- Email: [email protected]
Partial anomalous pulmonary venous connection and drainage
DIAGNOSTIC SHELF
Partial Ammalaus PulmonaryVenous Connection and Drainage EUGENE MASCARENHAS. ROGER P. JAVIER, MD PHILIP
SAMET,
MD,
MD
FACC
Miami. Florida
The clinical, diagnostic and pathophysiologic features of types of partial anomalous pulmonary venous connection age seen in 6 adult patients are presented. This distinct entity is perhaps more commonly prevalent than has been believed. It may be associated with other cardiac and anomalies and also with acquired rheumatic valve disease.
5 different and drainanatomic previously pulmonary
A pulmonary vein is said to be anomalously connected when it fails to communicate normally with the left atrium and instead connects to the right side of the heart, that is, right atrium, coronary sinus or the venae cavae or their tributaries. Partial anomalous pulmonary venous connection is said to be present when some, but not all, pulmonary veins are aberrantly connected. The term “connection” is used to define an anatomic relation and “drainage” to indicate its physiologic effect.’ The embryologic basis2*3 for these pulmonary venous aberrations is well recognized. However, this anomaly remained a pathologic curiosity until 1949 when Dotter et a1.4 and Irishman the clinical diagnosis by roentgenography, cardiac et al.” reported catheterization and angiography. Advances in surgical techniques have now made these anomalies at least potentially correctable. Opt imal preoperative planning requires accurate determination of the sites of anomalous connection, evaluation of the magnitude of shunt flow and presence of associated cardiac lesions. The purpose of this paper is to present the clinical and diagnostic features of 5 different types of partial anomalous pulmonary venous connection
seen
in 6 adult
patients.
Methods All patients were evaluated hy a clinical history, physical examination, electrocardiogramS radiography and fluoroscopy. Right heart catheterization and attempts to enter the anomalous pulmonary veins and to cross an atrial septal defect were made in each patient. I,eft heart transseptal catheterization was carried out in :! patients. Blood oxygen determinations were obtained in 4 cases. Standard angiographic methods were adopted to visualize aberrant vessels and their connections. Differential bronchospirometry was performed in 1 case. I,eft to right shunt flow was determined by the nitrous oxide method in 3 patients. lndocyanine green dye-dilution curves were recorded” in 4 patients and ascorhate indicator dilution curves in 1 patient.
Results From the Division of Cardiology, Department of Internal Medicine, Mount Sinai Hospital of Greater Miami and the University of Miami Medical School. Miami. Fla. Manuscriot received May 9. 1972; revised manuscript received Au&st 15. 1972. accepted Sebtemhm37 _“.
_.
,
IQ73 .-SC.
Address for reprints: Eugene Mascarenhas. MD, Mount Sinai Hospital. 4300 Alton Rd.. Miami Beach, Fla. 33140.
512
April 1973
The clinical, patients presented
with
electrocardiographic partial
in Table
anomalous
I. The
and
radiologic features of the 6 venous connection are findings are shown in Table
pulmonary
hemodynamic
II. Case I. Anomalous drainage of the left superior pulmonary vein (LSPV) into the left innominate vein: A 31 year old housewife was referred to us in March 19,X3 for evaluation of a heart murmur that was first detected at age 1:). She had had no cardiovascular symptoms even during 3
The American Journal of CARDIOLOGY
Volume 31
PARTIAL
TABLE
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
I
Clinical,
Electrocardiographic
and Radiologic
in 6 Patients with Partial Anomalous
Features
Pulmonary
Venous Connection
Physical Signs
Case
Age
no.
Race/Sex
1
N/P
31
2
C/P
54
3 4
C/F
5
C/F C/M
41 la 30
6
C/M
35
C = Caucasian;
Symptoms
(yr)
Thrill
Cardiac neurosis, heart murmur Dyspnea Fatigue Effort dyspnea Recurrent bronchitis Asymptomatic
N = negro;
IRBBB
+
Chest Rosntgenogram
Accentuated P2
Grade
Location
-
316
ULSB
Normal
-
+
316
IRBBB
+
+
-
+ -
316
Mitral area ULSB ULSB -
IRBBB IRBBB ST-T wave
+ + -
+ + -
+
ULSB
changes IRBBB
Systolic Murmur
416
216
= incomplete
right
bundle
branch
block; ULSB
ECG
= upper
left sternal
Heart Size
Increased Pulmonary Vascularity
Anomalous Vein
+ border.
