CLINICOPATHOLOGIC CORRELATIONS Alternate Pathways to ...

CLINICOPATHOLOGIC CORRELATIONS

Alternate Pathways to Pulmonary Venous Flow inLeft-sided Obstructive AnomaliesBy CHARLES B. BECKMAN, M.D., JAMES H. MOLLER, M.D.,

AND JESSE E. EDWARDS, M.D.

SUMMARYIn cardiac anomalies causing severe obstruction in the left side of the heart, such as aortic atresia, mitral

atresia, or occasionally severe aortic stenosis, maintenance of circulation depends upon shunting ofpulmonary venous blood into the right atrium. The usual pathway by which the shunt is achieved is across

the atrial septum through the foramen ovale.When this route is closed or severely narrowed, alternate but less common pathways may exist. These in-

volve either anomalous connections of pulmonary veins to systemic veins or communications with the cor-

onary venous system. In the latter, as commonly occurs in aortic atresia, left ventricular myocardialsinusoids carry pulmonary venous blood from the left ventricular cavity and into the cardiac veins. In otherinstances of severe left-sided obstruction, a direct communication may exist between the left atrium and thecoronary sinus.

CERTAIN CONGENITAL ANOMALIES repre-

sent major or absolute barriers to the flow of bloodthrough the left side of the heart. Mitral atresiaand/or aortic atresia are absolute barriers. In each ofthese, maintenance of circulation depends upon thepulmonary venous blood reaching the right atrium inwhich chamber it mixes with the returning systemicvenous blood. From the right atrium, blood is carriedinto either the right ventricle or a single ventricle,depending upon the type of cardiac anomaly (fig. 1).While aortic and/or mitral atresia represent ab-

solute barriers to flow through the left side of theheart, other conditions such as aortic stenosis, al-though possessing a patent orifice, may be sufficientlyobstructive to show a similar pattern of the cir-culation to that of mitral or aortic atresia.

Although in these obstructive lesions, the flow intothe right atrium usually occurs through the foramenovale route, alternatives to this may exist in certainpatients. Such pathways involve systemic and/orpulmonary veins. Angiographic demonstration of

From the Department of Pathology, United Hospitals-MillerDivision, St. Paul, and the Departments of Pathology, Surgery andPediatrics, University of Minnesota, Minneapolis, Minnesota.

Supported by USPHS Research Grant 5 ROI HL05694 andResearch Training Grant 5 TOI HL05570 from the National Heartand Lung Institute.

Address for reprints: Jesse E. Edwards, M.D., Department ofPathology, United Hospitals-Miller Division, St. Paul, Minnesota55102.

Circulation, Volume 52, September 1975

these channels may lead to confusion in interpreta-tion. They may be interpreted incorrectly as primaryanomalies of the pulmonary veins or other structureswhen, in fact, they represent compensatory phenom-ena to a fundamental obstructive condition within theleft side of the heart.Our discussion will consider the major alternative

pathways that may occur in patients with left-sidedobstructive lesions. In all patients with obstructiveanomalies of the left side of the heart, certaincollateral pathways are present but are ineffectivesince the volume of flow through them is small. Theseinclude pulmonary-bronchial venous connectionswithin the lungs' and thebesian venous connectionsbetween the two atria.

The Usual Alternate Route - The Foramen Ovale

In the conditions under discussion, the usualalternate route for pulmonary venous flow is across theatrial septum through the foramen ovale.The normal structure of the foramen ovale mech-

anism allows free flow of blood from the right atriuminto the left atrium and prevents flow in the oppositedirection. In mitral atresia or other conditionscharacterized by obstruction through the left side ofthe heart, including aortic atresia or some cases of aor-tic stenosis, the left atrial pressure rises to abnormallyhigh levels. The elevated pressure causes the valve ofthe foramen ovale to bulge toward the right. Even-tually, the free edge of this valve herniates into the

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BECKMAN, MOLLER, EDWARDS

Figure 1

Diagrammatic portrayal of classic examples of obstructive anomalies in the left side of the heart that require alternateroutes for the flow of blood. a) Mitral atresia uith common ventricle. b) Mitral atresia with two ventricles and a ven-tricular septal defect. c) Aortic atresia.

right atrium (fig. 2). This process leads to in-competence of the valve of the foramen ovale andallows a transatrial left-to-right shunt of pulmonary

Figure 2

Diagrammatic representation of the region of the foramen ovaleshowing progressive herniation of the valve of the foramen ovale (I)through the foramen ovale into the right atrium (R.A.). L.A. = leftatrium. Such changes create the usual alternate route for flow ofblood in severely obstructive anomalies in the left side of the heart.

venous blood into the right atrium (fig. 3). Althoughthe transatrial shunt permits the circulation of blood,the opening in the atrial septum is usually of limitedcaliber and signs of pulmonary venous hypertensionare present.

