World Journal for Pediatric and

Congenital Heart Surgery http://pch.sagepub.com/

Anomalous Pulmonary Venous Connections and Related Anomalies : Nomenclature, Embryology,

Anatomy, and Morphology
Michael J. Walsh, Ross M. Ungerleider, Vera D. Aiello, Diane Spicer and Jorge M. Giroud
World Journal for Pediatric and Congenital Heart Surgery 2013 4: 30
DOI: 10.1177/2150135112458439

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Proceedings of the WSPCHS Symposium on Anomalies of the Pulmonary Veins

World Journal for Pediatric and

Congenital Heart Surgery
Anomalous Pulmonary Venous 4(1) 30-43
ª The Author(s) 2012
Reprints and permission:
Connections and Related Anomalies: sagepub.com/journalsPermissions.nav
DOI: 10.1177/2150135112458439
Nomenclature, Embryology, Anatomy, and pch.sagepub.com

Morphology

Michael J. Walsh, MD1, Ross M. Ungerleider, MD1,

Vera D. Aiello, MD2, Diane Spicer, BS3,4 and Jorge M. Giroud, MD3

Abstract
This article combines material from three complementary overviews presented in the Symposium on Pulmonary Venous
Anomalies during the Joint Meeting of the World Society for Pediatric and Congenital Heart Surgery and Sociedad Latina de
Cardiologia y Cirugia Cardiovascular Pediátrica in Lima, Peru. We discuss the embryologic basis for nomenclature, the
hierarchical diagnostic categories, and the important anatomic and morphologic characteristics of anomalous pulmonary venous
connections. The anatomic descriptions help to guide an understandable and sensible approach to the diagnosis and surgical
management of these various disorders.

Keywords
congenital heart disease, Internet, cardiac encyclopedia, cardiac images, archiving working group, international pediatric and
congenital cardiac code, the international society for nomenclature of paediatric and congenital heart disease, total anomalous
pulmonary venous connections

Submitted May 08, 2012; accepted July 17, 2012.

Presented at the joint meeting of the World Society for Pediatric and Congenital Heart Surgery and Sociedad Latina de Cardiologı́a y Cirurgı́a Cardi-
ovascular Pediátrica, Lima, Peru; March 19, 2012.

Introduction Congenital Cardiac Code (IPCCC). The IPCCC is the end

Pulmonary venous anomalies comprise a broad spectrum of
relatively uncommon disorders of cardiac development. It has
long been appreciated that this varied group of malformations
is best understood by consideration of the embryologic basis of
each anomaly.1-4 There has been some controversy about the
embryological origin of the pulmonary veins. The main point
of discordance is whether or not the pulmonary venous primor-
dium belongs to the embryonic sinus venosus.5,6 Recent
observations, based on molecular and three-dimensional analy-
ses of human embryos, support the idea that the systemic and
pulmonary myocardial sleeves are derived from different pre-
cursors, and thus the primitive pulmonary vein represents a
new development at the venous pole of the embryonic heart
tube.6 Krabill, Lucas and colleagues have proposed a cogent,
all-inclusive classification of pulmonary venous anomalies that
follows from earlier embryologic work.7 A modification of this
classification is shown in Table 1 and serves as a foundation for
understanding the variety of anomalies that comprise the
spectrum of defects covered in this article.3
Currently, the most widely used system of nomenclature for
congenital cardiac anomalies is the International Pediatric and
result of the collaboration of many societies and members,
predominantly that of the European Association for Cardio-
Thoracic Surgery (EACTS), the Society of Thoracic Surgeons
(STS) and the Association for European Paediatric Cardiology
(AEPC). This system is promoted and maintained by the Inter-
national Society for Nomenclature of Paediatric and Congeni-
tal Heart Disease (ISNPCHD). The entire IPCCC is available
online (www.ipccc.net). The ISNPCHD has three working
1
Brenner Children’s Hospital, Wake Forest University Medical Center,
Winston Salem, NC, USA
2
Heart Institute (InCor), Sao Paulo University, School of Medicine, Sao Paulo,
Brazil
3
The Congenital Heart Institute of Florida (CHIF), Saint Petersburg and
Tampa, FL, USA
4
University of Florida College of Medicine, Gainesville, FL, USA
Corresponding Author:
Michael J. Walsh, Division of Pediatric Cardiology, Brenner Children’s Hospital,
Wake Forest University Medical Center, Medical Center Boulevard, Winston,
Salem, NC 27157, USA.
Email: mwalsh@wakehealth.edu