presence of a left to right shunt. Dye curves were then obtained after selective injection of dye into the right and left pulmonary arteries with simultaneous sampling from the femoral artery and right atrium (Fig. 1). The curves after right pulmonary arterial injection were normal; those after left pulmonary arterial injection revealed a left to right shunt and an early right atria1 appearance time. Constant left pulmonary arterial injection with serial sampling from the right heart chambers and at different sites in the superior vena cava localized the anomalous draining site to the left innominate vein (Fig. 2). Fifty cubic centimeters of contrast material injected into the left pulmonary artery subsequently outlined an anomalous left superior pulmonary vein, 2 cm in diameter, traversing the medial left upper lung field, overlapping the aorta and joining the left innominate vein (Fig. 3). The degree of shunt flow was calculated to be approximately 28 percent by the use of the nitrous oxide method. Case 2. Communication of left superior pulmonary vein and innominate vein by way of a persistent left superior vena cava in a patient with rheumatic mitral
uncomplicated pregnancies. For the past 5 years she showed marked concern over her heart murmur. Examination of the cardiovascular system was essentially normal, except for a grade 3/6 ejection systolic murmur along the left sternal border (Table I). The electrochest cardiac fluoroscopic examination, cardiogram, roentgenogram and right heart pressures were all found to be normal (Table II). Blood oxygen determinations during right heart catheterization revealed that the oxygen content of blood in the inferior vena cava (13.2 vol percent) was less than the oxygen content in the right atrium (15.5 vol percent) and superior vena cava (15.3 vol percent). The findings of this reverse relation in oxygen content alerted us to the presence of a left to right shunt. Since blood of high oxygen content was found in the superior vena cava with no significant step-up in the right atrium, it was considered probable that the interatrial septum was intact and that an anomalous pulmonary vein drained into the superior vena cava or its tributaries. Injection of indocyanine green dye into the main pulmonary artery and sampling in the femoral artery confirmed the
TABLE
ET AL.
II
Hemodynamic
Data and Oxygen Studies in 6 Patients with Partial Anomalous
Case
IVC or SVC
no.
02
RA
02
P
-__ OaC
RV
PA
P
02
Pulmonary
Pulmonary
LA
P
Venous Connections
o*c
P
Vein 02
Systemic Artery 02
P
Shunt
Asso-
flow No
ciated Cardiac Lesions
Me;hod
13.2*; 15.3 -
15.5 -
-2 5
15.0 -
20/O 37/Z
15.1 -
1718 36119
-
17
-
17.5 -
14cria5 124175
28% -
-
-
-
la.9
130185
45%
MS Ml ASD
13.4*; 15.2
16.4
1
16.9
24/Z
16.9
22113
12.3 -
16.3 -
4 1
16.7 -
2214 2212
17.4 -
1817 18/6
18.0 -
-
la.2 -
la.2 -
121170 110165
-
ASD -
19.2*; 15.8
17.8
2
17.8
2315
la.3
20/10
-
-
20.1
20.5
110166
36%
-
* Inferior vena cava. ASD = atrial septal defect; IVC = inferior vena cava; LA = left atrium; Ml = mitral insufficiency; MS = mitral stenosis; O2 = oxygen content (%); P = pressure (mm Hg); PA = pulmonary artery; RA = right atrium; RV = right ventricle; SVC = superior vena cava.
April 1973
The American Journal of CARDIOLOGY
Volume 31
513
PARTIAL
RPA
ANOMALOUS
to FA
and
PULMONARY
RA
VENOUS
CONNECTION-MASCARENHAS
LPA
to FA
and
ET AL.
RA
FIGURE 1. Case 1. Anomalous pulmonary venous connection and drainage of the left upper lobe pulmonary vein to the left innominate vein with an intact interatrial septum. Localization of the site of the left to right shunt by selective right (RPA) and left (LPA) pulmonary arterial injection. Simultaneous samplings from the femoral artery (FA) and right atrium (RA) reveals a left to right shunt after injection into the left but not the right pulmonary artery, The appearance times are corrected for the dead space volumes of the respective sampling systems.
5.8:.
L PA
TO SVC
2”ABOVE
R A
L PA
TO S VC
4”ABOVE
R A
Mid - point In /action
miwh
FIGURE 3. Case 1. Angiographic demonstration of anomalous left superior pulmonary venous (LSPV) drainage into the left innominate vein (IV).
