuspid atresia, isolated bulbar inversion, l-transposition of the great vessels, biventricular pulmonary trunk, and left-sided juxtaposition of atrial appendages. Double (subaortic and subpulmonary) coni (lIB). The characteristic abnormality of the 3 specimens in this subgroup was the presence of a subaortic as well as a subpulmonary conus. In I case, both coni arose from the left ventricle while, in the other 2, each ventricle possessed a conus. In each, the aorta lay to the right of the pulmonary trunk. The aorta was in the same frontal plane as the pulmonary trunk in 1 specimen and slightly anterior to it in the other 2. The aortic and pulmonary valves were in the same horizontal plane. The right atrioventricular valve was atretic and the left showed the morphologic features of a mitral valve. There was no
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continuity between either semilunar valve and the left atrioventricular valve. The right ventricle was hypoplastic in all instances. One of the cases showed pulmonary stenosis, whereas 2 exhibited no obstruction to pulmonary flow. No examples of pulmonary atresia were present among the 3 specimens with double conus (lIB a). PULMONARY STENOSIS (lIB b). In the single specimen with pulmonary stenosis (lIB b), the pulmonary trunk and aorta each arose from a respective conus of the left ventricle (Fig. 4, a). There were two large muscular ventricular septal defects connecting the hypoplastic right ventricle with the left ventricle. The membranous ventricular septum was well formed and hung over the higher ventricular septal defect as a curtain. The basis for pulmonary stenosis was a combination of dysplasia of the tricuspid pulmonary valve and a membranous ring in the subpulmonary area. Both coronary arteries arose from the anterior aortic sinus. The anatomic diagnosis in this case was tricuspid atresia with double-outlet left ventricle, two muscular ventricular septal defects, and valvular and subvalvular pulmonary stenosis. ABSENCE OF PULMONARY STENOSIS (lIB c). In each of the 2 cases of double conus without pulmonary stenosis (lIB c), the aorta and the pulmonary trunk each arose from a conus-the aorta from the right ventricle and the pulmonary trunk from the left. The left atrioventricular valve showed the morphologic characteristics of a mitral valve and was not in continuity with either the aortic or the pulmonary valve (Fig. 4, b). A large ventricular septal defect provided communication between the two ventricles. The ventricular septal defect was subaortic in both cases. It was relatively narrow in I specimen and resulted in subaortic stenosis. There was an accessory orifice in the anterior leaflet of the mitral valve in this case. Jet lesions on the left atrial wall were associated. The anatomic diagnosis in both cases was tricuspid atresia with transposition of the great vessels and double conus.
Fig. 5. Tricuspid atresia with persistent truncus arteriosus. Both pulmonary arteries (R .P.A., L.P.A.) arise separately from the truncus arteriosus (T.A.) The truncus valve forms the roof of a ventricular septal defect, providing the only inlet for the right ventricle.
Persistent truncus arteriosus (Type III). Among the 45 cases of tricuspid atresia, I was associated with persistent truncus arteriosus. The right atrioventricular valve was atretic and the left showed the characteristics of a mitral valve. The mitral valve led into a large morphologic left ventricle. A ventricular septal defect was present in the outflow tract occupying the site of membranous and the anterior smooth septum. The roof of the ventricular septal defect was formed by the truncus valve which arose from both ventricles. The truncus valve with three cusps was in continuity with the mitral valve (Fig. 5). The right ventricle was present as a small cavity and communicated with the left ventricle through the ventricular septal defect. The first set of branches from the truncus was represented by the two coronary arteries. These were followed by the two pulmonary arteries arising separately, one above the other. The right pulmonary artery arose 8
