PEDIATRIC CARDIOLOGY
Subdivided
Left Atrium: An Expanded Concept of
Cor Triatriatum
Sinistrum
OTTO G. THILENIUS, MD, FACC SAROJA BHARATI, MD MAURICE LEV, MD, FACC’ Chicago, Illinois
Twenty-four hearts with car triatriatum were studied. On the basis of this material and a review of the literature a new classification of “subdivided left atrium” is proposed. Type A, the most common form of subdivided left atrium, is the classic car triatrtatum with its multiple variations of partial anomalous pulmonary venous drainage; the fossa ovalis can be related to the proximal left atrial chamber (type A, a) or the distal left atrial chamber (type A, b). Type 6 hearts are related to (but not identical with) total anomalous pulmonary venous drainage into the coronary sinus; the coronary sinus opening is atretic in these hearts; abnormal defects connect the proximal left atrial chamber usually with the right atrium only, rarely also with the distal left atrial chamber. The Type C heart, first reported in this paper, has a superiorly and medially situated proximal chamber, located between the right and distal left atrium; it does not receive any pulmonary veins; the coronary sinus is normally formed. Current morphogenetic hypotheses that satisfactorily explain the Type A b and B heart fail to account for the Type A a and C heart.
Cor triatriatum, more specifically car triatriatum sinister, is a rare but distinct classic cardiac malformation that was apparently first recognized in 1868; in this heart1 a fibromuscular membrane divided the left atrium into two portions, one receiving the four pulmonary veins, the other having the atria1 appendage and the mitral valve. The membrane had a defect allowing blood to pass from the proximal to the distal chamber. Reviewing our cases and those previously reported, we have found hearts that differ in certain details from the classic car triatriatum, but that conform to the general morphologic pattern of this entity. It became necessary to expand the concept of car triatriatum into the more inclusive concept of subdivided left atrium. This paper presents the anatomic data in support of this expansion. Definition From the Department of Pediatrics, University of Chicago, Chicago, Illinois and the Congenital Heart Disease Research and Training Center, Hektoen Institute. Chicago, III. Manuscript accepted June 4, 1975. Career Investigator and Educator, Chicago Heart Association, Chicago, III. Address for reprints: Otto G. Thilenius, MD, Department of Pediatrics, University of Chicago, 5825 South Maryland Ave., Chicago, Ill. 60637. l
We include in the term “subdivided left atrium” all those hearts in which two left atria1 chambers can be demonstrated, a proximal and a distal chamber (see Nomenclature). The distal chamber possesses the atria1 appendage and the mitral valve. The location of the fossa ovalis in relation to these chambers is not part of this definition, nor is the presence or absence of a coronary sinus. Furthermore, the site of entrance of the pulmonary veins into the heart is not of primary importance for this definition, nor the number or size of the defects connetting the two left atria1 chambers with each other or the right atri-
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proximal chamber but others drain into the distal chamber or right atrium. In these exceptional hearts, just as in the classic hearts, the distal chamber is the one with the left atria1 appendage and the mitral valve.
urn. This expanded definition includes the many varieties of triatrial hearts under a common heading, obviating the coining of new terms for each variation from the classic concept. Mitral supravalvular stenosing rings of the left atrium are not included. Nomenclature
Case Material
and Classification
Our material includes 24 hearts examined at the Congenital Heart Disease Research and Training Center and 13 hearts previously described; the latter were selected because their anatomic features deviate from the classic concept of car triatriatum. Subdivided left atrium is classified into the types shown in Figure 1 and described herein: Type A: The proximal chamber is “funnel”shaped, basally situated and empties into the distal, more apically situated chamber. The coronary sinus is normal. In each subgroup listed the fossa ovalis can border either the proximal chamber (subtype a, Fig. 2) or the distal chamber (subtype b, Fig. 3). 1. All pulmonary veins drain into the proximal chamber (classic car triatriatum). 2. Subtotal pulmonary venous drainage: Some pul-
A variety of terms have been used to describe the two left atria1 chambers, including superior and inferior, proximal and distal, upper and lower, common pulmonary venous and left atria1 chamber, accessory and left atria1 chamber. The terms “proximal and distal” or “upper and lower” have been used with opposite meanings, and none of the terms are consistently logical. In this paper our terms are based on the direction of blood flow. There is a proximal chamber, from which the blood (usually) enters a distal chamber; the latter has, without exception, the left atria1 appendage and mitral valve. Our terms “proximal” and “distal” thus do not refer to proximity to the mitral valve but imply upstream and downstream location. The rigor of this definition is weakened only when some pulmonary veins drain into the
1. Diagrammatic presentation of classification of subdivided ieft atrium, inciuding previously reported cases and our own material.Furof this classification are given under Case Material and Classification. The atrial appendages are drawn schematicatfy and do not reflect their relation to the atrial septum. Hearts without reference are our own material. CS = coronary sinus; FO = fossa ovalis; proximal and distal = proximal and distal left atrial chamber; RA and LA = right and left atrium; RAA and LAA = right and left atrial appendage; SVC and WC = superior and inferior vena cava. Open diamond = normal coronary sinus; closed diamond = rudimentary coronary sinus; oval = fossa ovalis; open circles designate right and closed circles left pulmonary veins; open squares = communicating defects other than secundum atrial septal defects: arrow = direction of blood flow. FIGURE
ther details
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5. Car triatriatum with additional pulmonary venous connections. Type B: The proximal chamber is “wedge”shaped, located adjacent to the distal, inferior portion of the interatrial septum (midline chamber). The coronary sinus is rudimentary. The fossa ovalis borders the distal chamber.
monary veins drain into the proximal, some into the distal chamber. 3. Subdivided left atrium with partial anomalous pulmonary venous drainage into the right atrium. 4. Subdivided left atrium with partial anomalous pulmonary venous drainage into right superior vena cava or similar vascular structures.
FIGURE 2. Case 2. Anatomy of a type A la heart. The fossa ovalis opens into the proximal chamber. A, right-sided view; B, left-sided view. ASD = atrial septal defect (fossa ovalis type); C = coronary sinus: D = diaphragm: DC = distal chamber; L = limbus; LAP = left atrial appendage; LPV = left pulmonary vein: LV = left ventricle; MV = mitral valve; C = proximal chamber; RA = right atrium: RPV = right pulmonary vein; RV = right ventricle.
FIGURE 3. Case 15. Anatomy of a type A lb heart. The fossa ovalis opens into the distal chamber. A, right-sided view; B, left-sided view. FASO = fossa ovalis type atrial septat defect; PC = proximal chamber; SASD = sinus venosus type atrial septal defect. Other abbreviations as in Figure 2.
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2338 -7
18.
