Partial or Total Direct Pulmonary Venous Drainage to Right Atrium Due to Malposition of Septum Primum

clinical investigations Partial or Total Direct Pulmonary Venous Drainage to Right Atrium Due to Malposition of Septum Primum* Anatomic and Echocardiographic Findings and Surgical Treatment: A Study Based on 36 Cases Stella Van Praagh, MD; Maria E. Carrera, MD; Stephen Sanders, MD 1; john E. Mayer ]r, MD; and Richard Van Praagh, MD The clinical and anatomic findings in 36 patients (21 postmortem cases and 15 living patients) with partially anomalous (16 [44%]) or totally anomalous (20 [56%]) pulmonary venous drainage directly to the right atrium constitute the material basis of this report. Displacement of septum primum-leftward in atrial situs solitus or rightward in atrial situs inversus-was present in all and appeared responsible for the anomalous pulmonary venous drainage. The pulmonary veins were connected with what normally constitutes the posterior wall of the left atrium, which became incorporated into the right atrium because of atrial septal displacement. This abnormality occurred predominantly in patients with visceral heterotaxy, usually with polysplenia, or rarely with asplenia or a normally formed spleen. Poor devel-

The common pulmonary vein represents the direct blood route from the venous plexus of the pulmonary parenchyma of the human embryo to its developing heart. Although there is no unanimous agreement about the exact site of its origin, 1-9 it is generally accepted that by the end of the first month of gestation, the common pulmonary vein can be identified as a vessel containing blood, draining the pulmonary venous plexus and entering the sinoatrial portion of the embryonic heart cephalic to the junction of the left and right horns of the sinus venosus.3·5-7 The normal development of the superior limbic band of septum secundum 10•11 provides the necessary background for the attachments of septum primum . *From the Departments of Cardiology (Drs. S. Van Praagh and Sanders) , Cardiac Surgery (Dr. Mayer), and Pathology (Drs. Carrera and R. Van Praagh), Children's Hospital, Boston, and the Departments of Pediatrics (Dr. S. Van Praagh), Surgery (Dr. Mayer), and Pathology (Drs. Carrera and R. Van Praagh), Harvard Medical School, Boston. tCurrently at The Aldo Castaneda Institute for Congenital Cardiac Disease, Clinique de Grenolier, CH-1261, Grenolier, Switzerland. Supported in part by the Karen Arbia Scholarship Fund. Manuscript received July 7, 1994; revision accepted November 22. Reprint requests: Dr. Van Praagh, 300 Longwood Avenue, Children's Hospital, Boston , MA 02115

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opment or absence of septum secundum appeared responsible for the malposition of septum primum. Echocardiographic recognition of the displacement of septum primum facilitated surgical management. (CHEST 1995; 107:1488-98) AV=atrioventricular; {I, D, S}=inverted atria, D-loop ventricles, solitus normally related great arteries; {1, L, !}=inverted atria, L-loop ventricles, inverted normally related great arteries; IVC=inferior vena cava; LA=Ieft atrium; RA=right atrium; {S, D, S}=solitus atria, D-loop ventricles, solitus normally related great arteries; SPM=septum primum malposition; SVC=superior vena cava; 2-D=two-dimensional

Key words: malposition, septum primum; polysplenia; pulmonary veins, right atrium

The septum primum , which grows parallel and to the left of the left sinoatrial valve,? normally attaches on the left side of the superior limbic band immediately to the right of the site of entrance of the common pulmonary vein.l 2 It is thus established as the valve of the foramen ovale. In conjunction with septum secundum, septum primum outlines the septal limits of the two atria and places the entrance of the common pulmonary vein into the cavity of the left atrium (LA) . If the superior limbic band of septum secundum fails to develop, the crescentic cephalad border of septum primum remains unattached and could be carried leftward in cases of atrial situs solitus or rightward in cases of atrial situs in versus by the blood stream of the fetal circulation that proceeds from the right atrium (RA) toward the LA. Depending on the degree of septum primum displacement toward the LA, half or all of the pulmonary veins can drain into the cavity of the anatomically RA despite their normal connection with the posterior wall of the LA. In the cases of this study, the connection of the pulmonary veins with the lungs and with the heart appeared normal externally. Yet either half or all of the Clinical Investigations

Table 1-Criteria for Visceral Heterotaxy* Criteria l. Symmetric liver in the chest radiograph or at postmortem examination 2. Viscero-atrial discordance, ie, solitus atria, with inversus abdominal viscera or vice versa; also, discrepancy between the situs of the lungs and atria 3. Levocardia with right-sided stomach or dextrocardia with left-sided stomach 4. Interrupted inferior vena cava with unilateral azygos continuation to the ipsilateral or contralateral superior vena cava (SVC) 5. Interrupted inferior vena cava with bilateral azygos continuation to bilateral SVCs 6. Atrioventricular discordance with normally related great arteries 7. Symmetric lung lobation and bronchoarterial relationships at postmortem examination or symmetric bronchi in the chest radiograph 8. Discordance between lung lobation and bronchoarterial relationship 9. Intestinal malrotation with or without intestinal obstruction 10. Evidence of multilobed spleen or multiple spleens by postmortem examination, radioisotope scanning, or abdominal ultrasound 11. Evidence of asplenia by postmortem examination 12. Common mesentery 13. The presence of ectopic atrial pacemaker or nodal rhythm or complete AV block in the preoperative electrocardiogram