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mm. and the left pulmonary artery 14 mm. above the truncus valve. Thus, the truncus arteriosus was of Type II according to the classification of Collett and Edwards." Associated anomalies. The foregoing material reviewed some of the anomalies that are associated with tricuspid atresia, excluding variations in ventricular structure and relations with great vessels. Associated anomalies and others not mentioned are summarized for convenience. Anomalies of the aortic arch system. RIGHT AORTIC ARCH WITH MIRROR-IMAGE BRANCHING. A right aortic arch with mirrorimage branching was present in 3 of the 45 cases. In 1 case each, the great vessels showed normal relationship (Ib ), d-transposition (IIA lc) , and l-transposition (IIA 2a). DOUBLE AORTIC ARCH. Double aortic arch was found in 1 case. This showed normally related great vessels (Ib). OBSTRUCTIVE ANOMALIES OF THE ARCH. Tubular hypoplasia of the aortic arch, coarctation, interruption, and atresia of the arch were present only in the group with dtransposition of the great vessels and have been covered in the main body of the paper (Table II). Pulmonary atresia. Pulmonary atresia of some type was observed in 4 cases. In 3 of these, the atresia was at the level of the pulmonary valve. It occurred once among each of the following types of tricuspid atresia: with normally related great vessels, with d-.. transposition, and with l-transposition. A patent ductus arteriosus provided the pulmonary blood flow in each case. In the fourth case, the "pulmonary atresia" was unusual in type. It resulted from spontaneous closure of the ventricular septal defect. The consequence was complete obstruction to pulmonary blood flow. The great vessels were normally related in this case (Ib) and the ductus arteriosus had closed spontaneously. Unusual communications between the atria. In 43 of the 45 specimens the communication between the two atria was at the fossa ovalis. In some of these, the com-
munication was represented by a valvular competent patent foramen ovale, while in others an atrial septal defect resulted from valvular incompetence of the foramen ovale. In 1 of the 2 remaining specimens, an ostium primum type of atrial septal defect was present, and in the other the atrial septum was intact. In the latter case, the coronary sinus communicated with both atria and was the only route through which the right atrial blood could reach the left atrium." Juxtaposition of atrial appendages. Juxtaposition of atrial appendages was observed in 6 cases. In each, both atrial appendages lay to the left of the great vessels. The great vessels were normally related in 1 case, exhibited d-transposition in 4, and I-transposition in the sixth. Comments In 1906, Kuhne 7 classified tricuspid atresia into those cases associated with transposition of great vessels and those without associated transposition of great vessels. Based on Kuhne's observations, a clinicopathological classification was proposed in 1949 by Edwards and Burchell' and later modified by Edwards." It included the recognition of two types of great vessel relationships-normal or transposed-and of the basic clinical patterns resulting from the presence or absence of obstruction to pulmonary blood flow. Keith, Rowe, and Vlad" reviewed 143 specimens of tricuspid atresia of which 92 were from the literature. They modified the classification of Edwards and Burchell to include l-transposition (inverted transposition) of the great vessels, a condition seen in 4 of the 143 specimens they reviewed. Those authors referred to this form as Type III tricuspid atresia and restricted d-transposi tion (noninverted) to Type II. In the classification here presented, we adhere basically to that of Edwards and Burchell, while accepting the modification of Keith and associates in dividing transposition into d- and 1- types. This classification adds the recognition of double conus and persistent truncus arteriosus in association with tricuspid atresia.
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Tricuspid atresia
Number 4 April, 1974
The incidence of transposition in our series was somewhat higher than that in the series reviewed by Keith (42 per cent in this series; 30 per cent in Keith's). To our knowledge, no other case of persistent truncus arteriosus with tricuspid atresia, as seen in 1 of our cases, has previously been reported. When transposition was associated with a single conus, the more common type was d-transposition, the less common, l-transposition (ratio 3:1). Our studies indicate that, in tricuspid atresia with obstruction to pulmonary blood flow, normally related great vessels are more common than transposition, whereas, in the absence of obstruction to pulmonary blood flow, some type of transposition of the great vessels is more frequent than normally related great vessels. Among our various groups of tricuspid atresia, 27 of 45 cases (60 per cent) showed obstruction to pulmonary blood flow, whereas in 18 specimens (40 per cent) there was no obstruction to pulmonary blood flow. Of the 27 specimens with obstruction to pulmonary blood flow, 21 cases (78 per cent) showed normally related great vessels, while 6 cases (22 per cent) exhibited transposition of the great vessels. On the other hand, of the 18 specimens without obstruction to pulmonary blood flow, 13 (72 per cent) showed transposition of the great vessels, 4 (22 per cent) exhibited normally related great vessels, and 1 specimen (6 per cent) had persistent truncus. When the great vessels were normally related, obstruction to pulmonary flow was common (21 of 25 cases; 84 per cent). When they were transposed, obstruction to pulmonary flow was less common (6 of 19 cases; 32 per cent). In instances of single conus and transposition, obstruction to pulmonary flow was less common in d-transposition (3 of 12 cases; 25 per cent) than in l-transposition (2 of 4 cases; 50 per cent). Although in our series the number of cases of double conus is small, obstruction to pulmonary flow was less common than