514
April 1973
The American
Journal of CARDIOLOGY
FIGURE 2. Case 1. The left to right shunt after left pulmonary arterial injection is evident in the superior vena cava after sampling 2 inches above the right atrium but not 4 inches above this chamber.
m(nat IIi I
valve disease7: A 54 year old white married woman with rheumatic valvular heart disease was referred to us for hemodynamic evaluation in March 1965 because of progressively increasing dyspnea over the past 10 years (Tables I and II). The pertinent hemodynamic abnormalities were moderate mitral valve stenosis (left atrial-left ventricular mean diastolic gradient 8 mm Hg), mild mitral and tricuspid valvular insufficiency and mild pulmonary hypertension. At transseptal left heart catheterization injection of indocyanine green dye into the left atrium with right heart sampling from the pulmonary artery, right ventricle and right atrium revealed an early appearance time in each chamber, suggesting a left to right shunt. An early appearance time was also observed by sampling the superior vena cava, but not in the high right jugular system. Left atria1 and left ventricular cineangiograms showed no interatrial or interventricular septal defects. The site of the left to right shunt was not clearly established at the time of this study. During open heart surgery moderately severe mitral valve stenosis was noted. The dependent portion of the
Volume 31
PARTIAL
S.V.C.
FIGURE injection
to
L.B.A.
(G-6-4WIW”tR.A.)
ANOMALOUS
PULMONARY
Low R.A. to L.B.A.
(G-6-42)
VENOUS
CONNECTION-MASCARENHAS
1.v.c. t0
L.B.A.
(~-6-42)
ET AL.
(~“AR.A.)
4. Case 3. Sinus venosus type of atrial septal defect. Systemic arterial sampling after inferior vena caval (C) and right atrial (B) reveals a small right to left shunt. However, the shunt is best noted after injection into the superior vena cava (A).
left atrium showed a brisk flow of unoxygenated blood in the area of the left superior pulmonary vein. Insufflation of the lung failed to change the color of the blood. The heart and mediastinum were rotated to the right, and a large vein (left superior vena cava) on the left side was seen to communicate with the normally placed left superior pulmonary vein. After the left superior vena cava was ligated, the flow of unoxygenated blood ceased. A mitral valvuloplasty was performed, and the patient was discharged after an uneventful hospital course. On restudy 6 months postoperatively the left to right shunt was no longer demonstrable. Case 3. Drainage of right pulmonary veins into the right atrium with an atria1 septal defect (sinus venosus type): A cardiac murmur was first detected in a 41 year
old white woman at age 4 years. For the past three years she had been experiencing paroxysmal attacks of atria1 fibrillation. The salient features on examination in 1960 were right ventricular and pulmonary arterial pulsations. The second heart sound was widely split, varied little with respiration, and the pulmonic component was accentuated. A grade 3/6 ejection systolic murmur was best heard over the pulmonic area. Fluoroscopic examination of the chest showed an enlarged heart (right atrium and right ventricle) and a very prominent pulmonary arterial segment with increased pulmonary vascular markings but no hilar dance. The electrocardiogram showed incomplete right bundle branch block (QRS duration 0.11 second). Intracardiac right heart pressures were normal. (Table II). Blood oxygen studies revealed a significant oxygen step-up at the atria1 level. The catheter tip could not be passed either into an anomalous pulmonary vein or into the left atrium by way of an atria1 septal defect. Indocyanine curves obtained after selective injections into the right and left pulmonary artery with systemic arterial sampling showed a greater magnitude of left to right shunt flow after right rather than left pulmonary arterial injection. Such preferential flow is not pathognomonic of an atria1 septal defect with partial anomalous pulmonary venous return from the right lung, and since it can also occur in an ostium secundum atria1 septal defect with normal pulmonary venous connections.8 Indocyanine green dye curves after inferior and superior venae caval injection with systemic arterial sampling were carried out.