*Visceral heterotaxy (ie, other than normal order of the viscera) appears to result mainly from: (1 ) persistence of the normal, early embryonic symmetry of the lungs, the liver, the atrial appendages, and the systemic veins, and (2) inconsistent situs of the various viscera and/ or cardiac segments.

pulmonary veins drained directly into the cavity of the RA. We present detailed photographic documentation of the pathologic anatomic findings that support the above-outlined explanation of this apparent paradox. In addition, echocardiographic documentation of the malposition of the septum primum is demonstrated for the first time (to our knowledge). METHODS

The two-dimensional (2-D) echocardiograms and Doppler studies of all the patients who were diagnosed as having partial or total direct pulmonary venous return to the RA from March 1986 to December 1993 were reviewed. The unsatisfactory quality of 2-D echocardiograms prior to March 1986 dictated the time limits of this study. The 2-D echocardiograms were performed using a cardiac imager (Hewlett-Packard 77020 or Sonos 1000 or an Acuson 128) with a 7.5-, 5-, or 3.5-MHz transducer focused appropriately for the size of the patient. Since 1987, Doppler color flow mapping has been used routinely in addition to imaging. All examinations were recorded on 1.25-cm video cassette tape for subsequent review. A complete examination , including subxiphoid, apical, left and right parasternal, and suprasternal notch views, was performed in each patient. The subxiphoid long-axis and apical four-chamber views usually displayed the position and orientation of the septum primum. The defect between the septum primum and the septum secundum or the posterior atrial wall could be seen in these views as well. The superior limbic band of the septum secundum was seen best in the subxiphoid short-axis view at or just to the left of the plane of the superior vena cava (SVC). Absence or hypoplasia of the superior limbic band was diagnosed when no ridge of tissue was seen on the posterior atrial wall between the SVC-RA junction and the ipsilateral pulmonary veins. The anomalous drainage of some or all of the pulmonary veins to the RA was usually apparent in the apical four-chamber and subxiphoid long-axis views. Doppler color flow mapping in these views was useful for identifying pulmonary vein flow and confirming anomalous drainage to the RA. The malposition of the septum primum was confirmed at sur-

gery in the 11 patients who underwent intracardiac biventricular repair. All the postmortem cases with the diagnosis of partial or total direct pulmonary venous drainage to the RA in the Cardiac Registry of the Children's Hospital, Boston, were reexamined. Thirteen of the 21 postmortem cases associated with visceral heterotaxy and polysplenia or asplenia have been previously reported as part of a larger group of heterotaxic patients in a chapter describing the systemic and pulmonary venous connections in visceral heterotaxy. 13 They were also included in a chapter about cardiac malpositions. 14 The cases with only the right pulmonary veins draining into the RA in association with a sinus venous defect represent a different kind of cardiac malformation and have been reported separately. 15 Special attention was given to the morphology and position of the atrial septa (superior limbic band of septum secundum and septum primum), the atrial connections of the pulmonary veins, and the identification of the anatomically RA. The anatomically RA was considered to be: (1) the atrium that exhibited the orifice of a normal (ie, not unroofed) coronary sinus with or without a persistent SVC; (2) the atrium that received all the systemic and half or all of the pulmonary veins, regardless of the presence or absence of a coronary sinus orifice; and (3) the atrium contralateral to a SVC that was connected with a partially unroofed coronary sinus. These three prerequisites for the identification of the anatomically RA are based on the well-documented embryologic facts that indicate that the right horn of the sinus venosus becomes incorporated into the RA and contributes the orifices of the SVC and the inferior vena cava (IVC). The left horn contributes the orifice of the coronary sinus with or without a persistent left SVC. 16 Although malposition of septum primum can allow half or all of the pulmonary veins to drain into the RA, this anomalous drainage into the RA cavity does not interfere with the identification of the anatomically RA. The atrial situs, the ventricular loop, and the morphology of the atrioventricular (A V) valves, ventricular septum, semilunar valves, and great arteries were assessed echocardiographically and by surgical observation in the living patients and by postmortem examination in the deceased cases. The clinical history and findings, the preoperative cardiac catheterization report(s), and the preoperative electrocardiograms (available in 30 of 36 patients) were reviewed. CHEST /107/6/ JUNE, 1995

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FIGURE 1. The heart and lungs of a 2-month-old male infant with double outlet right ventricle, mitral atresia, and total direct pulmonary venous return to the anatomically right atrium, right-sided (C93177). Left, A. Interior view of the right atrium and right ventricle (RV). The right pulmonary veins (RPVs) and the left pulmonary veins (LPVs) (solid arrow ), the HV confluence (open arrow), the coronary sinus (CoS), and the right superior vena cava (RSVC) with the azygos (AZ) extension of the interrupted inferior vena cava all drain into the anatomically right atrium. The septum primum (Sl 0 ) attachments on the posterior atrial wall are magnified in the inset. Although not fused with the atrial wall, the malpositioned septum primum prevented the normal right to left atrial flow during fetal life and was possibly responsible for the atresia of the mitral valve. Right, B. Interior of hypoplastic left atrium (LA) and left ventricle (LV). The orifice of the mitral valve is atretic (MAt). Ao=aorta; LAA =left atrial appendage; MPA=main pulmonary artery.