Type Cl 24
Type A5b 23
Type A5a 22
Type A3b 21
Type A2a 20
3868 -5
1124 -2
260 -1
3419 -11
2827 -8
3409 -1
1679 -10
17
Type Al 19
2665 -12
Autopsy
I (Continued)
16
TABLE
8 mo
19 wk
F
M
Double outlet right ventricle with mitral atresia and ventricular septal defect; adult coarctation; patent ductus arteriosus; fenestrated aortic valve
Transitional coarctation with aortic and mitral stenosis; the coronary sinus continuing as a partial left superior vena cava entering into the two left pulmonary veins which then enter the proximal atrial chamber; bicuspid aortic valve
Left pulmonary veins drain both into innominate vein via left superior vena cava and into left atrium
1 Yr
Large ventricular septal defect; pulmonary hypertension; bicuspid pulmonary valve; tricuspid insufficiency; left superior vena cava into the coronary sinus
Common atrioventricular orifice with fetal coarctation; common atrium; probe patent ductus arteriosus
Incomplete vascular ring caused by right aortic arch with left ductus arteriosus Ventricular septal defect; mitral insufficiency; straddling coronary sinus; possible herniation of the right aortic cusp Tetralogy of Fallot; patent ductus arteriosus; abnormal limbus; left superior vena cava into the coronary sinus; abnormal pulmonary artery from descending aorta to right lung; right lower pulmonary veins entering the inferior vena cava
Associated Abnormalities
Patent ductus arteriosus
M
Sex
3 mo
20 yr
2.5 mo
20 yr
7 vr
Age
atrium
Chamber
ovale closed
Fossa ovalis type of defect
Foramen
Foramen
ovale closed
Normal
Minute opening
Normal
-
Large
Normal
atrium
Fossa ovalis type of defect
Common
Normal
Large
Fossa ovalis type of defect
with a
0.3 cm defect between the two left atrial chambers; all pulmonary veins drain Into distal chamber
Band formation with a large opening between the two left atrial chambers
No communication between the two left atrial chambers. Proximal chamber is in typical location of type A subdivided left atrium but drains into right atrium via coronary sinus Fibromuscular septum with an opening of 0.2 to 0.3 cm between the two left atrial chambers
Proximal left atrium receives the right pulmonary veins which are obstructed; the distal left atrium receives the left pulmonary veins; they are somewhat obstructed
Membrane between the two left atrial chambers with small opening
Membrane-like septum with 0.5 cm large opening in muscular portion
Ridge-like formation large opening
Opening into both atriastraddling
ovale closed
Fossa ovalis type of defect
Foramen
with a large
Description of Subdividing Membrane Band formation opening
Nature of Coronary Sinus Normal
In Distal Chamber
of the Atrial Septal Defect
Fossa ovalis type of defect
Common
In Proximal
Description
SUBDIVIDED
LEFT
ATRIUM-THILENIUS
ET AL.
1. All pulmonary veins drain into the proximal chamber and from there only into the right atrium. 2. Subtotal pulmonary venous drainage: Some pulmonary veins drain into the proximal chamber from there into the right atrium; others straddle chambers or drain into the distal chamber.
basic anomaly, not different from type A 1. The size of the atria1 chambers is quite variable and largely dependent on the number of pulmonary veins draining into them. Type B: Described by Lam,12 this type is characterized by an atretic opening of the coronary sinus, an almost always intact subdividing membrane, and a fossa ovalis invariably related to the distal chamber. Eight such hearts have been reported.12m14 Type C: This is the rarest form of subdivided left atrium. The coronary sinus is normally formed and the fossa ovalis borders the proximal chamber. The location of the proximal chamber is unique: It is interposed superiorly between the right and the distal left atrium. Since this type of subdivided left atrium has not been reported, a more detailed description will be given:
and both
Type C: The proximal chamber is a midline chamber situated superiorly and is interposed between the right atrium and the distal chamber. The coronary sinus is normal. The foramen ovale borders the proximal chamber. All pulmonary veins enter the distal chamber (Fig. 4). Results The anatomic details of our cases are given in Table I and, schematically, in Figure 1. They are presented according to the classification given. It can be seen that the basic differentiating characteristics of the various types of subdivided left atrium pertain to (1) the location of the left atria1 chambers receiving the pulmonary veins, (2) the relation of the coronary sinus to these chambers, (3) the location of the fossa ovalis, (4) the absence or presence of associated partial anomalous pulmonary venous drainage, and (5) the site of such drainage. Type A: This is by far the most commonly observed category (23 of our 24 hearts). Within this category, group 1, the classic car triatriatum, is the largest subdivision (19 hearts). The membrane separating the two left atria1 chambers is fibromuscular and funnel shaped, with openings of various sizes. The proximal chamber is thick-walled, whereas the walls of the distal chamber are thin. The right atrium and right ventricle are hypertrophied and enlarged; the left ventricle is, on an absolute scale, smaller than normal. The various forms of subtotal car triatriatum and partial anomalous pulmonary venous drainage, type A, groups 2 to 5,2-11 are rare variations and are, as a
Case 24: This heart is from a 7 month old black girl who was mildly cyanotic and slightly tachypneic since early infancy. She failed to thrive (weight 4.3 kg at 7 months), but there were no other striking symptoms. When seen first at age 7 months her cardiac examination revealed: a heart rate of 120 beats/min, respiratory rate of 30/min, and blood pressure of 90/50 mm Hg. There was mild cyanosis but she had no signs of congestive failure. She had a mild right ventricular impulse. The first heart sound was normal; the second sound was narrowly split with an accentuated pulmonary closure. A third heart sound was present at the apex. A grade 3/6 pansystolic murmur was heard along the lower left sternal border. There was no diastolic murmur. The electrocardiogram revealed a mean frontal axis of 130’ and biatrial and right ventricular hypertrophy. The chest X-ray film demonstrated mild right ventricular enlargement and mildly increased pulmonary vascular markings. Cardiac catheterization data are given in Table II. Characteristic angiocardiographic frames are shown in Figures 4 and 5. Surgical procedure: Under deep hypothermia the right atrium was opened during complete circulatory arrest. A small defect in the fossa ovalis led into the proximal chamber. A normally formed limbus was present. A larger opening, leading from the proximal into the distal left atria1
FIGURE 4. Case 24. Frontal (left) and lateral (right) views of angiocardiogram after injection into the proximal left atrial chamber (bold arrow) of heart 24. In the frontal view the obligatory left to right shunt through a secundum type atrial septal defect (fine arrow) from the proximal chamber to the right atrium (RA) is seen as a cloud of contrast escaping into the right atrium. In the lateral view, a narrow stream of contrast medium from the proximal chamber into the posterior distal chamber (d LA) is seen (fine arrow). RV = right ventricle.
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(Table I). Of the remaining hearts 5 had associated lesions of milder character (patent ductus arteriosus in 3 cases, bicuspid aortic valve and straddling inferior vena cava); 14 hearts had complex lesions, involving predominantly the systemic venous return, the atria1 or ventricular septum or the large arteries.
TABLE II Cardiac
Catheterization
Data for Heart 24
0,
Saturation (%I Superior vena cava Right atrium Right ventricle Pulmonary artery Pulmonary capil!ary Proximal left atrial chamber Ascending aorta Pulmonary blood flow (liters/min par m*) Systemic blood flow (literslmin per ml) a = a wave; ED = enddiastolic;
Pressure (mm Ho)
42 67 77 79 99 96
a16.v8,m7 llO/ll ED 11 O/60. m 75 a 38, v 32, m 32 a 42, v 34, m 34
78
75155,
ET AL.
Discussion Classification
m 60
5.0 3.1
m = mean; v = v wave.
chamber, was probed. The entire proximal chamber was excised. After the infant was rewarmed, the main pulmonary artery was banded so that the peripheral pulmonary systolic pressure was reduced from 80 to 50 mm Hg. The infant died 36 hours after completion of the operation.
Pathologic findings: The heart was enlarged. Adjacent to the limbus fossa ovalis, which was well formed, was a large surgically created opening that included almost the entire atria1 septum. The roof of what was apparently a small proximal chamber was seen superiorly between the cut surfaces of septa separating the proximal chamber from the right atrium on the one side, the distal left atrium on the other. There was mitral atresia. Both the aorta and pulmonary artery arose from the right ventricle in a normal anteroposterior relation; a small ventricular septal defect led into a slit-like posterior left ventricle. The right and distal left atria as well as the right ventricle were hypertrophied and enlarged. A discrete coarctation of the aorta was present in typical location.