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Walsh et al 31

Abbreviations and Acronyms

AEPC Association for European Paediatric
Cardiology
ASDs atrial septal defects
AWG Archiving Working Group
CPT current procedural terminology
CT computerized tomography
DWG Definitions Working Group
EACTS European Association for Cardio-Thoracic
Surgery
EPCC European Paediatric Cardiac Code
ICD International Classification of Diseases
IPCCC International Pediatric and Congenital
Cardiac Code
ISNPCHD International Society for Nomenclature of
Paediatric and Congenital Heart Disease
MR magnetic resonance
NWG Nomenclature Working Group
PAPVC partially anomalous pulmonary venous
connection
STS Society of Thoracic Surgeons
TAPVC totally anomalous pulmonary venous
Figure 1. Left posterior view of a normal heart showing the opened
connection
left atrium, its body, vestibule, appendage, and the connection of the
pulmonary veins to its roof. This image is from the Web portal of
Table 1. An Embryologic Classification for Pulmonary Venous the Archiving Working Group of The International Society for
Anomalies. Nomenclature of Paediatric and Congenital Heart Disease
(ISNPCHD; http://ipccc-awg.net) and courtesy of Diane E. Spicer
I. Atresia of the common pulmonary vein (early) while pulmonary-to- BS, PA(ASCP) (The Congenital Heart Institute of Florida [CHIF]).
systemic venous connections are still present http://ipccc-awg.net/Normal_Heart/Left_Heart/Nl_Cor_Pos_LA_LV/
A. Partially anomalous pulmonary venous connection Nl_Cor_Pos_LA_Post.html.
B. Totally anomalous pulmonary venous connection
II. Atresia of the common pulmonary vein (late) after pulmonary-to- In some related anomalies, the word connection is some-
systemic venous connections are obliterated
A. Atresia of the common pulmonary vein
times replaced with ‘‘drainage’’ or ‘‘return.’’ Edwards has
III. Stenosis of the common pulmonary vein emphasized that drainage refers to a physiologic or hemody-
A. Cor triatriatum namic phenomenon, whereas connection refers to an anatomic
IV. Abnormal absorption of the common pulmonary vein into the left relationship.2 Pulmonary veins may be connected normally, but
atrium nonetheless drain abnormally. There are some situations when
A. Stenosis of individual pulmonary veins a vein or group of veins is normally connected to an atrial
B. Abnormal number of pulmonary veins chamber but the blood drains to a different vessel or chamber.
A classic example is the patency of the levoatrial cardinal vein,
which is the route for drainage of normally connected pulmon-
groups, one of which is the Archiving Working Group (AWG). ary veins in the setting of mitral stenosis or atresia and intact
The AWG collects images of all types which illustrate the spec- atrial septum.
trum of congenital cardiac malformations and presents them Another group of anomalies usually referred as causing par-
together with the corresponding codes contained within the tially anomalous pulmonary venous drainage is the sinus veno-
IPCCC. Examples of these images are included in this article sus defects. They are not recognized as true atrial septal defects
to help illustrate the various anomalies of pulmonary venous (ASDs) since they are located far from the confines of the atrial
connection. Further important and historical information septum. They will not be discussed in depth here, but we should
related to the development of the IPCCC is provided (see remember that the essence of the malformation is the anoma-
Appendix A). lous connection of right pulmonary vein/veins to one of the
caval veins, while still retaining their left atrial connection and
thus allowing interatrial communication.
For the purposes of this article, an abnormal connection of
Abnormal Connections of the Pulmonary Veins the pulmonary vein or veins is defined when one, some, or all
It is usually described that in the normal heart each one of the the pulmonary veins connect to a site other than the morpholo-
four pulmonary veins connects to one of the corners of the pul- gically left atrium. Additional information regarding the
monary venous component, at the roof of the morphologically laterality, the number of the abnormally connected veins, and
left atrium (Figure 1). the specific site of connection is used as complementary

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32 World Journal for Pediatric and Congenital Heart Surgery 4(1)

classification. The presence or absence of obstruction to the

venous drainage is important in the clinical setting and is
included in the classification hierarchy for some defects.
In instances where the pulmonary veins connect predomi-
nantly to the right atrium or systemic venous system, an intera-
trial communication is almost invariably present, so that the
venous return can reach the left-sided cardiac chambers.
In the presence of atrial isomerism, the venoatrial connec-
tions are highly variable and must be described rather than
considered as a marker of the atrial situs or arrangement. For
example, in the presence of isomerism of the right atrial appen-
dages, even if all the veins connect at the roof of one of the
atrial chambers, it is considered to be anomalous, since the
atrium which receives the veins is not the morphologically left
atrium.