RESULTS

A total of 36 cases were identified. Fifteen cases were diagnosed by 2-D echocardiography and Doppler interrogation and 21 cases were diagnosed by postmortem examination. Partial (only one lung) pulmonary venous drainage to the anatomically RA was present in 16 patients, and total drainage to the anatomically RA was present in 20 cases. The gender was known in 35 patients. Male/ female ratio was 0.45/1.

Visceral Heterotaxy Two or more of the characteristic findings usually seen in patients with visceral heterotaxy (Table 1) were present in 33 of the 36 cases (92%). Three or more characteristics of visceral heterotaxy were present in 29 of 36 (81%) of the patients. In the four patients with only two heterotaxic signs, we had no information regarding the symmetry of their lungs or the situs of all of the abdominal viscera_since three of four are alive and the one who is deceased did not have a postmortem examination. The three patients with one or no heterotaxic signs are also alive. 1490

Splenic Anomalies The status of the spleen was determined by postmortem examination in 20 patients and by radioisotope liver-spleen scan in 4. Twenty-two patients had polysplenia, 1 had asplenia, and 1 had a normal spleen. In 1 deceased and llliving patients, the status of the spleen was not known.

Cardiac Findings The pulmonary veins appeared to be connected normally with the atrial wall externally regardless of partial or total pulmonary venous drainage into the anatomically RA. Their orifices were located between the two SVCs in all the cases with bilateral SVCs, 16 of 36 (44%), as expected in normal pulmonary venous connection, or to the left of a single right SVC and to the right of a single left SVC. The superior limbic band of septum secundum was unidentifiable in the hearts of all the postmortem cases and in all but one of the 2-D echocardiograms of the living patients. This one patient had a small atrial ridge in her 2-D echocardiogram that could possibly represent an underdeveloped superior limClinical Investigations

FIGURE 2. The heart of a 7-year, 2-month-old girl with total direct pulmonary venous return to the right atrium (RA), a membranous ventricular septal defect, and visceral heterotaxy with right polysplenia (A68-66). Top left, A. Interior of right atrium and right ventricle. All the systemic and pulmonary veins enter the RA which is right-sided. The RV is very hypertrophied. The interatrial communication is between the upper border of the mal positioned Sl 0 and the posterior atrial wall. IVC=inferior vena cava; PVs=pulmonary veins; RAA=right atrial appendage. Top right, B. Interior view of the RV outflow. Note the marked hypertrophy of the septal band (SB). The white arrow is through a very small membranous ventricular septal defect (VSD). PV=pulmonary valve. Bottom left, C. Interior view of LA and LV. Note absence of attachments of Sl 0 on atrial septal surface (AS); MV =mitral valve. Other abbreviations are described in Fig l. B reproduced with permission. 13

hie band. The septum primum was always shifted toward the anatomically LA, attaching on the posterior atrial wall. Its attachments were, as a rule, visible from the RA side (Figs lA, 2A and C, SA and B, and 4). Above the characteristic half-moon-shaped upper border of septum primum and between the septum primum and the posterior atrial wall, there was usually an interatrial communication of variable size (Figs. 2A, SA , and 4). In a few cases (Table 2) where the attachment of septum primum to the posterior wall of the LA did not permit any blood flow from the RA to the LA, the mitral valve was atretic (Fig lB). In the cases where the interatrial communication was small and the great arteries related normally to the ventricles, the survival of the patient depended on the presence of a ventricular septal defect (Fig 2B) or a common AV canal (Fig SA and B). This interatrial communication is not, accurately speaking, the foramen ovale (because it is not located

between septum primum and the superior limbic band of septum secundum), or an ostium secundum defect, or a sinus venosus defect. An accurate designation is as follows: interatrial communication associated with absence of septum secundum and malposition of septum prim urn. In short, this is a "septum primum malposition (SPM) defect." In four cases, the septum primum fused with the posterior atrial wall, and in those cases the atrial septum appeared intact but without the normally seen fossa ovalis. The malposition of septum primum was clearly visualized echocardiographically (Figs 5A and B and 6) . In a postmorten case of dextrocardia and inversus atria, the malposition of septum prim urn was extreme allowing both SVCs and both atrial appendages to communicate with the left-sided RA (Figs 7A and B and 8) . The right-sided LA was a small cavity receiving only the right pulmonary veins via a single orifice and communicating with the RAvia an ostium prim urn defect and a very small SPM defect (Figs 7 A and Band 8). This type of extreme septum primum malposition resulting in the above most unusual relationships of the RA has not, to our knowledge, been reported previously . CHEST / 107 / 6 / JUNE, 1995

1491

Associated Cardiac Malformations The type and frequency of the major associated cardiac malformations are presented· in Table 2. The high frequency of AV discordance with normally related great arteries and double-outlet right ventricle with only subpulmonary conus reaffirms our earlier observation that the hearts of patients with visceral heterotaxy and polysplenia have, as a rule, subpulmonary conus 13•14 and very seldom have transposition of the great arteries with subaortic conus (Table 2).