A larger right to left than from the inferior This finding favors a defect with anomalous the right lung rather atria1 septal defect.
shunt from the superior vena cava vena cava was noted. (Figure 4.) sinus venosus type of atria1 septal pulmonary venous connection from than an ostium secundum type of
Case 4. Drainage of right pulmonary veins into the right atrium with an atria1 septal defect (sinus venosus type): An 18 year old white girl9 had noted mild, nonprogressive exertional dyspnea for many years and was first seen by us in 1957. The clinical, fluoroscopic and electrocardiographic features (Table I) suggested a diagnosis of atria1 septal defect or anomalous pulmonary venous drainage, or both. On cardiac catheterization (Table II), the catheter tip was easily manipulated from the caudal superior vena cava and right atrium into the right pulmonary veins establishing the diagnosis of anomalous connection of right pulmonary veins. However, the catheter tip could not be manipulated through an atria1 septal defect, and the presence of this additional lesion could not be ruled out. To determine whether the entire right pulmonary venous drainage was into the right atrium, bronchospirometry was performed. A Carlens catheter9 was passed into the trachea so as to separate the ventilatory pathways of the right and left lungs. Different gas mixtures were then applied to the 2 lungs and serial measurements of arterial blood oxygen saturation were made. On room air the arterial oxygen saturation was 94 percent. When pure nitrogen (oxygen content 0.16 percent) was given to the right lung (the site of the anomalous pulmonary venous connection), and 24 percent oxygen to the left lung, the arterial oxygen saturation remained unchanged after 10 minutes. When the gas mixtures were reversed, arterial saturation decreased rapidly to 73 percent within 3 minutes. These findings together with the catheterization data, led to the diagnosis of virtually total unilateral (right-sided) anomalous venous connection and drainage. A second cardiac catheterization study was performed a year later. On this occasion the catheter tip was passed through an atria1 septal defect into the left atrium and left ventricle. At operation in 1961, the entire venous drainage of the right lung was noted to return to the right side of the heart, the superior pulmonary vein emptying into the
April 1973
The American Journal of CARDIOLOGY
Volume 31
515
PARTfAL
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
ET AL.
calized. Auscultation of the heart was normal. A chest X-ray film showed the typical radiologic features of the “scimitar syndrome,“10 that is, (1) a scimitar-shaped density parallel to the right paracardiac border; (2) decreased right hemithorax; (3) shift of the cardiac shadow to the right; and (4) hypoplastic right pulmonary artery (Fig. 5). Cardiac catheterization revealed normal right heart pressures. Ascorbic acid dye curves with injection into each pulmonary artery with femoral arterial sampling detected a large left to right shunt after right pulmonary arterial injection. Injection of indocyanine green dye into the right pulmonary artery revealed an early right atria1 appearance time; when the tip of sampling catheter was positioned 3 inches below the diaphragm, a normally delayed appearance time was noted (Fig. 6). Pulmonary angiocardiograms demonstrated that the right pulmonary arterial tree was hypoplastic. The veins from the right lung joined to form a single large vessel adjacent to the right cardiac border and drained into the inferior vena cava 1 l/2 inches below the diaphragm. FIGURE 5. Case 5. “Scimitar syndrome.” The chest roentgenogram illustrates displacement of the cardiac silhouette to the right. A multibranching scimitar-shaped shadow is seen parallel to the right heart border and courses toward the diaphragm.
lower superior vena cava and the right inferior pulmonary vein into the upper right atrium. The lesions were appropriately corrected, and a 2 year follow-up evaluation showed no left to right shunt. Case
rior
5. Drainage
vena
cavae
of right pulmonary (scimitar syndrome):
veins into infeA 30 year old
white man complained of recurrent asthmatic bronchitis since age 10. Physical examination in 1965 revealed a mildly tachypneic patient. Diffuse rhonchi were heard over both lung fields. The right hemithorax was less expansile than the left. The cardiac impulse could not be lo-
I RPA
toFA
Case 6. Scimitar sign: A 35 year old asymptomatic man was referred to us in 1958 because a routine chest X-ray examination disclosed a scimitar-shaped opacity, parallel to the right heart border. Physical examination was essentially normal except for a Grade 3/6 ejection systolic murmur along the left sternal border. On cardiac catheterization oxygen content of the inferior vena caval blood (19.2 vol percent) was greater than that of blood samples obtained from the superior vena cava (15.8 vol percent) and right atrium (17.8 vol percent). The catheter tip was manipulated from the right atrium into the inferior vena cava and out into the right lower lung fields (Fig. 7). The oxygen content (20 vol percent) in this pulmonary vein matched the arterial oxygen content. The atria1 septum was ‘probed and felt to be intact. Shunt flow was calculated to be 36 percent of the total pulmonary blood flow.
andRA
, , RPA
toFA.andIVC
Mid-point Injection
7 set 1A T: 6.3-3.4 set
: I I I
FIGURE 6. Case 5. After right pulmonary arterial injection, the inferior vena cava 4 inches below the diaphragm.
