Pediatr Cardiol t3:187-189, 1992
Pediatric Cardiology ,~ Springer-Verlag New York Inc. 1992
Total Anomalous Pulmonary Venous Connection: Persistence and Atresia of the Common Pulmonary Vein M a r k W. B e c h e r , J Sol R o c k e n m a c h e r , z a n d Miguel M a r i n - P a d i l l a , ~ Departments of ~Pathology and :Pediahics, Dartmouth Medical School, Hanover, New Hampshire, USA
SUMMARY. A unique patient with subdiaphragmatic total anomalous pulmonary venous connection (TAPVC) in whom individual pulmonary veins drain into a myocardium-encircled saccular confluence, which may represent a persistent and atretic common pulmonary vein (CPV), is presented. KEY WORDS: Total anomalous pulmonary venous c o n n e c t i o n - Common pulmonary vein - - Congenital cardiac defects - - Heart specimen
Total anomalous pulmonary venous connection and d r a i n a g e ( T A P V C ) is a rare form of c o n g e n i t a l heart d i s e a s e in which the c o m m o n p u l m o n a r y vein (CPV) is c o n s i d e r e d to be a b s e n t a n d the p u l m o n a r y venous plexus maintains persistent embryologic a n a s t o m o s e s with s y s t e m i c v e i n s [1-4], T h e s e conn e c t i o n s c a n be at s u p r a c a r d i a c , c a r d i a c , or subd i a p h r a g m a t i c levels c o r r e s p o n d i n g to a n t e r i o r cardinal, s i n u s v e n o s u s , a n d o m p h a l o m e s e n t e r i c r e m n a n t s , r e s p e c t i v e l y . W e report here a case of s u b d i a p h r a g m a t i c T A P V C with d r a i n a g e into the portal v e i n in w h i c h there is ,evidence to suggest that the " a n o m a l o u s " vertical vein may in tact repr e s e n t a p e r s i s t e n t , a b n o r m a l l y c o n n e c t e d , CPV.
Case Report The patient was a 16-day-old female infant delivered at term without complications and an uneventful perinatal period. She became acutely cyanotic while being fed and despite resuscitation measures expired. Autopsy revealed TAPVC with drainage into the portal vein via a long vertical vein (Fig. IA and B). The cranial aspect of this vertical vein consisted of a saccular structure which lay posterior to the base of the heart without recognizable connection to the heart and was encircled by brown tissue resembling myocardium (Fig. 2). This saccular confluence received two veins from the left upper lobe and a single vein from the right upper lobe superiorly, as well as a vein from the right middle lobe inferiorly. Veins from the: left and right lower lobes
Address offprint requests to: Dr. Miguel Marin-Padilla, Depart-
ment of Pathology, Dartmouth Medical School, Hanover, NH 03756, USA.
joined the vertical vein distal to the saccular dilatation prior to crossing the diaphragm to the left of the esophagus, lnfradiaphragmatically, the vertical vein joined lhe portal vein in continuity with the superior mesenteric and splenic veins. The remainder of the systemic venous sytem was normal. The heart had normally interrelated chambers, right atrial and ventricular dilatation and hypertrophy, a small left atrium and ventricle, a large patent foramen ovale, and an intact ventricular septum. The apex was formed by the markedly enlarged right ventricle and the great vessels were normally placed. The pulmonary and systemic arterial systems were intact with a long, patent ductus arteriosus distal to the left subclavian artery. The lungs had prominent subpleural varicosities and severe congestion. There was hepatosplenomegaly with marked congestion and approximately 20 ml of serous ascites in the peritoneum. The remainder of the internal organs were normal with proper relationships. Microscopic examination of the saccular confluence of the anomalous vertical vein showed a central layer of striated cardiac muscle overlying a thin layer of connective tissue endocardium and surrounded by loose vascular connective tissue. Sections taken from the distal aspect of the saccu[ar confluence showed merging of this laminated wall with normal vein.
Discussion In o r d e r to u n d e r s t a n d d e v e l o p m e n t a l a b n o r m a l i t i e s o f the C P V , i n c l u d i n g cor t r i a t r i a t u m , partial a n o m alous p u l m o n a r y v e n o u s c o n n e c t i o n , and T A P V C , m u c h w o r k has c e n t e r e d o n the m o r p h o g e n e s i s of the C P V [1, 5, 6]. it has b e e n s h o w n that the C P V d e v e l o p s as a n o u t g r o w t h o f the dorsal atrial wall w h i c h c o n t a c t s the p u l m o n a r y v e n o u s plexus a n d is e v e n t u a l l y i n c o r p o r a t e d into the left a t r i u m . I n cor t r i a t r i a t u m a third a t r i u m - l i k e c h a m b e r is c r e a t e d
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Pediatric Cardiology Vol. 13, No. 3, 1992
Fig. I. Infradiaphragmatic TAPVC with saccular confluence (S) encircled by myocardium (persistent CPV) connected to the vertical vein (VV) which drains into the portal vein (PV). (A) Posterior view of the internal organ block showing native location of saccular confluence, vertical vein, inferior vena cava (1VC), and trachea (T), Prominent subpleural venous varicosities are marked by large white arrows. The saccular confluence and individual pulmonary veins are detailed in Fig. 2. (B) Reflected right lung (R) is shown revealing the anterior aspect of the saccular confluence and the heart. The probe enters the superior vena cava, and the right atrium (RA) has been opened. L, left lung.