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absence of this condition (l case of pulmonary stenosis among 3). Obstruction to systemic arterial flow was seen in 7 of the 45 cases of tricuspid atresia. Each was associated with transposed great vessels. The obstruction was more frequently extracardiac (aortic) than intracardiac, but in some cases both were present together. We did not observe aortic obstruction in any of our cases in which the great vessels were normally related. We are, however, aware of 1 reported case of tricuspid atresia and normally related great vessels in which coarctation of the aorta was present." Pulmonary stenosis was absent in that case. Of particular interest, from a developmental viewpoint, are our 4 cases of l-transposition. For discussion, these cases might be considered to be examples of "corrected transposition with mitral atresia." If this were so, the main ventricle would be expected to be the anatomic right ventricle and the atretic valve a right-sided mitral valve; yet the internal features of the hearts did not support such a concept, as the main ventricle showed the characteristics of a left ventricle and the intact valve those of a mitral valve. These cases, therefore, are considered to be examples of bulbar inversion without inversion of the ventricular sinuses." Theoretically, further variability in the group represented by the only case of persistent truncus arteriosus is possible. In our specimen, the truncus arteriosus was of Type II according to the classification of Collett and Edwards. G In a study of the literature, we did not find any reported cases of persistent truncus arteriosus associated with tricuspid atresia.
Addendum Since the completion of this study, 2 cases have been added to our collection. Since both provide additional features of interest, we would like to summarize them. In I case reported by MarinGarcia and associates.t- the tricuspid atresia was associated with normally related great vessels, intact ventricular septum, patent ductus arteriosus, and absence of the pulmonary valve. The other
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case was characterized by tricuspid atresia, normally related great vessels, pulmonary stenosis, and absence of the atrial septum (common atrium). REFERENCES
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Edwards, 1. E., and Burchell, H. B.: Congenital Tricuspid Atresia: A Classification, Med. Clin. North Am. 33: 1177, 1949. Fontan, F., and Baudet, E.: Surgical Repairs of Tricuspid Atresia, Thorax 26: 240, 1971. Stanford, W., Armstrong, R. G., Cline, R. E., and King, T. D.: Right Atrium-Pulmonary Artery Allograft for Correction of Tricuspid Atresia, I. THORAC. CARDIOVASC. SURG. 66: 105, 1973. Van Praagh, R., and Vlad, P.: Transposition of the great arteries, in Keith, I. D., Rowe, R. D., and Vlad, P., editors: Heart Disease in Infancy and Childhood, ed. 2, New York, 1967, Macmillan Publishing Co., Inc. Edwards, I. E.: Congenital Malformations of the Heart and Great Vessels. C. Malformation of the Valves, in Gould, S. E., editor: Pathology of the Heart and Blood Vessels, ed. 3, Springfield, III., 1968, Charles C Thomas, Publisher, p. 313. Collett, R. W., and Edwards, I. E.: Persistent
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Truncus Arteriosus: A Classification According to Anatomic Types, Surg. Clin. North Am. 33: 1245, 1949. KUhne, M.: Uber zwei Faile kongenitaler Atresie des Ostium venosum dextrum, 1ahrb. Kinderh. 63: 235, 1906. Keith, 1. D., Rowe, R. D., and Vlad, P.: Tricuspid Atresia, in Keith, I. D., Rowe, R. D., and Vlad, P., editors: Heart Disease in Infancy and Childhood, ed. 2, New York, 1967, Macmillan Publishing Co., Inc., p. 644. Chiche, P.: Etude anatomique et clinique des atresies tricuspidiennes, Arch. Mal. Coeur 44: 981, 1952. Raghib, G., Anderson, R. c., and Edwards, 1. E.: Isolated Bulbar Inversion in Corrected Transposition, Am. 1. Cardiol. 17: 407, 1966. Rose, A. G., Beckman, C. B., and Edwards, 1. E.: Communication Between the Coronary Sinus and the Left Atrium, Br. Heart 1. In press. Marin-Garcia, I., Roca, 1., Blieden, L. c., Lucus, R. V., Ir., and Edwards, I. E.: Congenital Absence of the Pulmonary Valve Associated With Tricuspid' Atresia and Intact Ventricular Septum, Chest 64: 658, 1973.