Clinical Findings Signs of congestive heart failure and chest radiographic findings of cardiac enlargement and increased pulmonary blood flow were present in all the patients who did not have pulmonary stenosis or atresia. Clinical cyanosis or arterial unsaturation or both were present in all patients. Rhythm disturbances such as ectopic atrial pacemakers or nodal rhythm or complete A Vblock were present in 26 of the 30 patients (87%) in whom preoperative electrocardiograms were available for review.

Surgical Management and Results Since many of the patients with partial or total direct pulmonary venous return to the RA had additional heart defects, the surgical treatment was individualized. There were three main categories of patients.

Table 2-Major Associated Malformations in 36 Patients With Partial or Total Pulmonary Venous Drainage to the Right Atrium* Partial APYD, (n=16) Associated Major Cardiac Malformations Partial or complete CAYC Mitral atresia DORY with Pul conus DORY with Bil conus AY discordance with NRGAs TGAs Pul atresia

Total APYD, (n=20)

No.

(%)

No.

(%)

6 1

(37) (6)

1

(6) (25) (6)

8 2 4 4 5

(40) (10) (20) (20) (25)

3

(15)

4

*APYD=anomalous pulmonary venous drainage; Bil=bilateral; CAYC=common AY canal; DORY=double-outlet right ventricle; NRGAs=normally related great arteries; Pul=pulmonary; TGAs= transposition of the great arteries.

(1) The patients with AV concordance, two welldeveloped ventricles, and normally related great arteries either did not have any additional defects or had defects that could be corrected easily such as ostium primum defect, ventricular septal defect, aortic valve stenosis, coarctation of the aorta, or tetralogy of Fallot. There were 15 such patients (12 {S, D, S} and 3 {1, L, I}) but only 11 were operated on (Table 3). Nine underwent atrial septal resection and construction of a new appropriately positioned atrial septum with either pericardium or prosthetic materiaL All are doing well, except for one patient who died following surgery for scoliosis. Two were mis-

3. The heart of a 12-year, 7-month-old boy with dextrocardia, visceral heterotaxy, right-sided polysplenia, in versus atria and ventricles, common AY canal, and in versus normally related great arteries (A67-2) Left, A. Interior of the anatomically right atrium, left-sided, which receives all of the systemic and pulmonary veins. A small interatrial communication is present between the upper border of the malpositioned Sl 0 and the posterior wall. CAYY=common atrioventricular valve; CT=crista terminalis. Right, B. The interior of the very small left atrium of the same heart that does not receive any vessels. Note the absence of Sl 0 attachments on its septal surface. Abbreviations are described previously. Reproduced with permission. 38 FIGURE

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Clinical Investigations

diagnosed as having a common atrium and died during or after surgery. Four died without surgery prior to 1973. (2) There were three patients with AV discordance, two well-developed ventricles, normally related great arteries (all 3 {I, D, S}) , and repairable additional defects. All underwent atrial septal resection and baffling of the pulmonary veins to the LV or the systemic veins to the R V .One of these patients who has a transitional common A Vcanal defect has developed significant mitral regurgitation . The other two are doing well. (3) There were 18 patients with associated complex heart defects usually precluding biventricular repair. Five died without surgery. Thirteen underwent an aorticopulmonary shunt and/ or a cavopulmonary anastomosis. In this group, the malposition of septum primum resulting in partial or total pulmonary venous drainage to the RA was not relevant for the

surgical procedure performed. A summary of the operated, unoperated, and deceased patients is presented in Table 3. DISCUSSION

"Anomalous connection [of the pulmonary veins] with the superior portion of the right atrium may be explained on the basis of abnormality of the atrial septum. If the septum develops farther to the left than is normal, that outpouching of the sinoatrial region which joins the pulmonary vessels may lie to the right of the atrial septum and the entire venous system of the lungs will then connect with the right atrium. Lesser degrees of abnormal positioning of the atrial septum may account for cases in which the left pulmonary veins enter the left atrium while those of the right lung enter the right atrium." This most accurate observation reported 41 years ago by Edwards 17 and reaffirmed by Moller et aP 8 14

FIGURE 4. The heart of a 6-month-old boy with dextrocardia, visceral heterotaxy, asplenia, inversus atria, D-loop ventricles, common AV canal, and double-outlet right ventricle (A66-76). Interior of the left-sided anatomically RA and the left-sided left ventricle. TheRA receives all of the pulmonary veins and the left-sided SVC and lVC. The mal positioned Sl 0 has three small fenestrations. Alarger interatrial communication (arrow) is between the upper border of Sl 0 and the posterior atrial wall (ie, a septum primum malposition defect). Abbreviations are described previously. Reproduced with permission. 38

CHEST / 107/6/ JUNE, 1995

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FIG URE 6. An apical four- chamber view of a 2-year-old infant with atrial situs solitus, interrupted IVC, ventricular D-loop, and tetralogy of Fallot (104-15-23 ). There is extrem e malposition of septum primum (S1°) so that all of the pulmonary veins drain into the RA. In this view, both a right pulmonary vein (RPV ) and a left pulmonary vein (LPV ) can be seen entering the RA. In addition to the septum primum m alposition d efect, there are multiple fenestrations in the substance of septum primum. The ori· fi ce of the right atrial appendage (RAA) is seen on the right side of the atrium. The markedly mal positioned S1 °may erroneously suggest comm on atrium with supramitral m embrane.