Associated cardiac lesions of subdivided left atrium: In only 5 of our 24 hearts was the subdivided left atrium the sole congenital cardiac anomaly
of car triatriatum have A variety of classifications been proposed15-1g stressing anatomic or hemodynamic characteristics, or both. Whereas James’s classification16 is a very broad one (including total anomalous pulmonary venous drainage into the coronary sinus, car triatriatum dexter and atria1 aneurysms), Van Praagh and Corsiniig restrict the name “car triatriatum” to only one particular heart (type A lb). From a pathologic viewpoint it seems more logical to include under the heading “subdivided left atrium” all hearts that have two distinct left atria1 chambers, regardless of the presumed morphogenetic origin.
Criteria for classification: Our classification of subdivided left atrium is an extension of the description by Lam et al. l2 of type A and B hearts. The extension was necessary to account for the anatomic variations of this complex in a systematic manner. Two criteria were used: 1. Anatomy: Separation of types A, B and C was based on the distinctly different location of the proximal chamber. For further grouping we chose, because of immediate surgical implications, the site of the partial anomalous pulmonary venous drainage. It is recognized that combined forms exist, for example, A3 and A4 (Fig. 1, heart of Wilson et al-?). 2. Embryology: The second criterion was the (presumed) morphogenetic origin of each heart. As will be shown, the proximal chamber in types A, B and C
FIGURE 5. Case 24. Frontal (left) and lateral (right) views of an angiocardiogram after right ventricular injection of contrast medium in heart 24. Both aorta (AO) and pulmonary artery (PA) arise from the right ventricle (RV). A slit-like posterior ventricle left was present (but not seen in this frame) with a small membraneous ventricular septal defect. The subaortic stenosis is not clearly visible.
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differs in embryologic origin. Furthermore, the relation of the fossa ovalis to either the proximal or distal chamber implies-according to our current understanding-a different morphogenetic pathway. To accent this nonuniform embryologic background of different forms of subdivided left atrium, groups 1 to 5 of type A were classified according to this relation of the fossa ovalis into subtypes a and b. Our classification is based on anatomy and does not depend on the physiologic disturbance created in an individual heart; it is meant to inform about the anatomic variations of this complex so that suitable surgical decisions can be reached.
nary sinus a common pulmonary venous trunk joins the coronary sinus by way of the remnant of the vertical vein, whereas in our type B the right or left pulmonary veins, or both, enter the proximal chamber separately. Incidence: Of all hearts with subdivided left atrium, type A lb is by far the most common. Exactly how many such hearts have been reported is difficult to estimate. Like Church,’ who failed to note the location of the fossa ovalis in his original description of this lesion, many subsequent investigators have not considered the location of the fossa ovalis with respect to the proximal or distal chambers a crucial criterion for car triatriatum. In our own material type A lb accounts for 50 percent of hearts. Since Van Praagh and Corsini’s review of slightly less than 100 hearts of this type in 1969, approximately 35 additional cases of type A have been reported, usually in surgical journals and with limited anatomic detail.2046 The various forms of subtotal car triatriatum (A 2) and car triatriatum with partial anomalous pulmonary venous drainage (A 3 to 5) are quite rare and almost always appear in single case reports. They represent the intriguing variations of the basic lesion. Similarly, type B and C hearts are extremely rare and, with the exception of type B 1,12have beenindividually reported.
Differentiation of types: Type A hearts are closely related to classic car triatriatum, whereas type B hearts resemble some aspects of total anomalous pulmonary venous drainage into the coronary sinus. The type C heart has some features in common with types A and B but has specific, separate characteristics. For the differentiation of these groups the location of the proximal chamber and the status of the coronary sinus are important. In general, in type A the proximal chamber is positioned at the basal aspect of the left atrium and drains primarily into the distal left atria1 chamber; the coronary sinus and its valve are normally formed. In type B the proximal chamber is located more medially and inferiorly at the posterior aspect of the left atrium. The coronary sinus ostium is demarcated by the coronary sinus valve, and the sinus consists of a rudimentary short channel. Most of the coronary venous blood appears to drain into the proximal chamber directly. In type C the coronary sinus is normally formed; the “proximal” chamber is a midline structure lying superiorly and interposed between right and distal left atrium. It opens into the right atrium through an atria1 septal defect (fossa ovalis type) and to the distal left atria1 chamber through an abnormal defect. The latter chamber receives all four pulmonary veins.
Hemodynamics
Type B versus total anomalous pulmonary venous drainage: These anatomic features described for type B hearts raise the question whether the proximal chamber in type B is a markedly dilated coronary sinus with an abnormal opening into the right atrium, associated with atresia of the distal portion of the coronary sinus immediately upstream to the coronary sinus valve. Type B subdivided left atrium and total anomalous pulmonary venous drainage into the coronary sinus are likely to be closely related; the presence or absence of a smaller or larger defect in the subdividing membrane is not of decisive significance. However, there are differences between the two lesions: (1) In total anomalous pulmonary venous drainage into the coronary sinus the mouth of the coronary sinus is a single large opening, related to the coronary sinus valve; in our type B it is small and usually blind; the proximal chamber drains through an abnormal defect into the right atrium. (2) In total anomalous pulmonary venous drainage into the coro-
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Diagnosis
Hemodynamics: The hemodynamic disturbance of these hearts is variable, and depends on (1) the size of the communication between the proximal and distal chamber, (2) the extent of left to right shunting through a defect between the proximal chamber and the right atrium directly or through an anomalous pulmonary venous connection, and (3) the character of associated cardiac lesions. The classification of Gasul et a1.17 (triatrial hearts with absent, small and large atria1 communications) accents these hemodynamic abnormalities. The patient with a subdivided left atrium of type A 1 and a large communicating defect between proximal and distal chambers will be virtually asymptomatic (a 70 year old patient of Loeffler47), whereas a small communication would result in early death (a 25 day old infant of Hosch48). The degree of right ventricular hypertrophy and pulmonary hypertension, typically found in patients with a subdivided left atrium, will parallel the degree of obstruction to outflow from the proximal chamber, and will determine the clinical findings if it is not complicated by associated defects. When there is significant obstruction to flow between the proximal and distal chambers or right atrium, severe dyspnea and related signs of pulmonary venous obstruction are dominant. If there are communications between the right atrium and the distal chamber, right to left shunts may occur and the child can be expected to be cyanotic. Angiographic diagnosis: A correct diagnosis can be made in most cases by cardiac catheterization. In
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type A 1 hearts the subdividing membrane can be demonstrated well only by cineangiography; pressure data and the blood oxygen saturation levels will indicate the approximate extent of communicating defects between the left atria1 chambers and, possibly, the right atrium. Angiograms of the rarer types A 2 to 5 are more difficult to analyze; familiarity with the possible varieties of subdivided left atrium will permit selective and diagnostic injections of contrast medium. Cardiac catheterization data in type B hearts will have a striking resemblance to data in total anomalous pulmonary venous drainage into the coronary sinus. From a therapeutic point of view it is not significant to separate these two entities since the surgical methods of correction are virtually identical. Type C hearts are clearly diagnosed when injection of contrast medium into the midline chamber can be performed: The location of the chamber and the absence of retrograde filling of pulmonary veins clearly confirm the anatomy of the type C heart (Fig. 4). Surgical correction: For all hearts with subdivided left atrium surgical excision of the subdividing membrane is the treatment of choice. It will abolish obstruction, which almost always exists at this level. Closure of defects between the left and right atrium, and, for hearts of types A 3 to 5, correction of the anomalously draining pulmonary veins will establish normal hemodynamic relations. These repairs are life-saving, but they require correct preoperative diagnosis. When associated cardiac defects . are present, surgical corrections have to be tailored according to the entire complex. Associated
Cardiac
Lesions
Although some reports imply that car triatriatum is seldom associated with other cardiac defects, our material bears evidence to the opposite: In 19 of our 24 hearts there were significant additional anomalies, including, in 8 hearts, milder lesions such as patent ductus arteriosus, and in 11 hearts, severe and complex lesions such as mitral atresia (Table I). There was no particular pattern of associated lesions. Atrioventricular valve anomalies were noted as often (five hearts) as coarctation of the aorta (four hearts) and patent ductus arteriosus (four hearts). Tetralogy complex (three hearts) was seen as often as isolated ventricular septal defect (three hearts). This wide variety of associated malformations indicates a profound and diffuse disturbance in the development of the fetal heart rather than a specific lesion that might be explained by a single developmental defect. Morphogenesis
of the Subdivided
Left Atrium
It is tempting to search for a uniform embryologic explanation for the development of the subdividing membrane. The malseptation, the malincorporation and entrapment hypotheses are examples of such attempts; they have been discussed in detail by Van Praagh and Corsinilg and others.14J5**s-s2 The shortcoming of these hypotheses is that individual hearts
ET AL.