Partially Anomalous Pulmonary Venous Connection

(IPCCC: 04.07.01)
Partially anomalous pulmonary venous connection (PAPVC)
has been noted in 0.6% to 0.7% of autopsies, but clinical stud-
ies have noted fewer such occurrences.7 As the number of
permutations of anomalously draining pulmonary veins and
their site of connection is quite large, no concise classification
system has been proposed for this disorder. Unlike the require- Figure 2. Chest radiograph in a patient with Scimitar syndrome.
ment for the presence of an interatrial communication (to Note the rightward displacement of the cardiac silhouette within the
provide flow to the left heart) in cases of total anomalous chest cavity. Anomalous pulmonary venous return (arrows), draining
pulmonary venous connection, an interatrial communication to the inferior caval vein, resembles a curved sword.
may or may not be present with PAPVC.
One subgroup of PAPVC, which has received separate
attention in the literature, is that of Scimitar syndrome. This
is a group of anomalies in which the right pulmonary vein/veins
connect anomalously to the inferior caval vein or to the right
atrium at the insertion of the inferior caval vein. The name of
the syndrome arose because the descending vertical vein
resembles a scimitar, or curved sword, on the frontal chest
radiograph (Figure 2). Scimitar syndrome is frequently associ-
ated with hypoplasia of the right lung (along with bronchial
anomalies), dextroposition and/or dextrorotation of the heart,
hypoplasia of the right pulmonary artery, and anomalous
subdiaphragmatic systemic arterial supply to the lower lobe
of the right lung directly from the aorta or its main branches
(Figure 3). Some would require the presence of these
associated anomalies to make the diagnosis of the Scimitar
‘‘syndrome,’’ while others would require only the presence of
the abnormal pulmonary venous connection from the right lung Figure 3. In this anatomical specimen, the hypoplastic right lung has a
to the inferior caval vein.8,9 vein (arrow) connecting to the inferior caval vein just before it joins
The PAPVC can also occur in non-Scimitar anatomy such as the right atrium, in an example of the scimitar syndrome. RAA indi-
when the left pulmonary veins connect to the systemic circula- cates right atrial appendage.
tion via the innominate vein, or when some (or all) of the right
pulmonary veins connect abnormally to the superior caval vein Totally Anomalous Pulmonary Venous Connection
(as is occasionally seen in some forms of sinus venosus ASD
with PAPVC) or even directly to the right atrium.
(IPCCC: 04.08.05)
The hierarchical description of PAPVC is that it is either (a) Totally anomalous pulmonary venous connection (TAPVC) is
Scimitar or (b) non-Scimitar. an uncommon congenital cardiac anomaly. In TAPVC, all of

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Walsh et al 33

Figure 4. Subtypes of totally anomalous pulmonary venous connection are based on the site of drainage of the common pulmonary venous
sinus (confluence).

the pulmonary veins connect anomalously with the right atrium
or to one or more of its venous tributaries. None of the
pulmonary veins connect normally to the left atrium. As
mentioned above, an interatrial communication is an obligatory
requirement in order for babies born with this defect to survive.
These disorders have a reported incidence that varies between
5.9 and 7.1 per 100 000 live births10 and comprise 1% to 5% of
cases of congenital heart disease in various series.3 There has
been a progressive improvement in outcomes and survival in
the recent era of surgical interventions.11 Among others, signif-
icant risk factors associated with postoperative death include
associated cardiac lesions as well cardiac connection type,
earlier year of operation, earlier age at repair, single ventricle
anatomy (heterotaxy), obstructed, hypoplastic or stenotic
pulmonary veins, and postoperative pulmonary venous
obstruction.12,13
In a report published in 1957, Craig and colleagues
described TAPVC according to the site of connection, with the
four major types being (a) supracardiac; (b) intracardiac; (c)
infracardiac; and (d) mixed type. This is probably the most
widely used classification today14 and does not require
knowledge of embryology to understand (Figure 4).
Simply classifying the TAPVC by site of anatomic connec-
tion, however, is not sufficient. In some cases (more often for
those connections below the diaphragm), there is obstruction
to the pulmonary venous drainage, and this has important
consequences in terms of management and prognosis. When
obstruction is present, it can occur at various levels (Table 2).

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34 World Journal for Pediatric and Congenital Heart Surgery 4(1)

Table 2. Possible Sites of Obstruction in Patients With TAPVC.