FIGURE 5. Top, A. Apical four- chamber view in a 3-year 9-monthold child with atrial situs solitus and ventricular D-loop, malpo· sition of septum primum, and drainage of the right pulmonary veins to the RA (30-87-94). The LA is smaller than usual due to leftward displacem ent of the septum primum. The left lower pulmonary vein (LLPV ) is seen entering the LA. TheRA and RV are dilated. The interatrial communication, a septum primum malposition defect, is seen between the posterior margin of septum primum and the posterior atrial wall (arrowhead ). Bottom, B. Color flow mapping in the same view confirms flow from the left lower pulmonary vein (LLPV ) into the LA and flow from the right upper pulmonary vein (RUPV ) into the RA. The descending thoracic aorta (DAo) is indicated as a reference marker to distinguish right and left pulmonary veins. Abbreviations are described previously.

years later has not as yet achieved its deserved recognition in the diagnosis of partial or total pulmonary venous return to RA.l 9 The findings of this study strongly support the above observation and in addition suggest that the reason for the malposition of septum primum is the absence of the superior limbic band of septum secundum. To our knowledge, this is the only malformation that exhibits the attachments of the upper border of septum primum on the RA side. The ear1494

liest description of such a heart may be the one published by Maude Abbott 20 in a very accurate drawing of a case with dextrocardia, atrial situs inversus, and ipsilateral pulmonary venous drainage. The patient, a 9-week-old male infant , died from "volvulus of the intestines," reminiscent of the intestinal malrotation and obstruction that often occur in visceral heterotaxy with polysplenia and which was observed in two of the patients of this study. Table 3-Summary of Operated and

Unoperated Patients Operated

l. AV concordance

and NRGAsl n=l5 2. AV discordance and NRGAs n=3 3. Complex associated heart defects n=18

Alive

Dead

Unoperated*

8

3t

4

3

0

0

4

9

5

*The unoperated patients are all postmortem cases. The living unoperated patients were not included since the criteria for inclusion in this study were documentation of the cardiac anatomy by echocardiography and surgical observation or b y postmortem examination. tone of these patients died following surgery for scoliosis. I RGAs= normally related great arteries. Clinical Investigations

lAC

FIGURE 7. Posterior view of the heart of an 8-year, 2-month-old boy with visceral heterotaxy, dextrocardia, double-outlet RV, in versus atria and ventricles, common AV valve almost entirely above the right \'C'ntricle, severe subpulmonary stenosis, and ipsilateral pulmonary veins (C92-375). Left, A. Interior of the markedly enlarged RA, left-sided, seen from behind. The suture lines of the transected RSVC and LSVC (seen more clearly in the diagrammatic outline of this case) indicate that both these vessels drained into the RA. The ostium primum defect (marked by the open arrow) functions as the outlet of the small right-sided LA that received the right pulmonary veins via a common orifice (see diagram). The black arrow points toward the probe placed into the very small septum primum malposition defect. Both the anteriorly directed RAA left-sided (Lt) and the posteriorly directed LAA right-sided (Rt) communicate with the large RA. A miniscule right-sided LV is on the posterior surface of this globular, shaped heart. Right, B. Diagrammatic representation of the systemic and pulmonary venous connections and the internal morphology of the same heart (posterior view). Black arrow points toward the ostium 1° defect. White arrows indicate the interventricular communication.

Normally the septum primum grows from sinus venosus tissue adjacent to the IVC-RA junction parallel with the left venous valve. 7 When it completes its normal growth, it is attached on the LA side of the superior limbic band. It is the valve of the foramen ovale for the fetal circulation and forms part of the interatrial septum for the postnatal heart. Its normal growth and its normal attachments on septum secundum are essential for the alignment of the common pulmonary vein with the cavity of the LA. If the sinoatrial outpouching, which becomes the common pulmonary vein, becomes established and remains patent, one could always expect a normal pulmonary venous connection with the atrial portion of the heart. Abnormal pulmonary venous connections occur when the common pulmonary vein does not develop or becomes obliterated and the pulmonary venous plexus maintains its early embryonic connections with the cardinal or vitelline veinsP·21 Hence, when the pulmonary veins are connected with the atrial portion of the heart, they are normally connected even if half or all of them drain into the anatomically RA. This conclusion is supported by the fact that externally they occupy the posterior atrial wall between the two SVCs (when two SVCs are present), which is the posterior wall -of the LA. It is the malposition of septum primum (ie, its displacement toward the anatomically LA) that allows half or