are taken to prove a cause, excluding other hearts that do not fit into the concept. For instance, both the malincorporation and entrapment hypotheses require that the fossa ovalis open into, or be directlyadjacent to, the distal chamber; although this frequently occurs (Fig. 3), there are hearts (Ref. 9, 51, Case 4 in Ref. 52 and our cases 1 to 6, 20 and 22) in which the foramen ovale opens unequivocally into the proximal chamber (Fig. 2). The entrapment hypothesislg is very convincing for type A lb hearts. For types A 2 to 5 there are additional anomalous pulmonary venous connections that are not uncommonly observed as separate malformations: drainage of one or more pulmonary veins into the right atrium or right superior vena cava. Such pulmonary venous anomalies can be explained by failure of some pulmonary veins to find their connection to the common pulmonary vein directly, joining instead other vascular structures. Considerable difficulties arise when one attempts to use current hypotheses to account for type A la or type C hearts in which the fossa ovalis (foramen ovale or secundum atria1 septal defect) separates the right atrium from the proximal chamber. Van Praagh and Corsini’s studiesi of the normal development of the left atria1 region and common pulmonary vein in human embryos are instructive in this context. At the 10 mm stage (horizon 16) the sinus venosus tissue, the common pulmonary vein and the left horn of the sinus venosus are directly adjacent structures. The sinus venosus tissue, derived from the right horn of the sinus venosus, differentiates into the septum primum and the left venous valve; a cleftlike intersepto-valvular space is formed between them. The common pulmonary vein passes immediately beneath this tissue. One might speculate that abnormal growth in this area results in an abnormal communication of the common pulmonary vein with the sinus venous tissue and that possibly the intersepto-valvular space might be the predecessor of the proximal chamber of type A la and type C hearts. The fossa ovalis would then indeed be related to the proximal and not the distal chamber. This would represent a type of malseptation and the hypothesis is consistent with Van Praagh and Corsini’s conclusion “that the basic abnormality involves the endothelium of the right horn of the sinus venosus, not the endothelium of the common pulmonary vein.“ig The direct spatial proximity of the left horn of the sinus venosus (the future coronary sinus) and the common pulmonary vein at the 10 mm stage lends itself to the formation of an abnormal direct communication between these two structures, resulting in the B malformation of subdivided left atrium. Although these speculations cannot be proved, they represent possible morphogenetic pathways to explain the anatomic fact of a type A la or type C heart just as the entrapment hypothesis explains the type A lb heart.
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References 1. Church WS: Congenital malformation of the heart; abnormal
2. 3.
4.
5.
6. 7.
septum in left auricle. Trans Pathol Sot Lond 19:188-190, 1867168 Donatelli R, Meriggi A, Santoli C, et al: II “car triatriatum.” Minerva Cardioangiol 17:65 l-664, 1969 Michaud P, Dalloz C, Age C, et al: A propos d’un nouveau cas de coeur triatrial de I’adulte, opere avec succes. Arch Mal Coeur 63:291-300, 1970 Wilson JW, Graham TP, Gehweiler JA, et al: Cor triatriatum with intact subdividing diaphragm and partial anomalous pulmonary venous connection to the proximal left atrial chamber (an unreported type). Pediatrics 47:745-750, 1971 Stoeber H: Ein weiterer Fall von car triatriatum mit eigenartig gekreuzter Mundung der Lungenvenen. Virchows Arch [Pathol Anat] 193:252-257, 1908 Somerville J: Masked car triatriatum. Br Heart J 28:55-61, 1966 Shone JD, Anderson RC, Amplatz K, et al: Pulmonary venous obstruction from two separate coexistent anomalies. Am J Car-
diol 11:525-531, 1963 8. Grondin C, Leonard AS, Anderson RC, et al: Cor triatriatum: a
diagnostic surgical enigma. J Thorac Cardiovasc Surg 48: 527-539, 1964 9. Maxwell GM, Young WP, Rowe G,G, et al: Cor triatriatum. J Pediatr 50:71-75, 1957 Vinh LT, Due TV, Caldera R, et al: Le coeur triatrial bi-auriculaire gauche. Ann Pediatr (Paris) 43:2418-2423, 1967 11. Arrants JE, Riopel DA, Catalona PW: Cor triatriatum: preoperative diagnosis and successful surgical correction in a tenweek-old infant. Chest 63:1027-1028, 1973 12. Lam CR, Green E, Drake E: Diagnosis and surgical correction of two types of triatrial heart. Surgery 51:127-137, 1962 AL, Lucas RV, Castaneda AR: Surgical correction 13. Wedemeyer in infancy of an unusual form of triatrial heart. J Thorac Cardio10.
vast Surg 59:685-690, 1970 14. Patten BM, Taggart WB: An unusual type of triatrial heart. Arch Pathol 8:894-905,
26. 27.
terization and left atrial angiocardiography in the diagnosis of car triatriatum. Stand J Thorac Cardiovasc Surg 4:149-152, 1970
Tesler UF, Hallman GL, McNamara DG, et al: II trattamento chirurgico del car triatriatum. Minerva Cardioangiol 19:397408, 1971 29. Danielson G, Feldt R: Successful repiar of co-existing car tri-
28.
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34.
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41.
p 869-881
42.
18. Lucas RV, Schmidt RE: Anomalous venous connections, pulmonary and systemic, chap 32. In, Heart Disease in Infants,
43.
delphia,
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(Moss AJ, Adams p 702-707
F, ed). Baltimore, 44.
19. Van Praagh R, Corsini I: Cor triatriatum: pathologic anatomy and a consideration of morphogenesis based on 13 postmortem cases and a study of normal development of the pulmonary vein
45.
and atrial septum in 83 human embryos. Am Heart J 78:379405, 1969 20. Beller B, Childers R, Eckner F, et al: Cor triatriatum in the adult. Am J Cardiol 19:749-754, 1967 21. Ahn C, Hosier D, Sirak H: Cor triatriatum. J Thorac Cardiovasc
46.