Fig. 2. Detail of opened saccular confluence (S), representing persistent CPV from posterior, showing cardiac muscle with atrium-like fenestrations and continuity with vertical vein (VV). Pulmonary veins from left (L) and right (R) lungs are labeled as follows: L1,2, left upper lobe; L3, left lower lobe; R1, right upper lobe; R2, right middle lobe; R3, light lower lobe, T, trachea. The four pins are for positioning only.
most likely by the incomplete incorporation of the CPV into the left atrium with a resultant dividing membrane [6]. Partial anomalous pulmonary venous connection [ 1] and TAPVC, on the other hand, are felt to be due to the abnormal development of the CPV with resultant incomplete and absent communication with the left atrium, respectively, and persistance of embryologic pulmonary-systemic venous anastomoses. While several cases of TAPVC have been reported where there is an atretic cord-like remnant present in the proper location, which may represent an atretic common pulmonary vein [I, 2, 4], the majority of cases have been best explained by either agenesis or involution of the CPV [1]. The presence of myocardium within the saccular confluence of the "anomalous" vertical vein of the present case suggests that it must have been in continuity with the heart at one time. Thus, the CPV began to develop normally, but lost this connection at a time when pulmonary-systemic (specifically, omphalomesenteric) venous anastomoses were still patent. This saccular confluence encircled by myocardium may, therefore, be an example of a persistent CPV with an abnormal connection. If so, it would be most accurate to conclude that this case of TAPVC resulted from atresia of the CPV rather than agenesis. In our search of the literature, we found three
Becher et al.: Total Anomalous Pulmonary Venous Connection
189
cases of TAPVC which had briel[ descriptions of a sac-like region of the anomalous vein [3] and only a single case of TAPVC with a similar saccular confluence encircled by myocardium [2]. The latter was described by Edwards et al. in 1951 [2] as an example of atresia of the CPV with TAPVC to the superior vena cava (case 3). The case presented in this report, with infradiaphragmatic TAPVC and a myocardium-encircled remnant of the CPV, supports atresia (up to complete involution) of the CPV as an important mechanism for the development of TAPVC. It also raises the possibility that atresia may have occurred in many cases of TAPVC, although morphologic evidence of this has been lost and it is not possible to exclude agenesis in many of these cases. Perhaps the present case, together with renewed analysis of the previously reported supracardiac TAPVC case of Edwards et al. [2], will further contribute to our understanding of the morphogenesis of this unusual cardiac malformation.
rological and Communicative Disorders and Stroke, grant NS22897, NIH.
Acknowledgments. We would like to thank Drs. Stella and Richard Van Praagh for their insightful observations and discussion of this case. This work was supported by the National Institute of Neu-
References l. Delisle G, Ando M, Calder AL, Zuberbuhler JR, Rochenmacher S, Alday LE, Mangini O, Van Praagh S, Van Praagh R (1976) Total anomalous pulmonary venous connection: report of 93 autopsied cases with emphasis on diagnostic and surgical considerations. Am Heart J 91:99-122 2. Edwards JE, DuShane JW, Alcott DL, Burchell HB (1951) Thoracic venous anomalies: III. Atresia of the common pulmonary vein, the pulmonary veins draining wholly into the superior vena cava: IV. Stenosis of the common pulmonary vein (cor triatriatum). Arch Patho151:446-460 3. Kanffman SL, Ores CN, Andersen DH (1962) Two cases of total anomalous pulmonary venous return of the supracardiac type with stenosis simulating infradiaphragmatic drainage. Circulation 25:376-382 4. Lucas RV, Woolfrey BF, Anderson RC, Lester RG, Edwards JE (1962) Atresia of the common pulmonary vein. Pediatrics 29:729-739 5. Neill CA (1956) Development of the pulmonary veins: with reference to the embryology of anomalies of pulmonary venous return. Pediatrics 18:880-887 6. Van Praagh R, Corsini I (1969) Cor triatriatum: pathologic anatomy and a consideration of morphogenesis based on 13 postmortem cases and a study of normal development of the pulmonary vein and atrial septum in 83 human embryos. Am Heart J 78:379-405
Pediatric Cardiology ,~ Springer-Verlag New York Inc. 1992
Total Anomalous Pulmonary Venous Connection: Persistence and Atresia of the Common Pulmonary Vein M a r k W. B e c h e r , J Sol R o c k e n m a c h e r , z a n d Miguel M a r i n - P a d i l l a , ~ Departments of ~Pathology and :Pediahics, Dartmouth Medical School, Hanover, New Hampshire, USA