I. At the interatrial septum

II. Within the anomalous channel
A. Intrinsic narrowing
B. Obstruction secondary to a long channel length
C. Extrinsic narrowing
1. At the diaphragm
2. At the ductus venosus
3. In the hepatic sinusoids
4. Between the left pulmonary artery and the left main stem
bronchus
5. Between the right pulmonary artery and the trachea
6. At the entry into the right superior caval vein

TOTAL ANOMALOUS PULMONARY VENOUS

1 CONNECTION

Type 1 (supracardiac) Type 2 (cardiac)

2 Type 3 (infracardiac) Type 4 (mixed)

3 Obstructed Non-Obstructed

Figure 5. Nomenclature hierarchy for TAPVC includes presence and Figure 6. Left superior view of the thoracic organs in a case with
location of obstruction. supracardiac totally anomalous pulmonary venous connection. The
vertical vein (VV) is submitted to extrinsic obstruction as it
Thus the full nomenclature hierarchy for TAPVC includes the runs between the left pulmonary artery (LPA) and the main left
nature of the obstruction, as depicted in Figure 5. Features that bronchus (LB).
are specific to each of the four types are described below.
An example of extrinsic stenosis is the course of the vertical
vein between the left main bronchus and the left pulmonary
artery (Figure 6). Intrinsic stenosis is defined when there is
focal or tubular narrowing of the venous channel carrying the
venous flow (Figure 7). The liver sinusoids are also considered
as a blockage to the venous return, because a capillary bed
interposes between the common venous channel and the right
atrium. A restrictive interatrial communication is functionally
an obstruction to the venous drainage to the left atrium.
The consequences to the lung vasculature in the presence of
obstructive drainage are disastrous and may be present even at
birth. Besides hypertrophy of intrapulmonary veins and dila-
tion of lymphatic vessels, the intra-acinar arteries are highly
muscularized, which leads to pulmonary hypertension and has
been shown to negatively impact surgical outcome.

Supracardiac (IPCCC: 04.06.00)

In this form of anomalous connection, the four pulmonary Figure 7. Detail of a vertical vein in a case of supracardiac totally
veins join together in a common venous center located behind anomalous pulmonary venous connection. There is discrete narrow-
the left atrium, from where a vertical vein usually takes origin ing of the venous channel (arrow), causing intrinsic obstruction.