Surg 56:177-183, 1968 22. Barrillou A, Blondeau P, Cachin JC, et al: Le coeur triatrial de I’adulte. Arch Mal Coeur 61:1306-1320,
1968
23. Wolfe RR, Ruttenberg HD, Desilets DT, et al: Cor triatriatum. J Thorac Cardiovasc Surg 56:114-l 19, 1968 24. Jlmenez Martinez J, Vasquez JSF, Gutierrez Bosque R, et al: Cor triatriatum with pericardial agenesis. Thorax 24:667-672, 1969 25. Al Abdulla HM, Demany MA, Zimmerman HA: Cor triatriatum: preoperative 1970
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in an adult. Am J Cardiol
of Fallot. J Thorac
Cardiovasc
Surg 63:
Maftre MJ, Otero E, Querro Jimenez M, et al: Cor triatriatum. 1972
Park MK, Ricketta HJ, Guntheroth WG: Cor triatriatum, an operable form of pulmonary hypertension. Am J Dis Child 123: 500-503, 1972 Persson B, Johansson BD, Lundstrom NR, et al: Cor triatriatum. Acta Paediatr Stand 61:477-482, 1972 Bex JP, Bercot M, Motte G, et al: A propos d’un nouveau cas de coeur triatrial opere chez I’adulte. Ann Chir Thorac Cardiovast 12:147-148, 1973 From AHL, Mazzitello WF, Judd AS, et al: Ebstein’s malformation of the tricuspid valve associated with valvar stenosis and car triatriatum. Chest 64:248-25 1, 1973 Drut R, di Bitetti ME, Tau L: Cor triatriatum. ArQ Bras Cardiol 26:253-258, 1973 lnoue H: Cor triatriatum with ostium primum defect. Jap J Thorat Surg 25:593-596, 1973 (in Japanese) Kimura M: A case report of car triatriatum. Jap J Thorac Surg 25:370-374, 1973 (in Japanese) Nakano S: Surgical treatment of car triatriatum. Jap J Thorac Surg 25:541-547, 1973 (in Japanese) Noak R, Friebel L: Das car triatriatum. Kinderaerztl Prax 41: 407-412, 1973 Oelert H, Breckenridge IM, Rosland G, et al: Surgical treatment of car triatriatum in a 4% month-old infant. Thorax 28: 242-246, 1973 Singh R, Crampton RS, Wellons HA, et al: Adult car triatriatum: preoperative identification and successful correction. Chest 64:373-376, 1973 Carpena C, Colokathis B, Subramanian S: Cor triatriatum. Ann
Thorac Surg 17:325-331, 1974 Gibson DG, Honey M, Lennox SC: Cor triatriatum. Br Heart J 36:835-838, 1974 Neuhaus KL, Niessen HW, Loogen F: Cor triatriatum sinistrum. Z Kardiologie 63:573-580, 1974 Nimura Y, Matsumoto M, Beppu S, et al: Noninvasive preoperative diagnosis of car triatriatum with ultrasonocardiotomogram and conventional echocardiogram. Am Heart J 88:240-250, 1974 Wyler F, Rutishauser M, Grade1 E: Cor triatriatum in a 3 month old infant. Acta Paediatr Stand 63:619-622, 1974
Loeffler E: Unusual malformation of the left atrium: pulmonary sinus. Arch Pathol 48:371-376, 1949 48. Hosch HP: Zur Lehre der Missbildungen des linken Vorhofs. Frankfurt Z Pathol 1:563-580, 1907 49. Borst M: Ein car triatriatum. Verhandl. deutsch. pathol. Gesell. 9:178-191, 1905 50. Hagenauer J: Die Pathogenese einer seltenen Herzmissbildung 47.
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and tetralogy 1972
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1929
15. Niwayama G: Cor triatriatum. Am Heart J 59:291-317, 1960 16. James TN: Classification of triatrial hearts. Anat Ret 143:7991, 1962 17. Gasul BM, Arcilla RA, Lev M: Heart Disease in Children. Phila-
Brickman RD, Wilson L, Zuberbuhler JR, et al: Cor triatriatum. J Thorac Cardiovasc Surg 60523-530, 1970 Lyngborg K, Andersen M, Efsen F: Transseptal left heart cathe-
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(car triatriatum). Frankfurt Z Pathol 41:332-356, 1931 Palmer GA: Cardiac anomaly (so-called double left auricle). Am Heart J 6:230-236, 1930/31 Edwards JE, DuShane JW, Alcott DL, et al: Thoracic venous anomalies. Arch Pathol 5 1:446-460, 195 1
Subdivided
Left Atrium: An Expanded Concept of
Cor Triatriatum
Sinistrum
OTTO G. THILENIUS, MD, FACC SAROJA BHARATI, MD MAURICE LEV, MD, FACC’ Chicago, Illinois
Twenty-four hearts with car triatriatum were studied. On the basis of this material and a review of the literature a new classification of “subdivided left atrium” is proposed. Type A, the most common form of subdivided left atrium, is the classic car triatrtatum with its multiple variations of partial anomalous pulmonary venous drainage; the fossa ovalis can be related to the proximal left atrial chamber (type A, a) or the distal left atrial chamber (type A, b). Type 6 hearts are related to (but not identical with) total anomalous pulmonary venous drainage into the coronary sinus; the coronary sinus opening is atretic in these hearts; abnormal defects connect the proximal left atrial chamber usually with the right atrium only, rarely also with the distal left atrial chamber. The Type C heart, first reported in this paper, has a superiorly and medially situated proximal chamber, located between the right and distal left atrium; it does not receive any pulmonary veins; the coronary sinus is normally formed. Current morphogenetic hypotheses that satisfactorily explain the Type A b and B heart fail to account for the Type A a and C heart.
Cor triatriatum, more specifically car triatriatum sinister, is a rare but distinct classic cardiac malformation that was apparently first recognized in 1868; in this heart1 a fibromuscular membrane divided the left atrium into two portions, one receiving the four pulmonary veins, the other having the atria1 appendage and the mitral valve. The membrane had a defect allowing blood to pass from the proximal to the distal chamber. Reviewing our cases and those previously reported, we have found hearts that differ in certain details from the classic car triatriatum, but that conform to the general morphologic pattern of this entity. It became necessary to expand the concept of car triatriatum into the more inclusive concept of subdivided left atrium. This paper presents the anatomic data in support of this expansion. Definition From the Department of Pediatrics, University of Chicago, Chicago, Illinois and the Congenital Heart Disease Research and Training Center, Hektoen Institute. Chicago, III. Manuscript accepted June 4, 1975. Career Investigator and Educator, Chicago Heart Association, Chicago, III. Address for reprints: Otto G. Thilenius, MD, Department of Pediatrics, University of Chicago, 5825 South Maryland Ave., Chicago, Ill. 60637. l
We include in the term “subdivided left atrium” all those hearts in which two left atria1 chambers can be demonstrated, a proximal and a distal chamber (see Nomenclature). The distal chamber possesses the atria1 appendage and the mitral valve. The location of the fossa ovalis in relation to these chambers is not part of this definition, nor is the presence or absence of a coronary sinus. Furthermore, the site of entrance of the pulmonary veins into the heart is not of primary importance for this definition, nor the number or size of the defects connetting the two left atria1 chambers with each other or the right atri-
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proximal chamber but others drain into the distal chamber or right atrium. In these exceptional hearts, just as in the classic hearts, the distal chamber is the one with the left atria1 appendage and the mitral valve.