Uncommon Alternate Routes

While the foramen ovale represents the classicalroute for decompression of the left atrium in theobstructive anomalies being considered, there aresituations wherein the fbramen ovale is either sealedor so narrow as to be an even more ineffective channelthan usual. Under this circumstance other alternateroutes exist if life is maintained. These involve eitheranomalous pulmonary venous drainage to systemicveins or to the coronary venous system.

Anomalous Pulmonary Venous Drainage to Systemic Veins

When pulmonary veins contribute to decom-pression of the left atrium, one or more anomalousconnections may exist between the pulmonary venoussystem or left atrium on one hand, and a systemic veinon the other.Multiple Extrapulmonary Anomalous Pulmonary Venous Con-nections

In a case of mitral atresia, Shone and Edwards2observed that in each lung the veins converged toform one vein. From each lung, in turn, the singlemajor vein ascended in the mediastinum to join theleft innominate vein independently of the other (fig.4a).


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LEFT HEART OBSTRUCTIONS

D

Figure 3Herniation of the valve of the foramen ovale into the right atrium in a case of mitral atresia. a) Left atrium (L.A.). Thevalve (V.) of the foramen ovale has herniated toward the right atrium creating a defect (D.) in the atrial septum. b) Rightatrium (RA.). The valve (V.) of the foramen ovale has herniated into the right atrium creating a defect (D.) for anobligatory left-to-right shunt.

Solitarynection

Extrapulmonary Anomalous Pulmonary Venous Con-

In another case of mitral atresia, Shone andEdwards2 observed that the right upper and lower andthe left lower pulmonary veins joined the left atriumnormally. In contrast, the left upper pulmonary veinascended in the mediastinum to join the left in-nominate vein. Within the left lung, a bridging veinjoined its upper and lower veins. The connectionsallowed right pulmonary venous blood to enter theleft atrium whence it flowed into the left lower

Figure 4

Pulmonary venous anomalies associated with mitral atresiadescribed by Shone and Edwards.2 a) From each lung, an

anomalous vein extends to join a systemic vein (S. V.). b) The rightpulmonary veins (R.P.V.) join the left atrium normally, as does thelower of the left pulmonary veins (L.P. V.). Within the left lung, a

bridge joins the lower and upper veins. From the latter, an

anomalous vein joins a systemic vein (S. V.).

Circulation, Volume 52. September 1975

pulmonary vein. From the latter, the blood thenentered the left upper vein through the in-trapulmonary venous bridge in the left lung. Finally,through the anomalous connection of the left upperpulmonary vein, the blood was carried into the left in-nominate vein and ultimately terminated in the rightatrium (fig. 4b).A variant of the foregoing was observed by us in a

case of aortic stenosis with a hypoplastic left ventricleinvolved with endocardial fibroelastosis. In that case,described by Hunt and associates,3 the fourpulmonary veins joined the left atrium in normalfashion. An anomalous vein extended from the leftupper pulmonary vein to the left innominate vein (fig.5a). During life, a selective pulmonary arteriogramhad been performed. In the late phase of this study,the pulmonary venous structures, including theanomalous vein, were clearly identified (fig. 5b). Thecase serves to emphasize the point that clear visualiza-tion of an anomalous pulmonary vein might be inter-preted as a primary anomaly while, in fact, itrepresented a collateral channel in the presence of asevere degree of left ventricular inflow obstruction.

Levoatriocardinal Vein

In a variant of anomalous pulmonary venousconnection, the pulmonary veins join the left atriumand, in addition, another vein extends from the leftatrium to a systemic vein (fig. 6). McIntosh, in 1926,4recognized this vein as an avenue of exit of blood from

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Figure 5

Severe aortic stenosis with anomalous pulmonary venous connection between left upper pulmonary vein and innominatevein (from case described by Hunt and associates'). a) Diagrammatic representation of the central circulation. In additionto normal union of the pulmonary veins with the left atrium, an anomalous connection exists between the left upperpulmonary vein and left innominate vein in a case with severe aortic stenosis and hypoplastic left ventricle. b) Late phaseof selective pulmonary arteriogram showing the pulmonary venous system and the left side of the heart. An anomalousconnection between the left upper pulmonary vein and the left innominate vein is clearly visualized.

the left atrium in a case of mitral atresia andpremature closure of the foramen ovale. Later, similarcases were described by Harris and co-workers5 and byBellet and Gouley.6 In 1950, such a vein wasdesignated by Edwards and DuShane7 as alevoatriocardinal vein. Subsequently, Lucas andassociates8 described an additional case in a subjectwith mitral atresia.