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Walsh et al
Figure 8. Anterior view of an anatomical specimen in a case with the
supracardiac type of totally anomalous pulmonary venous connection.
The vertical vein (not shown) connected to the brachiocephalic vein
(BCV), which is hugely dilated and, in its turn, drains to the superior
caval vein (SCV).
to eventually reach the systemic circulation. This vertical vein
usually connects to the brachiocephalic vein, which in its
course joins to the superior caval vein (Figure 8). Over time,
the right-sided cardiac chambers, as well as the brachiocephalic
vein superior to the heart, become hugely dilated and form a
characteristic appearance on the thoracic radiograph that is
referred to as the snowman or 8 sign. The course of this vertical
vein is variable, as it may pass either anteriorly to the hilum of
the left lung (Figure 8) or between the left pulmonary artery
and left main bronchus—a condition that can cause extrinsic
obstruction to the venous drainage (Figure 6)
One morphological feature of the common venous conflu-
ence in supracardiac anomalous connection is that it is typically
oriented horizontally and it is usually short (Figure 9). Alterna-
tively, the vertical vein that originates from the common
venous confluence can take a different course, connecting
posteriorly to the azygous system (Figure 10) or directly to the
superior caval vein, taking an infratracheal course (Figure 11)
that runs between the carina and the right pulmonary artery,
which may be a possible site of extrinsic compression.
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35
Figure 9. The heart has been lifted up to show the common venous
center (asterisk) in a case with totally anomalous pulmonary venous
connection. In the supracardiac variant of the totally anomalous con-
nection, the venous center is usually short and horizontal. LA indicates
left atrium.
Cardiac (IPCCC: 04.08.10)
In this group, the pulmonary veins are connected to a cardiac
structure, as is the case when they connect to the coronary sinus
or directly to the right atrium.
Pulmonary venous connection to the coronary sinus
(Figure 12) results in massive dilation of this structure along its
course in the atrioventricular groove and of its opening into the
right atrium. Obstruction is rare in this form of anomalous
connection but may occur in the presence of a redundant
Thebesian valve or when the obligatory ASD is small. Direct
connection of all the pulmonary veins to the roof of the mor-
phologically right atrium is very rare.
Infracardiac (IPCCC: 04.08.20)
The infracardiac connection is most commonly associated with
isomerism of the right atrial appendages, although it may occur
in usual atrial arrangement (situs solitus) and in the mirror-
imaged atrial arrangement (situs inversus). The pulmonary
36
Figure 10. Posterior view of the thoracic organs in a case with totally
anomalous pulmonary venous connection of the supracardiac type.
The pulmonary veins are connected to the azygous vein. Note that the
common venous center is horizontal. Ao indicates descending aorta.
veins join together into a common vein, in a different fashion
when compared to the supracardiac variant. The veins usually
join sequentially the common channel, which is usually long
and vertical. This arrangement has potential surgical implica-
tions (Figure 13). The vertical vein passes through the
diaphragm and reaches a systemic vein inside the abdomen.
A common site of connection is the ductus venosus from the
fetal period, which directs the blood flow to the portal system
(Figure 14). Infracardiac variants are almost invariably stenotic
and present with obstruction. If not at the level of the dia-
phragm, the obstruction is represented by the liver capillary bed
that interposes between the pulmonary venous return and the
heart.
Anomalous Pulmonary Venous Connection of the Mixed
Type (IPCCC: 04.08.30)
In the mixed type of anomalous pulmonary venous connection,
the pulmonary veins join the systemic veins at two or more lev-
els (supracardiac, cardiac, or infracardiac; Figure 15). These
can be complex arrangements and it is important during the
diagnosis to define the connections of all the pulmonary veins.
The most common form of mixed type of TAPVC includes
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World Journal for Pediatric and Congenital Heart Surgery 4(1)
Figure 11. Right superior view of a specimen with supracardiac
totally anomalous pulmonary venous connection, showing the com-
mon vein (asterisk) running between the carina of the trachea and the
right pulmonary artery, in its way to connect to the superior caval vein
(SCV).
supracardiac connections from the left pulmonary veins via a
vertical vein to the brachiocephalic vein, and intracardiac
connections of the right pulmonary veins to the coronary sinus.
Atresia of the Common Pulmonary Vein (IPCCC:
04.08.02, Q1.01.58)
In this disorder, the pulmonary veins are normally formed and
connect normally to a pulmonary venous confluence that ends
blindly behind the left atrium. There is no connection between
this confluence and either the left atrium or the systemic
veins.15 This is a rare disorder that typically presents with
severe cardiorespiratory collapse in the newborn period. As can
be seen in Figure 16 the pulmonary venous confluence (arrow)
that ends without a connection cannot decompress the pulmon-
ary vascular bed without emergent intervention. If the conflu-
ence is large enough to be anastomosed to the back of
the left atrium, survival is possible, but initial management usu-
ally requires venoarterial extra-corporeal membrane oxygena-
tion (ECMO) for stabilization.16
Walsh et al
Figure 12. Posterior view of the thoracic organs showing a cardiac
variant of the totally anomalous pulmonary venous connection. All the
pulmonary veins connect to the coronary sinus. ICV indicates inferior
caval vein; CS, coronary sinus.
Stenosis of the Common Pulmonary Vein (Cor
Triatriatum, IPCCC: 05.02.01)
In this anomaly, a membrane divides the left atrium into a pos-
terior chamber that receives the pulmonary veins (Figure 17)
and an anterior chamber that communicates with the mitral
valve. This subdividing membrane inserts proximal to (poster-
ior to) the left atrial appendage and is thereby distinguished
from a supramitral stenosing ring. The pulmonary venous
chamber may communicate with the left atrium through an
opening in the membrane, or it may communicate with the right
atrium either directly or indirectly via an anomalous venous
channel.7 The posterior chamber (also called the pulmonary
or proximal compartment) receives some or all of the pulmon-
ary veins and the anterior chamber (usually called the mitral or
distal compartment) communicates with the left atrial appen-
dage and atrioventricular valve, most commonly the anatomi-
cally mitral valve. The partition, although described as a
‘‘membrane,’’ is usually a fibromuscular structure. There is
variability in the number and size of the orifices within the
fibromuscular membrane, allowing communication between
both compartments. An interatrial communication may be
absent or else may be found between any of the compartments
(or both) and the right atrium.
The most common pattern is the existence of a defect at
the oval fossa communicating with the mitral compartment
(Figure 18A1). Cases have been described with an intact
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37
Figure 13. Posterior view of the thoracoabdominal organs in a case
of totally anomalous pulmonary venous connection of the infracardiac
type. The vertical vein (vv) is usually long and the pulmonary veins join
the venous channel individually and at different levels (arrows). The
stomach and oesophagus have been displaced to show the anomalous
venous channel connecting to the portal system.
partition membrane and the pulmonary venous compartment
draining directly to the right atrium or to a systemic vein via
an anomalous venous channel (Figure 18B1, 2). In the latter
case, the distinguishing feature that separates cor triatriatum
from TAPVC is that, in the former, the membrane only