urn. This expanded definition includes the many varieties of triatrial hearts under a common heading, obviating the coining of new terms for each variation from the classic concept. Mitral supravalvular stenosing rings of the left atrium are not included. Nomenclature
Case Material
and Classification
Our material includes 24 hearts examined at the Congenital Heart Disease Research and Training Center and 13 hearts previously described; the latter were selected because their anatomic features deviate from the classic concept of car triatriatum. Subdivided left atrium is classified into the types shown in Figure 1 and described herein: Type A: The proximal chamber is “funnel”shaped, basally situated and empties into the distal, more apically situated chamber. The coronary sinus is normal. In each subgroup listed the fossa ovalis can border either the proximal chamber (subtype a, Fig. 2) or the distal chamber (subtype b, Fig. 3). 1. All pulmonary veins drain into the proximal chamber (classic car triatriatum). 2. Subtotal pulmonary venous drainage: Some pul-
A variety of terms have been used to describe the two left atria1 chambers, including superior and inferior, proximal and distal, upper and lower, common pulmonary venous and left atria1 chamber, accessory and left atria1 chamber. The terms “proximal and distal” or “upper and lower” have been used with opposite meanings, and none of the terms are consistently logical. In this paper our terms are based on the direction of blood flow. There is a proximal chamber, from which the blood (usually) enters a distal chamber; the latter has, without exception, the left atria1 appendage and mitral valve. Our terms “proximal” and “distal” thus do not refer to proximity to the mitral valve but imply upstream and downstream location. The rigor of this definition is weakened only when some pulmonary veins drain into the
1. Diagrammatic presentation of classification of subdivided ieft atrium, inciuding previously reported cases and our own material.Furof this classification are given under Case Material and Classification. The atrial appendages are drawn schematicatfy and do not reflect their relation to the atrial septum. Hearts without reference are our own material. CS = coronary sinus; FO = fossa ovalis; proximal and distal = proximal and distal left atrial chamber; RA and LA = right and left atrium; RAA and LAA = right and left atrial appendage; SVC and WC = superior and inferior vena cava. Open diamond = normal coronary sinus; closed diamond = rudimentary coronary sinus; oval = fossa ovalis; open circles designate right and closed circles left pulmonary veins; open squares = communicating defects other than secundum atrial septal defects: arrow = direction of blood flow. FIGURE
ther details
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5. Car triatriatum with additional pulmonary venous connections. Type B: The proximal chamber is “wedge”shaped, located adjacent to the distal, inferior portion of the interatrial septum (midline chamber). The coronary sinus is rudimentary. The fossa ovalis borders the distal chamber.
monary veins drain into the proximal, some into the distal chamber. 3. Subdivided left atrium with partial anomalous pulmonary venous drainage into the right atrium. 4. Subdivided left atrium with partial anomalous pulmonary venous drainage into right superior vena cava or similar vascular structures.
FIGURE 2. Case 2. Anatomy of a type A la heart. The fossa ovalis opens into the proximal chamber. A, right-sided view; B, left-sided view. ASD = atrial septal defect (fossa ovalis type); C = coronary sinus: D = diaphragm: DC = distal chamber; L = limbus; LAP = left atrial appendage; LPV = left pulmonary vein: LV = left ventricle; MV = mitral valve; C = proximal chamber; RA = right atrium: RPV = right pulmonary vein; RV = right ventricle.
FIGURE 3. Case 15. Anatomy of a type A lb heart. The fossa ovalis opens into the distal chamber. A, right-sided view; B, left-sided view. FASO = fossa ovalis type atrial septat defect; PC = proximal chamber; SASD = sinus venosus type atrial septal defect. Other abbreviations as in Figure 2.
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._ 5
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5
2338 -7
18.
Type Cl 24
Type A5b 23
Type A5a 22
Type A3b 21
Type A2a 20
3868 -5
1124 -2
260 -1
3419 -11
2827 -8
3409 -1
1679 -10
17
Type Al 19
2665 -12
Autopsy
I (Continued)
16
TABLE
8 mo
19 wk
F
M
Double outlet right ventricle with mitral atresia and ventricular septal defect; adult coarctation; patent ductus arteriosus; fenestrated aortic valve
Transitional coarctation with aortic and mitral stenosis; the coronary sinus continuing as a partial left superior vena cava entering into the two left pulmonary veins which then enter the proximal atrial chamber; bicuspid aortic valve
Left pulmonary veins drain both into innominate vein via left superior vena cava and into left atrium
1 Yr
Large ventricular septal defect; pulmonary hypertension; bicuspid pulmonary valve; tricuspid insufficiency; left superior vena cava into the coronary sinus
Common atrioventricular orifice with fetal coarctation; common atrium; probe patent ductus arteriosus
Incomplete vascular ring caused by right aortic arch with left ductus arteriosus Ventricular septal defect; mitral insufficiency; straddling coronary sinus; possible herniation of the right aortic cusp Tetralogy of Fallot; patent ductus arteriosus; abnormal limbus; left superior vena cava into the coronary sinus; abnormal pulmonary artery from descending aorta to right lung; right lower pulmonary veins entering the inferior vena cava
Associated Abnormalities
Patent ductus arteriosus
M
Sex
3 mo
20 yr
2.5 mo
20 yr
7 vr
Age
atrium
Chamber
ovale closed
Fossa ovalis type of defect
Foramen
Foramen
ovale closed
Normal
Minute opening
Normal
-
Large
Normal
atrium
Fossa ovalis type of defect
Common
Normal
Large
Fossa ovalis type of defect
with a
0.3 cm defect between the two left atrial chambers; all pulmonary veins drain Into distal chamber
Band formation with a large opening between the two left atrial chambers
No communication between the two left atrial chambers. Proximal chamber is in typical location of type A subdivided left atrium but drains into right atrium via coronary sinus Fibromuscular septum with an opening of 0.2 to 0.3 cm between the two left atrial chambers
Proximal left atrium receives the right pulmonary veins which are obstructed; the distal left atrium receives the left pulmonary veins; they are somewhat obstructed
Membrane between the two left atrial chambers with small opening
Membrane-like septum with 0.5 cm large opening in muscular portion
Ridge-like formation large opening
Opening into both atriastraddling
ovale closed
Fossa ovalis type of defect
Foramen
with a large
Description of Subdividing Membrane Band formation opening
Nature of Coronary Sinus Normal
In Distal Chamber
of the Atrial Septal Defect
Fossa ovalis type of defect
Common
In Proximal
Description
SUBDIVIDED
LEFT
ATRIUM-THILENIUS
ET AL.
1. All pulmonary veins drain into the proximal chamber and from there only into the right atrium. 2. Subtotal pulmonary venous drainage: Some pulmonary veins drain into the proximal chamber from there into the right atrium; others straddle chambers or drain into the distal chamber.