SUMMARY. A unique patient with subdiaphragmatic total anomalous pulmonary venous connection (TAPVC) in whom individual pulmonary veins drain into a myocardium-encircled saccular confluence, which may represent a persistent and atretic common pulmonary vein (CPV), is presented. KEY WORDS: Total anomalous pulmonary venous c o n n e c t i o n - Common pulmonary vein - - Congenital cardiac defects - - Heart specimen
Total anomalous pulmonary venous connection and d r a i n a g e ( T A P V C ) is a rare form of c o n g e n i t a l heart d i s e a s e in which the c o m m o n p u l m o n a r y vein (CPV) is c o n s i d e r e d to be a b s e n t a n d the p u l m o n a r y venous plexus maintains persistent embryologic a n a s t o m o s e s with s y s t e m i c v e i n s [1-4], T h e s e conn e c t i o n s c a n be at s u p r a c a r d i a c , c a r d i a c , or subd i a p h r a g m a t i c levels c o r r e s p o n d i n g to a n t e r i o r cardinal, s i n u s v e n o s u s , a n d o m p h a l o m e s e n t e r i c r e m n a n t s , r e s p e c t i v e l y . W e report here a case of s u b d i a p h r a g m a t i c T A P V C with d r a i n a g e into the portal v e i n in w h i c h there is ,evidence to suggest that the " a n o m a l o u s " vertical vein may in tact repr e s e n t a p e r s i s t e n t , a b n o r m a l l y c o n n e c t e d , CPV.
Case Report The patient was a 16-day-old female infant delivered at term without complications and an uneventful perinatal period. She became acutely cyanotic while being fed and despite resuscitation measures expired. Autopsy revealed TAPVC with drainage into the portal vein via a long vertical vein (Fig. IA and B). The cranial aspect of this vertical vein consisted of a saccular structure which lay posterior to the base of the heart without recognizable connection to the heart and was encircled by brown tissue resembling myocardium (Fig. 2). This saccular confluence received two veins from the left upper lobe and a single vein from the right upper lobe superiorly, as well as a vein from the right middle lobe inferiorly. Veins from the: left and right lower lobes
Address offprint requests to: Dr. Miguel Marin-Padilla, Depart-
ment of Pathology, Dartmouth Medical School, Hanover, NH 03756, USA.
joined the vertical vein distal to the saccular dilatation prior to crossing the diaphragm to the left of the esophagus, lnfradiaphragmatically, the vertical vein joined lhe portal vein in continuity with the superior mesenteric and splenic veins. The remainder of the systemic venous sytem was normal. The heart had normally interrelated chambers, right atrial and ventricular dilatation and hypertrophy, a small left atrium and ventricle, a large patent foramen ovale, and an intact ventricular septum. The apex was formed by the markedly enlarged right ventricle and the great vessels were normally placed. The pulmonary and systemic arterial systems were intact with a long, patent ductus arteriosus distal to the left subclavian artery. The lungs had prominent subpleural varicosities and severe congestion. There was hepatosplenomegaly with marked congestion and approximately 20 ml of serous ascites in the peritoneum. The remainder of the internal organs were normal with proper relationships. Microscopic examination of the saccular confluence of the anomalous vertical vein showed a central layer of striated cardiac muscle overlying a thin layer of connective tissue endocardium and surrounded by loose vascular connective tissue. Sections taken from the distal aspect of the saccu[ar confluence showed merging of this laminated wall with normal vein.
Discussion In o r d e r to u n d e r s t a n d d e v e l o p m e n t a l a b n o r m a l i t i e s o f the C P V , i n c l u d i n g cor t r i a t r i a t u m , partial a n o m alous p u l m o n a r y v e n o u s c o n n e c t i o n , and T A P V C , m u c h w o r k has c e n t e r e d o n the m o r p h o g e n e s i s of the C P V [1, 5, 6]. it has b e e n s h o w n that the C P V d e v e l o p s as a n o u t g r o w t h o f the dorsal atrial wall w h i c h c o n t a c t s the p u l m o n a r y v e n o u s plexus a n d is e v e n t u a l l y i n c o r p o r a t e d into the left a t r i u m . I n cor t r i a t r i a t u m a third a t r i u m - l i k e c h a m b e r is c r e a t e d
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Pediatric Cardiology Vol. 13, No. 3, 1992
Fig. I. Infradiaphragmatic TAPVC with saccular confluence (S) encircled by myocardium (persistent CPV) connected to the vertical vein (VV) which drains into the portal vein (PV). (A) Posterior view of the internal organ block showing native location of saccular confluence, vertical vein, inferior vena cava (1VC), and trachea (T), Prominent subpleural venous varicosities are marked by large white arrows. The saccular confluence and individual pulmonary veins are detailed in Fig. 2. (B) Reflected right lung (R) is shown revealing the anterior aspect of the saccular confluence and the heart. The probe enters the superior vena cava, and the right atrium (RA) has been opened. L, left lung.