needs to be incised or removed, whereas, in TAPVC, an
anastomosis is required to connect the pulmonary veins to
the left atrium.
There is some dispute on whether cor triatriatum sinister
represents a developmental anomaly of the pulmonary veins
or of the left atrium. According to the ‘‘malincorporation’’
theory, there is a failure in the normal incorporation of the
pulmonary veins into the left atrium. Another interpretation
is the so-called entrapment theory, which states that the
embryonic left horn of the sinus venosus entraps the common
pulmonary vein, preventing its normal incorporation to the
left atrium.
Synonyms for ‘‘cor triatriatum’’ include ‘‘cor triatriatum
sinister,’’ ‘‘divided left atrium,’’ and ‘‘triatrial heart.’’ What
some have called cor triatriatum dexter is not a disorder of
pulmonary venous development, but rather a rare congenital
malformation in which a membrane (possibly an enlarged
Eustachian valve) divides the right atrium into two cham-
bers and often streaming from the inferior caval vein
38
Figure 14. This posterior view of the pulmonary veins illustrates total
anomalous venous drainage below the diaphragm via a pulmonary vein
confluence (PVC) that drains to the portal vein. The right (RLPV) and
left (LLPV) lower pulmonary veins are much larger than the upper pul-
monary veins (RUPV, LUPV) as they enter the confluence. DAo indi-
cates descending aorta; T, trachea; RL, right lung; LL, left lung; ICV,
inferior caval vein. This image and description is from the Archiving
Working Group (AWG) Web portal (International Society for
Nomenclature of Paediatric and Congenital Heart Disease
[ISNPCHD]) and courtesy of Diane E. Spicer BS, PA(ASCP)(CHIF).
Adapted from http://ipccc-awg.net/TAPVC/TAPVC_Infracardiac_
04_08_20/TAPVC_Infracardiac_04_08_20_portal.html.
through a patent oval foramen into the left atrium, leading
to cyanosis.
Proposed classifications of cor triatriatum include those of
Loeffler, Niwagama, Grondin, and Lucas. Loeffler provided
the first classification of cor triatriatum. He divided the lesions
into cor triatriatum (1) without a communication between the
common pulmonary venous chamber and the left atrium
proper, (2) with such a communication, and (3) with partial cor
triatriatum with some veins draining into the stenotic common
pulmonary venous chamber and others draining normally.17
Niwayama likewise placed an emphasis on the opening in the
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World Journal for Pediatric and Congenital Heart Surgery 4(1)
Figure 15. In this mixed type of totally anomalous pulmonary venous
connection (TAPVC), the "left pulmonary veins return to the heart via
a vertical vein which drains into the left brachiocephalic vein. The right
pulmonary veins drain below the diaphragm through a vein that
extends to the portal vein. A left-sided inferior caval vein and right-
sided hepatic veins are identified as they extend toward the right-
sided, morphological right atrium (RmRA) in this heart with isomerism
of the right atrial appendages." This image and description is from the
Archiving Working Group (AWG) Web portal (International Society
for Nomenclature of Paediatric and Congenital Heart Disease
[ISNPCHD]) and courtesy of Diane E. Spicer BS, PA(ASCP)(CHIF).
Adapted from http://ipccc-awg.net/TAPVC/TAPVC_Mixed_04_08_30/
TAPVC_Mixed_04_08_30_SVC_Portal.html.
dividing septum and classified lesions as those with no opening
in the septum, those with a small opening in the septum, and
those with a wide opening in the septum.18 Grondin and associ-
ates viewed those anomalies in which there is no communica-
tion between the pulmonary venous chamber and either atrium
as cases of anomalous pulmonary venous connection, and thus
classified only those lesions in which there is an opening in the
dividing septum as cor triatriatum.19 Lucas has combined ele-
ments of each of these classification systems as described in
Table 3.7 A schematic representation of this anatomic classifi-
cation is shown in Figure 18 and reflected in the terms of the
IPCCC.
Walsh et al
Figure 16. Posterior view of an anatomical specimen showing the
pulmonary venous confluence behind the heart (arrow) but with no
connection to the left atrium or to the systemic veins.
Abnormal Absorption of the Common Pulmonary Vein
into the Left Atrium
There are circumstances when the pulmonary veins reach the
morphological left atrium but present abnormalities. Examples
are the atresia and the congenital stenosis of individual or
groups of pulmonary veins.
Pulmonary Vein Stenosis (IPCCC: 04.08.01)
Pulmonary vein stenosis may be discrete or involve a segment
of variable extension. Another possibility is the stenosis of the
venous ostium as it reaches the roof of the left atrium. The his-
tological analysis of the stenotic vein suggests that the mechan-
ism of lesion formation is a primary neoproliferative process
rather than an embryologic derangement.20 Postsurgical
reobstruction is also highly frequent (Figure 19), and the cellu-
lar proliferation is similar to the one found in the primary
lesion. The characteristic histologic presentation in the affected
vein is that of a nonspecific intimal thickening as a conse-
quence of spindle cell proliferation within a loose proteoglycan
matrix, fibrosis, and different degrees of medial involvement
(Figure 20). The proliferating cells have been identified as
myofibroblasts, since they express simultaneous features of
myocytes and fibroblasts, as detected under electron
microscopy and immunohistochemistry. No evidence of
inflammation is usually detected in the stenotic segments, but
recent or organized thrombosis has been described in some
cases. Intrapulmonary veins may show intimal occlusion by
fibrosis, medial hypertrophy, and adventitial enlargement. As
in other types of pulmonary venous obstruction, like in anom-
alous pulmonary venous connection, the lung parenchyma
exhibits diffuse congestion of capillaries, alveoli with edema,
and hemosiderin-laden macrophages, besides diffuse dilation
of subpleural and interlobular lymphatic vessels. Intra- and
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39
Figure 17. In this anatomical specimen with cor triatriatum or divided
left atrium, the four pulmonary veins connect to the proximal cham-
ber and communicate with the mitral or distal compartment via a
restrictive orifice (open arrow). LPA indicates left pulmonary artery;
RPA, right pulmonary artery; SCV, superior caval vein; Ao, aorta.
preacinar arterial occlusive lesions are also observed and may
vary from simple medial hypertrophy to intimal proliferation
and fibrosis.
Abnormal Connection With Normal Drainage
A few cases have been recognized showing a vein or veins
from one lung crossing the midline to join the contralateral
veins which, in turn, reach normally the left atrium. One such
case is published in the AWG Web portal (Figure 21).
Although this arrangement has not been formally acknowl-
edged in the nomenclature systems so far, it is being evaluated
for inclusion and described as ‘‘Anomalous pulmonary
venous connection with right pulmonary vein/veins
connecting to left pulmonary vein/veins and then to left
atrium.’’
Significant anatomical variation concerning the number of
venous orifices that reach the left atrium has been described
(see Table 1, IV).21 Some authors have found that in about
one-fourth of normal individuals, either the right or left pul-
monary veins connect to the left atrium via a common
orifice.22 While these findings were mainly directed at the
needs of electrophysiologists in the context of radiofrequency
ablation procedures involving the pulmonary veins, they do
describe anomalies that deviate from normal pulmonary
venous connections and are therefore mentioned in this
article.
Comment
Although uncommon, anomalies of pulmonary venous
return represent a wide spectrum of disorders of embryonic
cardiac development. It is hoped that this article will con-
tribute to understanding of the embryologic basis, the diag-
nostic categories, and the clinical and surgical implications
40 World Journal for Pediatric and Congenital Heart Surgery 4(1)