basic anomaly, not different from type A 1. The size of the atria1 chambers is quite variable and largely dependent on the number of pulmonary veins draining into them. Type B: Described by Lam,12 this type is characterized by an atretic opening of the coronary sinus, an almost always intact subdividing membrane, and a fossa ovalis invariably related to the distal chamber. Eight such hearts have been reported.12m14 Type C: This is the rarest form of subdivided left atrium. The coronary sinus is normally formed and the fossa ovalis borders the proximal chamber. The location of the proximal chamber is unique: It is interposed superiorly between the right and the distal left atrium. Since this type of subdivided left atrium has not been reported, a more detailed description will be given:
and both
Type C: The proximal chamber is a midline chamber situated superiorly and is interposed between the right atrium and the distal chamber. The coronary sinus is normal. The foramen ovale borders the proximal chamber. All pulmonary veins enter the distal chamber (Fig. 4). Results The anatomic details of our cases are given in Table I and, schematically, in Figure 1. They are presented according to the classification given. It can be seen that the basic differentiating characteristics of the various types of subdivided left atrium pertain to (1) the location of the left atria1 chambers receiving the pulmonary veins, (2) the relation of the coronary sinus to these chambers, (3) the location of the fossa ovalis, (4) the absence or presence of associated partial anomalous pulmonary venous drainage, and (5) the site of such drainage. Type A: This is by far the most commonly observed category (23 of our 24 hearts). Within this category, group 1, the classic car triatriatum, is the largest subdivision (19 hearts). The membrane separating the two left atria1 chambers is fibromuscular and funnel shaped, with openings of various sizes. The proximal chamber is thick-walled, whereas the walls of the distal chamber are thin. The right atrium and right ventricle are hypertrophied and enlarged; the left ventricle is, on an absolute scale, smaller than normal. The various forms of subtotal car triatriatum and partial anomalous pulmonary venous drainage, type A, groups 2 to 5,2-11 are rare variations and are, as a
Case 24: This heart is from a 7 month old black girl who was mildly cyanotic and slightly tachypneic since early infancy. She failed to thrive (weight 4.3 kg at 7 months), but there were no other striking symptoms. When seen first at age 7 months her cardiac examination revealed: a heart rate of 120 beats/min, respiratory rate of 30/min, and blood pressure of 90/50 mm Hg. There was mild cyanosis but she had no signs of congestive failure. She had a mild right ventricular impulse. The first heart sound was normal; the second sound was narrowly split with an accentuated pulmonary closure. A third heart sound was present at the apex. A grade 3/6 pansystolic murmur was heard along the lower left sternal border. There was no diastolic murmur. The electrocardiogram revealed a mean frontal axis of 130’ and biatrial and right ventricular hypertrophy. The chest X-ray film demonstrated mild right ventricular enlargement and mildly increased pulmonary vascular markings. Cardiac catheterization data are given in Table II. Characteristic angiocardiographic frames are shown in Figures 4 and 5. Surgical procedure: Under deep hypothermia the right atrium was opened during complete circulatory arrest. A small defect in the fossa ovalis led into the proximal chamber. A normally formed limbus was present. A larger opening, leading from the proximal into the distal left atria1
FIGURE 4. Case 24. Frontal (left) and lateral (right) views of angiocardiogram after injection into the proximal left atrial chamber (bold arrow) of heart 24. In the frontal view the obligatory left to right shunt through a secundum type atrial septal defect (fine arrow) from the proximal chamber to the right atrium (RA) is seen as a cloud of contrast escaping into the right atrium. In the lateral view, a narrow stream of contrast medium from the proximal chamber into the posterior distal chamber (d LA) is seen (fine arrow). RV = right ventricle.
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(Table I). Of the remaining hearts 5 had associated lesions of milder character (patent ductus arteriosus in 3 cases, bicuspid aortic valve and straddling inferior vena cava); 14 hearts had complex lesions, involving predominantly the systemic venous return, the atria1 or ventricular septum or the large arteries.
TABLE II Cardiac
Catheterization
Data for Heart 24
0,
Saturation (%I Superior vena cava Right atrium Right ventricle Pulmonary artery Pulmonary capil!ary Proximal left atrial chamber Ascending aorta Pulmonary blood flow (liters/min par m*) Systemic blood flow (literslmin per ml) a = a wave; ED = enddiastolic;
Pressure (mm Ho)
42 67 77 79 99 96
a16.v8,m7 llO/ll ED 11 O/60. m 75 a 38, v 32, m 32 a 42, v 34, m 34
78
75155,
ET AL.
Discussion Classification
m 60
5.0 3.1
m = mean; v = v wave.
chamber, was probed. The entire proximal chamber was excised. After the infant was rewarmed, the main pulmonary artery was banded so that the peripheral pulmonary systolic pressure was reduced from 80 to 50 mm Hg. The infant died 36 hours after completion of the operation.
Pathologic findings: The heart was enlarged. Adjacent to the limbus fossa ovalis, which was well formed, was a large surgically created opening that included almost the entire atria1 septum. The roof of what was apparently a small proximal chamber was seen superiorly between the cut surfaces of septa separating the proximal chamber from the right atrium on the one side, the distal left atrium on the other. There was mitral atresia. Both the aorta and pulmonary artery arose from the right ventricle in a normal anteroposterior relation; a small ventricular septal defect led into a slit-like posterior left ventricle. The right and distal left atria as well as the right ventricle were hypertrophied and enlarged. A discrete coarctation of the aorta was present in typical location.
Associated cardiac lesions of subdivided left atrium: In only 5 of our 24 hearts was the subdivided left atrium the sole congenital cardiac anomaly
of car triatriatum have A variety of classifications been proposed15-1g stressing anatomic or hemodynamic characteristics, or both. Whereas James’s classification16 is a very broad one (including total anomalous pulmonary venous drainage into the coronary sinus, car triatriatum dexter and atria1 aneurysms), Van Praagh and Corsiniig restrict the name “car triatriatum” to only one particular heart (type A lb). From a pathologic viewpoint it seems more logical to include under the heading “subdivided left atrium” all hearts that have two distinct left atria1 chambers, regardless of the presumed morphogenetic origin.
Criteria for classification: Our classification of subdivided left atrium is an extension of the description by Lam et al. l2 of type A and B hearts. The extension was necessary to account for the anatomic variations of this complex in a systematic manner. Two criteria were used: 1. Anatomy: Separation of types A, B and C was based on the distinctly different location of the proximal chamber. For further grouping we chose, because of immediate surgical implications, the site of the partial anomalous pulmonary venous drainage. It is recognized that combined forms exist, for example, A3 and A4 (Fig. 1, heart of Wilson et al-?). 2. Embryology: The second criterion was the (presumed) morphogenetic origin of each heart. As will be shown, the proximal chamber in types A, B and C
FIGURE 5. Case 24. Frontal (left) and lateral (right) views of an angiocardiogram after right ventricular injection of contrast medium in heart 24. Both aorta (AO) and pulmonary artery (PA) arise from the right ventricle (RV). A slit-like posterior ventricle left was present (but not seen in this frame) with a small membraneous ventricular septal defect. The subaortic stenosis is not clearly visible.
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differs in embryologic origin. Furthermore, the relation of the fossa ovalis to either the proximal or distal chamber implies-according to our current understanding-a different morphogenetic pathway. To accent this nonuniform embryologic background of different forms of subdivided left atrium, groups 1 to 5 of type A were classified according to this relation of the fossa ovalis into subtypes a and b. Our classification is based on anatomy and does not depend on the physiologic disturbance created in an individual heart; it is meant to inform about the anatomic variations of this complex so that suitable surgical decisions can be reached.
nary sinus a common pulmonary venous trunk joins the coronary sinus by way of the remnant of the vertical vein, whereas in our type B the right or left pulmonary veins, or both, enter the proximal chamber separately. Incidence: Of all hearts with subdivided left atrium, type A lb is by far the most common. Exactly how many such hearts have been reported is difficult to estimate. Like Church,’ who failed to note the location of the fossa ovalis in his original description of this lesion, many subsequent investigators have not considered the location of the fossa ovalis with respect to the proximal or distal chambers a crucial criterion for car triatriatum. In our own material type A lb accounts for 50 percent of hearts. Since Van Praagh and Corsini’s review of slightly less than 100 hearts of this type in 1969, approximately 35 additional cases of type A have been reported, usually in surgical journals and with limited anatomic detail.2046 The various forms of subtotal car triatriatum (A 2) and car triatriatum with partial anomalous pulmonary venous drainage (A 3 to 5) are quite rare and almost always appear in single case reports. They represent the intriguing variations of the basic lesion. Similarly, type B and C hearts are extremely rare and, with the exception of type B 1,12have beenindividually reported.