FIGURE 8. Two-dimensional echocardiogram of the same patient (parasternal short-axis view) as in Figure 7 shows the tiny LA receiving a single right pulmonary vein (RPV). Sl 0 demarcates the plane of the atrial septum. The septum primum malposition defect is seen between the anterosuperior edge of septum primum and the atrial wall. The large RA is seen to the left. The pulmonary valve (PV) is abnormal and stenotic and posterior to the larger Ao. The RSVC is seen lateral to the great arteries. Other abbreviations are described previously. CHEST /107/6/ JUNE, 1995

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Table 4-Di.fferential Diagnosis of Interatrial Communications Associated With Direct Pulmonary Venous Drainage Into the Right Atrium*

Right PVs drain into RA All PVs drain into RA Normal attachments of septum 1° on septum 2° Size of lAC Intact AS Interrupted IVC CAVC Visceral heterotaxy Conduction disturbances (EAP and AVB 3°) Surgical treatment

Sinus Venosus Defect RA Type

Large ASD 2° With Posterior Extension

+

+

+

+

Small to moderate

+

+

Large

Small Occasionally Often Often Often Often

Patch closure of the large ASD, placing the PVs into the LA

Complete resection of septum l 0 and reconstruction of a normally placed atrial septum , or baffling of PVs to LV, or baffling the systemic veins to RV

Very seldom Seldom Enlarge the lAC, if necessary, by partial detachment of septum 1°, suture pericardia! patch between upper border of detached septum l 0 and the right border of the pulmonary veins

Septum Primum Malposition Defect

*ASD=atrial septal defect; PV =pulmonary vein; lAC= interatrial communication; AS= atrial septum; CA VC=common AV canal; EAP=ectopic atrial pacemaker; AVB=atrioventricular block, third degree; LV=left ventricle; RV=right ventricle. +=present; -=absent.

all of the pulmonary veins to drain into the anatomically RA . An alternative explanation has been proposed for the ipsilateral pulmonary venous drainage, ie, the development of two common pulmonary veins, one for each atrium.22 This theory cannot explain the anatomic and echocardiographic findings of the malposition of septum primum and the absence of septum secundum. The malposition of the septum primum is easily detected echocardiographically and it was diagnosed preoperatively in many of the living patients of this study (Figs SA and B, 6, and 7). By contrast, the accurate diagnosis of the interatrial communication was seldom accomplished (for the simple reason that we did not have an appropriate name for it). In the patients of this study, it was described as sinus venosus defect, a high or posterior ostium secundum defect, or a patent foramen ovale. As we explained in the "Results" section, none of the above terms is accurate. The interatrial communication in these patients is the space between the upper border of septum primum and the posterior atrial wall (Figs 2A, 3A, 4, SA, and 6B). We propose the term septum primum malposition (SPM) defect to describe this communication. In some cases, one or more fenestrations in the substance of septum primum, ie, ostium secundum defects coexisted with the SPM defect. Leftward deviation of septum primum has been 1496

described in cases of ostium primum defects with a very small LA 23 and in cases of hypoplastic left heart syndrome with aortic atresia. 24 In both of these situations, the superior limbic band is present and the septum primum attaches to it from the LA side. Hence, the septum primum is not truly malpositioned. In some cases of hypoplastic left heart syndrome with aneurysmal dilatation of septum primum, some blood from the right pulmonary veins may flow via the foramen ovale into the RA. 24 Nevertheless, the orifices of all the pulmonary veins are to the left of septum primum and open entirely into the LA cavity. 25 In our experience, the same is true in the ostium primum defect cases with a very small LA. There are two other malformations that allow the right pulmonary veins to drain into the RA and these need to be differentiated from the cases of atrial septal malposition because they require different surgical treatment: (1) sinus venosus defects of the RA type 15 with unroofing of the right pulmonary veins; and (2) large ostium secundum defects extending into the posterior border of the atrial septum, allowing the right pulmonary veins to drain into the RA, although they are normally connected with the LA.26- 28 The characteristics of these three defects, which make differentiation among them relatively easy, are presented in Table 4. The high incidence of visceral heterotaxy with polysplenia in the patients of this study is not Clinical Investigations