Figure 18. Classification of cor triatriatum according to Lucas. Schematic representation of Table 3.

of these anomalous pulmonary venous connections. In addi- Appendix A

tion, the authors wish to emphasize the use of a common
The IPCCC is the end result of the collaboration of many soci-
nomenclature, namely the IPCCC, and corresponding
eties and members, predominantly that of the European Asso-
images which are available via the AWG Web portal
ciation for Cardio-Thoracic Surgery (EACTS), the Society of
(http://ipccc-awg.net).

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Walsh et al 41

Table 3. Classification of Cor Triatriatum According to Lucas.

A. Accessory atrial chamber receives all pulmonary veins and

communicates with left atrium.
1. No other connections (classic cor triatriatum)
2. Other anomalous connections
a. To right atrium directly
b. With totally anomalous pulmonary venous connection
B. Accessory atrial chamber receives all pulmonary veins and does not
communicate with left atrium
1. Anomalous connection to right atrium directly
2. With totally anomalous pulmonary venous connection
C. Subtotal cor triatriatum
1. Accessory atrial chamber receives part of the pulmonary veins
and connects to the left atrium
a. Remaining pulmonary veins connect normally
b. Remaining pulmonary veins connect anomalously
2. Accessory atrial chamber receives part of the pulmonary veins
and connects to the right atrium
a. Remaining pulmonary veins connect normally
Figure 20. Photomicrography of a pulmonary vein showing con-
centric intimal proliferation of cells (myofibroblasts) immersed in a
loose connective tissue matrix, causing severe obstruction of the
venous lumen. Elastic-Van Gieson stain, objective magnification 5.