Anomalous Pulmonary Venous Drainage to Coronary VenousSystem

When the coronary venous system supplies analternate route for pulmonary venous flow, the essen-tial structure may be either the left ventricularmyocardial sinusoids or the coronary sinus.

Left Ventricular Myocardial Sinusoids

In aortic atresia with intact mitral valve and incertain cases of severe degrees of congenital aorticstenosis, an alternate route for pulmonary venous flowappears to be through myocardial sinusoids. In theseconditions, left ventricular systolic pressures are at ab-normally high levels, as blood in this chamber istrapped by a competent mitral valve and an

R.RV.

R.A.

Figure 6

Levoatriocardinal vein. In addition to nornal connection of thepulmonary veins with the left atrium, a levoatriocardinal vein(L.A.C. V.) extends to join a systemic vein (S. V.) and represents anessential alternate route for flow of blood in this case of mitralatresia with premature closure of the foramen ovale.

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Figure 7Enlarged myocardial sinusoids in aortic atresia. a) Leftatrium (L.A.) and left ventricle (L.V.) in a case of aorticatresia. The left ventricular cavity is small. Numerousdepressions in its lining represent ostia of enlarged myocar-dial sinusoids. Within the myocardium, the latter are visible.b) ILow power photomicrograph of left ventricular wall. Theendocardium (E.) is greatly thickened. A sinusoid (S.)courses from the left ventricular cavity (L. V.) into themyocardial wall. Elastic tissue stain; x 70. c) Postmortem leftventriculogram. Opacified vessels extend from the cavity ofthe left ventricle (I .V.) into the wall.

obstructed left ventricular outlet. It is probable thatblood from the left ventricle is forced out into myocar-dial sinusoids that communicate with this chamber.From the sinusoids, blood may escape through threeavenues, namely, (1) the myocardial veins, (2)ramifications of coronary arteries, or (3) directly into


myocardial capillaries. From any or all of these sites,blood would ultimately be delivered to the rightatrium through the coronary sinus.The escape of blood from the left ventricle is com-

parable to escape from the right ventricle in instancesof pulmonary atresia with intact ventricular septum

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4

Figure 8

Aortic atresia. a) Enlarged left ventricular myocardial sinusoids. Elastic tissue stain; x 20. b) Extenor Of ventricular portion

of heart. Enlarged and tortuous coronary arteries are present.

and competent tricuspid valve.9 10

Supportive anatomic evidencepulmonary venous blood through

R.R

for escape ofmyocardial sin-

L.R V.

S.V.C.

,tL.P.V.

b.

usoids in aortic atresia include (1) gross communi-cation of sinusoids with the left ventricular cavity (fig.7), (2) the presence of numerous dilated sinusoids inthe left ventricular wall (fig. 8a), and (3) prominentcoronary arteries (fig. 8b).

Coronary Sinus

Uncommonly, there may be one or several largeopenings between the coronary sinus and left atrium.If no other anomalies are associated, a left-to-rightshunt occurs through the abnormal opening(s) intothe coronary sinus and finally the right atrium. Suchan opening provided a vital route by allowing a right-to-left shunt in a case of tricuspid atresia withrestricted foramen ovale described from theselaboratories by Rose and associates."1

If an obstructive anomaly is present in the left sideof the heart, a communication between the coronary

sinus and left atrium may provide a route for left atrial

Figure 9

Communication of coronary sinus with left atrium in mitral atresta.a) An ostiurm of the coronary sinus communicates the vessel with theleft atrial cavity. This represents a hypothetical arrangementwhereby in mitral atresia left atrial blood may course into the rightatrinum through the coronary sinus. b) Communication of coronarysinus with left atrium and with a persistent left superior vena cava(L.S.V'.C.) in mitral atresia. From the case of which angiocar-diograms are shown in figure 10.