Differentiation of types: Type A hearts are closely related to classic car triatriatum, whereas type B hearts resemble some aspects of total anomalous pulmonary venous drainage into the coronary sinus. The type C heart has some features in common with types A and B but has specific, separate characteristics. For the differentiation of these groups the location of the proximal chamber and the status of the coronary sinus are important. In general, in type A the proximal chamber is positioned at the basal aspect of the left atrium and drains primarily into the distal left atria1 chamber; the coronary sinus and its valve are normally formed. In type B the proximal chamber is located more medially and inferiorly at the posterior aspect of the left atrium. The coronary sinus ostium is demarcated by the coronary sinus valve, and the sinus consists of a rudimentary short channel. Most of the coronary venous blood appears to drain into the proximal chamber directly. In type C the coronary sinus is normally formed; the “proximal” chamber is a midline structure lying superiorly and interposed between right and distal left atrium. It opens into the right atrium through an atria1 septal defect (fossa ovalis type) and to the distal left atria1 chamber through an abnormal defect. The latter chamber receives all four pulmonary veins.
Hemodynamics
Type B versus total anomalous pulmonary venous drainage: These anatomic features described for type B hearts raise the question whether the proximal chamber in type B is a markedly dilated coronary sinus with an abnormal opening into the right atrium, associated with atresia of the distal portion of the coronary sinus immediately upstream to the coronary sinus valve. Type B subdivided left atrium and total anomalous pulmonary venous drainage into the coronary sinus are likely to be closely related; the presence or absence of a smaller or larger defect in the subdividing membrane is not of decisive significance. However, there are differences between the two lesions: (1) In total anomalous pulmonary venous drainage into the coronary sinus the mouth of the coronary sinus is a single large opening, related to the coronary sinus valve; in our type B it is small and usually blind; the proximal chamber drains through an abnormal defect into the right atrium. (2) In total anomalous pulmonary venous drainage into the coro-
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Diagnosis
Hemodynamics: The hemodynamic disturbance of these hearts is variable, and depends on (1) the size of the communication between the proximal and distal chamber, (2) the extent of left to right shunting through a defect between the proximal chamber and the right atrium directly or through an anomalous pulmonary venous connection, and (3) the character of associated cardiac lesions. The classification of Gasul et a1.17 (triatrial hearts with absent, small and large atria1 communications) accents these hemodynamic abnormalities. The patient with a subdivided left atrium of type A 1 and a large communicating defect between proximal and distal chambers will be virtually asymptomatic (a 70 year old patient of Loeffler47), whereas a small communication would result in early death (a 25 day old infant of Hosch48). The degree of right ventricular hypertrophy and pulmonary hypertension, typically found in patients with a subdivided left atrium, will parallel the degree of obstruction to outflow from the proximal chamber, and will determine the clinical findings if it is not complicated by associated defects. When there is significant obstruction to flow between the proximal and distal chambers or right atrium, severe dyspnea and related signs of pulmonary venous obstruction are dominant. If there are communications between the right atrium and the distal chamber, right to left shunts may occur and the child can be expected to be cyanotic. Angiographic diagnosis: A correct diagnosis can be made in most cases by cardiac catheterization. In
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SUBDIVIDED LEFT ATRIUM-THILENIUS
type A 1 hearts the subdividing membrane can be demonstrated well only by cineangiography; pressure data and the blood oxygen saturation levels will indicate the approximate extent of communicating defects between the left atria1 chambers and, possibly, the right atrium. Angiograms of the rarer types A 2 to 5 are more difficult to analyze; familiarity with the possible varieties of subdivided left atrium will permit selective and diagnostic injections of contrast medium. Cardiac catheterization data in type B hearts will have a striking resemblance to data in total anomalous pulmonary venous drainage into the coronary sinus. From a therapeutic point of view it is not significant to separate these two entities since the surgical methods of correction are virtually identical. Type C hearts are clearly diagnosed when injection of contrast medium into the midline chamber can be performed: The location of the chamber and the absence of retrograde filling of pulmonary veins clearly confirm the anatomy of the type C heart (Fig. 4). Surgical correction: For all hearts with subdivided left atrium surgical excision of the subdividing membrane is the treatment of choice. It will abolish obstruction, which almost always exists at this level. Closure of defects between the left and right atrium, and, for hearts of types A 3 to 5, correction of the anomalously draining pulmonary veins will establish normal hemodynamic relations. These repairs are life-saving, but they require correct preoperative diagnosis. When associated cardiac defects . are present, surgical corrections have to be tailored according to the entire complex. Associated
Cardiac
Lesions
Although some reports imply that car triatriatum is seldom associated with other cardiac defects, our material bears evidence to the opposite: In 19 of our 24 hearts there were significant additional anomalies, including, in 8 hearts, milder lesions such as patent ductus arteriosus, and in 11 hearts, severe and complex lesions such as mitral atresia (Table I). There was no particular pattern of associated lesions. Atrioventricular valve anomalies were noted as often (five hearts) as coarctation of the aorta (four hearts) and patent ductus arteriosus (four hearts). Tetralogy complex (three hearts) was seen as often as isolated ventricular septal defect (three hearts). This wide variety of associated malformations indicates a profound and diffuse disturbance in the development of the fetal heart rather than a specific lesion that might be explained by a single developmental defect. Morphogenesis
of the Subdivided
Left Atrium
It is tempting to search for a uniform embryologic explanation for the development of the subdividing membrane. The malseptation, the malincorporation and entrapment hypotheses are examples of such attempts; they have been discussed in detail by Van Praagh and Corsinilg and others.14J5**s-s2 The shortcoming of these hypotheses is that individual hearts
ET AL.
are taken to prove a cause, excluding other hearts that do not fit into the concept. For instance, both the malincorporation and entrapment hypotheses require that the fossa ovalis open into, or be directlyadjacent to, the distal chamber; although this frequently occurs (Fig. 3), there are hearts (Ref. 9, 51, Case 4 in Ref. 52 and our cases 1 to 6, 20 and 22) in which the foramen ovale opens unequivocally into the proximal chamber (Fig. 2). The entrapment hypothesislg is very convincing for type A lb hearts. For types A 2 to 5 there are additional anomalous pulmonary venous connections that are not uncommonly observed as separate malformations: drainage of one or more pulmonary veins into the right atrium or right superior vena cava. Such pulmonary venous anomalies can be explained by failure of some pulmonary veins to find their connection to the common pulmonary vein directly, joining instead other vascular structures. Considerable difficulties arise when one attempts to use current hypotheses to account for type A la or type C hearts in which the fossa ovalis (foramen ovale or secundum atria1 septal defect) separates the right atrium from the proximal chamber. Van Praagh and Corsini’s studiesi of the normal development of the left atria1 region and common pulmonary vein in human embryos are instructive in this context. At the 10 mm stage (horizon 16) the sinus venosus tissue, the common pulmonary vein and the left horn of the sinus venosus are directly adjacent structures. The sinus venosus tissue, derived from the right horn of the sinus venosus, differentiates into the septum primum and the left venous valve; a cleftlike intersepto-valvular space is formed between them. The common pulmonary vein passes immediately beneath this tissue. One might speculate that abnormal growth in this area results in an abnormal communication of the common pulmonary vein with the sinus venous tissue and that possibly the intersepto-valvular space might be the predecessor of the proximal chamber of type A la and type C hearts. The fossa ovalis would then indeed be related to the proximal and not the distal chamber. This would represent a type of malseptation and the hypothesis is consistent with Van Praagh and Corsini’s conclusion “that the basic abnormality involves the endothelium of the right horn of the sinus venosus, not the endothelium of the common pulmonary vein.“ig The direct spatial proximity of the left horn of the sinus venosus (the future coronary sinus) and the common pulmonary vein at the 10 mm stage lends itself to the formation of an abnormal direct communication between these two structures, resulting in the B malformation of subdivided left atrium. Although these speculations cannot be proved, they represent possible morphogenetic pathways to explain the anatomic fact of a type A la or type C heart just as the entrapment hypothesis explains the type A lb heart.
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SUBDIVIDED LEFT ATRIUM-THILENIUS
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