Figure 19. Posterior view of a heart specimen demonstrating a long

segment of stenosis in one of the left pulmonary veins (white arrow).
The patient had been previously submitted to surgical repair of totally
anomalous pulmonary venous connection.
Thoracic Surgeons (STS) and the Association for European
Paediatric Cardiology (AEPC). In 1998, in an effort to promote
standardization of nomenclature and database definitions, the
EACTS and STS created the International Congenital Heart
Surgery Nomenclature and Database Project. A common
nomenclature and data set were adopted by the EACTS and
STS and published in 2000.23 In the same year, the AEPC
published their system of nomenclature that they named the
European Paediatric Cardiac Code (EPCC).24 The members
of the EACTS/STS and AEPC quickly realized the wisdom
of working together to create a common system of nomencla-
ture and in October 2000, representatives from the AEPC,
EACTS, STS as well as other societies gathered in Frankfurt,
Germany and created the International Nomenclature Commit-
tee for Pediatric and Congenital Heart Disease.25 Ultimately
Figure 21. ‘‘The heart has been lifted cephalad. The inferior or dia-
phragmatic aspect of the right atrium shows the inferior caval vein and
just posterior to that are the right and left pulmonary veins as they join
the left atrium. The right pulmonary veins join the left atrium via a
short, stenotic vein. There are two right lower pulmonary veins, one
of which is small and the other large and dilated. The dilated right
lower pulmonary vein crosses the midline to drain into the left atrium
along with the left pulmonary veins. The entrance of the left pulmon-
ary veins into the left atrium is also markedly stenotic.’’ This image and
description is from the Archiving Working Group (AWG) Web portal
(International Society for Nomenclature of Paediatric and Congenital
Heart Disease [ISNPCHD]) and courtesy of Diane E. Spicer BS,
PA(ASCP)(CHIF). Source: http://ipccc-awg.net/Pulm_Vein_Stenosis/
Pulm_Vein_Stenosis_04_08_01/Pulm_Vein_Stenosis_04_08_01.html.
this committee evolved into its modern version and renamed
the International Society for Nomenclature of Pediatric and
Congenital Heart Disease and incorporated as a not-for-profit
corporation in Canada in 2005. The initial outcome of the com-
bined effort was to create a bidirectional cross-map of the Short

Downloaded from pch.sagepub.com by Marshall Jacobs on January 10, 2013

42
Lists of both systems, using the six digit numerical code
derived from the EPCC as the backbone for the cross-map
structure. The results were presented and endorsed at the First
International Summit on Nomenclature for Congenital Heart
Disease at a the Third World Congress of Pediatric Cardiology
and Cardiac Surgery in Toronto, Canada on May 2001. Four
years later, the IPCCC and expanding cross-map that by now
included the Long Lists, were presented at the Second Interna-
tional Summit on Nomenclature for Pediatric and Congenital
Heart Disease at the Fourth World Congress of Pediatric
Cardiology and Cardiac Surgery in Argentina, in September
2005.26 The most recent version of the IPCCC was presented
at the Third International Summit on Nomenclature for Pedia-
tric and Congenital Heart Disease at the Fifth World Congress
of Pediatric Cardiology and Cardiac Surgery in Australia in
June 2009. In its current version the IPCCC is mapped to the
codes developed by the International Congenital Heart Surgery
Nomenclature and Database Project of the EACTS/STS; the
EPCC of the AEPC; Canadian Congenital Heart Disease
Codes; Fyler Codes of Boston Children’s Hospital and Harvard
University; the International Classification of Diseases (ICD-9
and ICD-10) maintained by the World Health Organization and
the Current Procedural Terminology code (CPT) which is a
trademark registered and maintained by the American Medical
Association.
There are three working groups of the International Soci-
ety for Nomenclatures of Paediatric and Congenital Heart
Disease (ISNPCHD)27 The Nomenclature Working Group
(NWG), the Definitions Working Group (DFW) and the
Archiving Working Group (AWG). The NWG is the oldest
of the three working groups and charged with communica-
tions with individuals and organizations interested in the
IPCCC as well as the preservation and maintenance of the
IPCCC by the process of cross-mapping and creation of new
codes as needed. The DWG is responsible for the creation
of textual definitions of the terms of the IPCCC building
on the previously published definitions of the ISNPCHD.
The primary responsibility of the AWG is to identify with
representative images the different codes of the Interna-
tional Pediatric and Congenital Cardiac Codes (IPCCC) of
the ISNPCHD. In keeping with this mission, and using the
IPCCC as the organizational structure, the AWG has devel-
oped a Web site (http://ipccc-awg.net) where images of all
types illustrate the different forms of congenital and
acquired heart disease that affect children and increasingly
those successfully treated who survive into adulthood. On
a periodic basis, the images are reviewed and certified by
an international panel of experts. The AWG Web portal is
open to all and everyone is welcome to participate and con-
tribute representative images. Please visit us at the AWG
Web portal and help us in fulfilling the mission of the AWG
and ISNPCHD.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article.
Downloaded from pch.sagepub.com by Marshall Jacobs on January 10, 2013
World Journal for Pediatric and Congenital Heart Surgery 4(1)
Funding
The author(s) received no financial support for the research, authorship,
and/or publication of this article
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