Fig. 2. Detail of opened saccular confluence (S), representing persistent CPV from posterior, showing cardiac muscle with atrium-like fenestrations and continuity with vertical vein (VV). Pulmonary veins from left (L) and right (R) lungs are labeled as follows: L1,2, left upper lobe; L3, left lower lobe; R1, right upper lobe; R2, right middle lobe; R3, light lower lobe, T, trachea. The four pins are for positioning only.
most likely by the incomplete incorporation of the CPV into the left atrium with a resultant dividing membrane [6]. Partial anomalous pulmonary venous connection [ 1] and TAPVC, on the other hand, are felt to be due to the abnormal development of the CPV with resultant incomplete and absent communication with the left atrium, respectively, and persistance of embryologic pulmonary-systemic venous anastomoses. While several cases of TAPVC have been reported where there is an atretic cord-like remnant present in the proper location, which may represent an atretic common pulmonary vein [I, 2, 4], the majority of cases have been best explained by either agenesis or involution of the CPV [1]. The presence of myocardium within the saccular confluence of the "anomalous" vertical vein of the present case suggests that it must have been in continuity with the heart at one time. Thus, the CPV began to develop normally, but lost this connection at a time when pulmonary-systemic (specifically, omphalomesenteric) venous anastomoses were still patent. This saccular confluence encircled by myocardium may, therefore, be an example of a persistent CPV with an abnormal connection. If so, it would be most accurate to conclude that this case of TAPVC resulted from atresia of the CPV rather than agenesis. In our search of the literature, we found three
Becher et al.: Total Anomalous Pulmonary Venous Connection
189
cases of TAPVC which had briel[ descriptions of a sac-like region of the anomalous vein [3] and only a single case of TAPVC with a similar saccular confluence encircled by myocardium [2]. The latter was described by Edwards et al. in 1951 [2] as an example of atresia of the CPV with TAPVC to the superior vena cava (case 3). The case presented in this report, with infradiaphragmatic TAPVC and a myocardium-encircled remnant of the CPV, supports atresia (up to complete involution) of the CPV as an important mechanism for the development of TAPVC. It also raises the possibility that atresia may have occurred in many cases of TAPVC, although morphologic evidence of this has been lost and it is not possible to exclude agenesis in many of these cases. Perhaps the present case, together with renewed analysis of the previously reported supracardiac TAPVC case of Edwards et al. [2], will further contribute to our understanding of the morphogenesis of this unusual cardiac malformation.
rological and Communicative Disorders and Stroke, grant NS22897, NIH.
Acknowledgments. We would like to thank Drs. Stella and Richard Van Praagh for their insightful observations and discussion of this case. This work was supported by the National Institute of Neu-
References l. Delisle G, Ando M, Calder AL, Zuberbuhler JR, Rochenmacher S, Alday LE, Mangini O, Van Praagh S, Van Praagh R (1976) Total anomalous pulmonary venous connection: report of 93 autopsied cases with emphasis on diagnostic and surgical considerations. Am Heart J 91:99-122 2. Edwards JE, DuShane JW, Alcott DL, Burchell HB (1951) Thoracic venous anomalies: III. Atresia of the common pulmonary vein, the pulmonary veins draining wholly into the superior vena cava: IV. Stenosis of the common pulmonary vein (cor triatriatum). Arch Patho151:446-460 3. Kanffman SL, Ores CN, Andersen DH (1962) Two cases of total anomalous pulmonary venous return of the supracardiac type with stenosis simulating infradiaphragmatic drainage. Circulation 25:376-382 4. Lucas RV, Woolfrey BF, Anderson RC, Lester RG, Edwards JE (1962) Atresia of the common pulmonary vein. Pediatrics 29:729-739 5. Neill CA (1956) Development of the pulmonary veins: with reference to the embryology of anomalies of pulmonary venous return. Pediatrics 18:880-887 6. Van Praagh R, Corsini I (1969) Cor triatriatum: pathologic anatomy and a consideration of morphogenesis based on 13 postmortem cases and a study of normal development of the pulmonary vein and atrial septum in 83 human embryos. Am Heart J 78:379-405