surpnsmg because patients with polysplenia are known to have absence of the superior limbic band 18 (septum secundum) but not of the septum primum. The rare occurrence of this type of pulmonary venous drainage in patients with asplenia is probably due to the following two reasons: (1) patients with asplenia have a very high incidence of total pulmonary venous connection to a systemic vein; 13.l 4 •22 and (2) the hearts of patients with asplenia, as a rule, have absence of both septum primum and septum secundum. The single postmortem case of asplenia included in this series had a well-developed septum primum with multiple fenestrations, a rare finding for asplenia (Fig 4). Although most cases in our study (30 of 36 [83%]) had either postmortem-documented polysplenia or findings strongly suggestive of polysplenia (ie, interrupted IVC ±bilateral SVCs, AV discordance without transposition, ectopic atrial pacemakers, or complete AV block), at least three living patients had no detectable signs of visceral heterotaxy. This has been true in other reported cases.l9,29,30 It has been documented repeatedly 13,l 4,31-36 that ectopic atrial pacemakers, junctional rhythm, and complete AV block occur in heterotaxic patients with polysplenia and interrupted IVC. This was true for the patients of this study as well. Preoperative ECGs were available in 30 patients, and 26 of these (87%) had either atrial arrhythmias (22 cases) or complete AV block (4 cases). The other 4 cases had normal sinus rhythm. The presence of an ectopic atrial pacemaker or complete AV block in the ECG should warn the cardiologist about the possibility of visceral heterotaxy with probable polysplenia and interrupted IVC. In such patients, it is very important to accurately evaluate the position of the atrial septum echocardiographically. If all the pulmonary veins and all the systemic veins enter the same atrium, the incorrect diagnosis of a common atrium may be made with disadvantageous consequences for the patient. This was the case in two of the postmortem cases of our study in which the displaced septum primum was not identified and was not resected, thereby excluding blood flow into the small left atrium, left ventricle, and aorta-resulting in death. Surgical treatment can be very successful in the cases in which biventricular repair is possible if the correct diagnosis is established preoperatively. In the cases with solitus atria, ventricles, and great arteries, the malpositioned septum primum should be completely resected and a new appropriately positioned septum should be constructed. Incomplete resection of septum primum may result in pulmonary venous obstruction .37 In the cases with AV discordance and normally related great arteries, the baffling of the

systemic or pulmonary venous pathways may be individualized according to the presence of one or two SVCs, a large coronary sinus, interrupted IVC, and ipsilateral or totally right atrial pulmonary veins. Baffles to convey pulmonary venous return to the ventricle connected with the aorta must be carefully constructed to avoid pulmonary venous obstruction . The same is true for baffles conveying the systemic venous return to the right ventricle. In our experience, baffles that course very close to the orifices of the pulmonary veins may promote fibrous reaction, which results in progressive stenosis of these orifices. In conclusion, the cardinal features of partially or totally anomalous pulmonary venous drainage directly into the RA in the absence of a sinus venosus defect were the following: (1) The pulmonary venous connections with the atrial wall are externally normal. (2) The superior limbic band of septum secundum is markedly underdeveloped or absent, permitting malposition of septum primum toward the morphologically LA. (3) This malposition of septum primum allows half or all of the pulmonary veins to drain into the RA. (4) This constellation of malformations frequently is associated with visceral heterotaxy (mostly with polysplenia, and occasionally with asplenia or a normal spleen) . In our experience, 2-D echocardiography with Doppler interrogation provides a very reliable method for the diagnosis of this malformation. The preoperative realization of the true nature of this anomaly facilitates its successful surgical management. ACKNOWLEDGMENTS: We would like to express our great appreciation to Dr. F. Shiels of the Medical College of Virginia, Virginia Commonwealth University, Dr. Luis Alday of the National University of Cordoba, Argentina, Dr. Thomas Hougen and Dr. S. Farrell of the Children's National Medical Center, The George Washington University, and Dr. R. Doroshow of HarborUCLA Medical Center, UCLA School of Medicine, for providing five of the postmortem cases for this report. We would like to thank Gloria Gaskill for typing the manuscri{Jt, Terry Higgins for photography of the heart specimens, and Emily Mcintosh for art work. REFERENCES

1 Brown AJ. The development of the pulmonary vein in the domestic cat. Anat Record 1913; 7:299-330 2 Davies F, MacConaill MA. Cor biloculare, with a note on the development of the pulmonary veins. J Anat Lond 1937; 71:437-46 3 Streeter GL. Developmental horizons in human embryos: description of age group XV, XVI, XVII, XVIII, third issue. Contrib Embryo! Carneg Inst 1948; 32:145-46 4 Auer J. The development of the human pulmonary vein and its major variations. Anat Rec 1948; 101:581-94 5 Butler H. Some derivatives of the foregut venous plexus of the albino rat, with reference to man. J Anat Lond 1952; 86:95-109 6 Neill CA. Development of the pulmonary veins: with reference to the embryology of anomalies of pulmonary venous return. Pediatrics 1956; 18:880-87 7 Van Praagh R, Corsini I. Cor triatriatum : pathologic anatomy and a consideration of morphogenesis based on 13 postmortem CHEST / 107 16 1 JUNE, 1995