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decompression (fig. 9a). In the one case of this type Ductus Artwhich we observed, and to which reference is made inthe report of Rose and associates, we observed that svc R.PA

,<:~~~~~~~~~~~~~~~~~~~~~~~~~~~LPA^1 1 1@^ '- - V t T ~~~~~~~~~~~~~R.V

*|g:i;i;:0j;:;;0;:;; ;;;..g.,...,.(E~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~..........

Figure 11~~~~ ~~~Aortic atresia with premature closure of the foramen ovale and a

congenital arteriovenous fistula between the left circumflex coronary artery and the coronary sinus. Through myocardial sinusoids,blood from the left ventricular cavity may be carried into the cor-onary arteries and ultimately into the coronary sinus for delivery tothe t atri m. rom case descr bed by Raghib and associa tes.;

there was also a persistent left superior vena cava (fig.g9b). During right-sided catheterization with angiocar-diography, the catheter had been advanced into thecoronary sinus. Injection of contrast material resulted

_ in simultaneous opacification of the left atrium, the0:0 00:coronary sinus and the left superior caval system (fig.

~~~~~~~~~10).Another situation in which the coronary sinus par-

ticipated was described by Raghib and associates'2from these laboratories. It involved a newborn infantwith aortic atresia and premature closure of theforamen ovale. A fistula was present between the leftcircumflex coronary artery and the coronary sinus.Numerous ostia of myocardial sinusoids wereobserved in the left ventricle. It is presumed that

.....elevated left ventricular pressure caused left ven-tricular (pulmonary venous) blood to be forcedthrough myocardial sinusoids into the coronaryarteries. From the left coronary arterial system, bloodwas delivered through the fistula into the coronarysinus for ultimate arrival in the right atrium (fig. 11).

Figure 10

Successive angiograms in the case of mitral atresia of which theessentials are illustrated in figure 9b. The catheter has passedfromthe right atrium into the coronary sinus. There is opacification bothof the left atrial cavity and of the left superior vena cava and, ul-timately, the right side of the heart.

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References1. BECKER AE, BECKER MJ, EDWARDS JE: Dilated bronchial veins

within pulmonary parenchyma. Observations in congenitalpulmonary venous obstruction. Arch Pathol 21: 256, 1971

2. SHONE JD, EDWARDS JE: Mitral atresia associated withpulmonary venous anomalies. Br Heart J 241, 1964

3. HUNT CE, RAO S, MOLLER JH, EDWARDS JE: Anomalouspulmonary vein serving as collateral channel in aorticstenosis with hypoplastic left ventricle and endocardialfibroelastosis. Chest 57: 185, 1970

4. MCINTOSH CA: Cor biatriatum triloculare. Am Heart J 1: 735,1926

5. HARRIS HA, GRAY SH, WHITNEY C: Heart of child aged 22months presenting anomalous vein from pulmonary auricleto right internal jugular vein, transposition of great vesselsand left superior vena cava. Anat Rec 36: 31, 1927

6. BELLET S, GOULEY BA: Congenital heart disease with multiplecardiac anomalies. Report of a case showing aortic atresia,fibrous scar in myocardium and embryonal sinusoidal

remains. Am J Med Sci 183: 458, 19327. EDWARDS JE, DUSHANE JW: Thoracic venous anomalies. Arch

Pathol 49: 517, 19508. LUCAS RV JR, LESTER RG, LILLEHEI CW, EDWARDS JE: Mitral

atresia with levoatriocardinal vein. A form of congenitalpulmonary venous obstruction. Am J Cardiol 9: 607, 1962

9. WILLIAMS RR, KENT GB JR, EDWARDS JE: Anomalous cardiacblood vessel communicating with right ventricle; obser-vations in a case of pulmonary atresia with intact ventricularseptum. Arch Pathol 52: 480, 1951

10. LAUER RM, FINK HP, PETRY EL, DUNN MI, DIEHL AM:Angiographic demonstration of intramyocardial sinusoids inpulmonary-valve atresia with intact ventricular septum andhypoplastic right ventricle. N Engl J Med 271: 68, 1964

11. RoSE AG, BECKMAN CB, EDWARDS JE: Communication betweencoronary sinus and left atrium. Br Heart J 36: 182, 1974

12. RAGHIB G, BLOEMENDAAL RD, KANJUH VI, EDWARDS JE: Aorticatresia and premature closure of foramen ovale. Am Heart J70: 476, 1965


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C B Beckman, J H Moller and J E EdwardsAlternate pathways to pulmonary venous flow in left-sided obstructive anomalies.

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright © 1975 American Heart Association, Inc. All rights reserved.

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