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cases and a study of normal development of the pulmonary vein and atrial septum in 83 human embryos. Am Heart J 1969; 78:379-405 Kutsche LM, Van Mierop LHS. Development of the pulmonary vein in the American alligator (alligator mississippiensis). Anat Rec 1988; 222:170-76 Terwolbeck K, Rammos S, Wenink ACG. Early development and location of the central pulmonary vein. Cardiol Young 1993; 3(suppl 1):126 Odgers PNB. The formation of the venous valves, the foramen secundum and the septum secundum in the human heart. J Anat 1935; 69:412-24 Christie GA. The development of the limbus fossae ovalis in the human heart-a new septum. J Anat Lond 1936; 97:45-54 Licata RH. The human embryonic heart in the ninth week. Am J Anat 1954; 94:73-125 Van Praagh S, Kreutzer J, Alday L, eta!. Systemic and pulmonary venous connections in visceral heterotaxy, with emphasis on the diagnosis of atrial situs: astudy of 109 postmortem cases. In: Clark E, Takao A, eds: Developmental cardiology: morphogenesis and function. Mt Kisco, NY: Futura, 1990; 671-721 Van Praagh S, Santini R, Sanders SP. Cardiac malpositions with special emphasis on visceral heterotaxy (asplenia and polysplenia syndromes). In: Fyler DC, ed: Nadas' pediatric cardiology. 1st ed. Philadelphia: Hanley & Belfus, 1991; 589-608 Van Praagh S, Carrera ME, Sanders SP, et al. Sinus venosus defects: unroofing of the right pulmonary veins: anatomic and echocardiographic findings and surgical treatment. Am Heart J 1994; 128:365-79 Van Mierop LHS. Morphologic development of the heart. In: Berne RM, ed. Handbook of physiology, section 2: the cardiovascular system I. Baltimore: Williams & Wilkins, 1979; 1-28 Edwards JE. Symposium on anomalous pulmonary venous connection (drainage): pathologic and developmental considerations in anomalous pulmonary venous connection. Proc Staff Meetings Mayo Clin 1953; 28:441-52 Moller JH, Nakib A, Anderson RC, et a!. Congenital cardiac disease associated with polysplenia: a developmental complex of bilateral 'left-sidedness.' Circulation 1967; 36:789-99 Cochrane AD, Menahem S, Mee RBB. Divided left atrium with absence of the interatrial septum in monozygotic twins. Cardiol Young 1993; 3:51-4 Abbott ME. Atlas of congenital cardiac disease. New York: American Heart Association, 1936; 58-9 DeLisle G, Ando M, Calder AL, et al. Total anomalous pulmonary venous connection: report of 93 autopsied cases with emphasis on diagnostic and surgical considerations. Am Heart J 1976; 91:99-122 Van Mierop LHS, Gessner IH, Schiebler GL. Asplenia and polysplenia syndromes. Birth Defects 1972; 8:36-44

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23 Utley JR, Noonan JA, Walters LR, et al. Anomalous position of atrial septum with anomalous pulmonary and systemic venous drainage: correction including ligation of persistent left superior vena cava. J Thorac Cardiovasc Surg 1974; 67:730-32 24 Seliem MA, Chin AJ, orwood WI. Patterns of anomalous pulmonary venous connection/ drainage in hypoplastic left heart syndrome: diagnostic role of Doppler color flow mapping and surgical implications. J Am Coli Cardiol l992; 19:134-41 25 Bharati S, Lev M. The surgical anatomy of hypoplasia of aortic tract complex. J Thorac Cardiovasc Surg 1984; 88:97-101 26 Neptune WB, Bailey CP, Goldberg H. The surgical correction of atrial septal defects associated with transposition of the pulmonary veins. J Thorac Surg 1953; 25:623-34 27 Billig DM, Peguero FA. Total anomalous pulmonary venous return: successful total correction in a 44-year-old man with subtotal absence of interatrial septum, tricuspid insufficiency, and cardiac dextroversion. Chest 1976; 69:687-90 28 Hilwig RW, Bishop SP. Anomalous pulmonary venous return in a Great Dane. Am J Vet Res 1975; 36:229-33 29 Winter ST, Ehrenfeld EN, Feldman J. Total drainage of pulmonary veins into the right atrium. Arch Dis Child 1952; 27:539-41 30 Frye RL, Krebs M, Rahimtoola SH, et al. Partial anomalous pulmonary venous connection without atrial septal defect. Am J Cardioll968; 22:242-50 31 Hastreiter AR, Rodriguez-Coronel A. Anomalous inferior vena cava with azygos continuation, high (sinus venosus) atrial septal defect and alterations of sinoatrial rhythm. Am J Cardiol 1968; 21:575-81 32 Momma K, Linde LM. Abnormal P wave axis in congenital heart disease associated with asplenia and polysplenia. J E lectrocardioll969; 2:395-402 33 Momma K, Linde LM. Cardiac rhythms in dextrocardia. Am J Cardioll970; 25:420-27 34 Frt>edom RM. Ellison RC. Coronary sinus rhythm in the polysplenia syndrome. Chest 1973; 63:952-58 35 Vander Horst RL, Gotsman MS. Abnormalities of atrial depolarization in infradiaphragmatic interruption of inferior vena cava. Br Heart J 1972; 34:295-300 36 Garcia OL, Mehta AV, Pickoff AS, et al. Left isomerism and complete atrioventricular block: a report of six cases. Am J Cardioll981; 48:1103-07 37 Turley K, Tarnoff H, Snider R, et al. Repair of combined total anomalous pulmonary venous connection and anomalous systemic connection in early infancy. Ann Thorac Surg 1980; 31:70-7 38 Van Praagh S, Kakou-Guikahue M, Kim H-S, et al. Atrial situs in patients with visceral heterotaxy and congenital heart disease: conclusions based on findings in 104 postmortem cases. Coeur 1988; 19:484-502

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{1995} October 29- November 2, 1995 New York, New York The Sixty-First Annual International Scientific Assembly

American College ofChest Physiciam

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Clinical Investigations