516
April 1973
The American Journal of CARDIOLOGY
an early right atrial appearance
Volume 31
time is evident:
this finding
is not noted in
PARTIAL ANOMALOUS PULMONARY
VENOUS O~NNEOTI~N-MASCARENHAS
ET AL.
Discussion The development of new diagnostic techniques has increased the detection of partial anomalous pulmonary venous connection in a large number of patientsll-1s The detection in our laboratory of these various anomalies in 12 adult patients (6 described in this paper) within the last 14 years suggests that the condition is more common than has been previously believed.14 Although partial anomalous pulmonary venous connection constitutes a distinct anatomic entity, its clinical diagnosis may be difficult.ls The plain roentgenogram of the chest may be diagnostic, especially when the scimitar sign is visualized (Cases 5 and 6), whereas the electrocardiogram is not helpful in diagnosis. For diagnosis and precise localization of the lesion, reliance has to be placed on cardiac catheterization techniques, which include manipulation of the catheter into the anomalous vessels, oximetric studies, angiography and indicator dye-dilution techniques. Coexistence with mitral valve disease: The association of rheumatic mitral valve disease and partial anomalous pulmonary venous connection is being reported with increasing frequency.7J6J7 It has been estimated that approximately 1 of 350 subjectsI has anomalous pulmonary venous connections. The association of these 2 conditions was not suspected before cardiac catheterization in Case 2. However, a continuous murmur was heard in the left supraclavicular region and first 2 left interspaces in a similar case reported by Halpern et a1.17 This continuous murmur may prove to be a useful physical sign and should be sought for in patients with mitral valve disease. The communication between the persistent left superior vena cava and left superior pulmonary vein seen in our Case 2 does not represent a true partial anomalous pulmonary venous connection as the left superior pulmonary vein connected normally with the left atrium. However, it does demonstrate how an acquired mitral valve lesion with consequent left atria1 hypertension may cause reversal of blood flow through a seemingly benign congenital communication, thus producing a left to right shunt. Coexistence with atria1 septal defect: Since 15 to 20 percent of all patients with an atria1 septal defect are said to have associated partial anomalous pulmonary venous connection,lg optimal preoperative planning requires that every effort be made to detect the coexistence of these lesions. Both of our patients with partial anomalous pulmonary venous connection and atria1 septal defect (Cases 3 and 4) had clinical, electrocardiographic and radiologic features of an atria1 septal defect. No clue to the associated anomalous pulmonary venous connections was found before cardiac catheterization. Since it may not always be possible to manipulate the catheter into an anomalous pulmonary vein and because entry into the pulmonary vein may occur after the catheter has crossed the interatrial septum and entered a normally connected pulmonary vein, indicator-dilution curves are required to establish the pres-
FIGURE 7. Case 6. Scimitar sign. The catheter tip is seen within the large anomalous pulmonary vein adjacent to the right heart border, which has been opacified with contrast material. The right heart catheter was observed to enter the anomalous vessel below the diaphragm from the inferior vena cava close to its connection with the right atrium.
ence of partial anomalous pulmonary venous connection in patients with atria1 septal defect. Dye curves are inscribed after injection of dye into the right atrium and venae cavae with systemic arterial sampling. In ostium secundum defects a right to left shunt (if present) is usually greater after dye injection into the inferior than into the superior vena cava; right to left shunt is often absent from the latter vessel. The finding of greater right to left shunt after superior than after inferior vena caval injection (Fig. 4) is strong evidence for a sinus venosus atria1 septal defect with partial anomalous pulmonary venous connection of the right upper and middle pulmonary lobes. In Case 4, the diagnosis of sinus venosus atria1 septal defect was established by cardiac catheterization. However, it was not possible by these methods to determine whether only part or all of the right lung drained anomalously. The question was resolved by differential bronchospirometry. This technique demonstrated that blood draining the right lung in this patient did not directly reach the periphery, but reached the systemic arterial blood only after circulation through the left lung. These data were confirmed at operation. The scimitar sign: Although partial anomalous pulmonary venous connection of the right lung into the superior vena cava or right atrium may often be associated with a patent interatrial septum, an atria1 septal defect is rarely seen when right lung veins drain into the inferior vena cava.12 The diagnosis of partial anomalous pulmonary venous connection of the right lung into the inferior vena cava in Cases 5 and 6 was made by the characteristic “scimitar sign”
April 1973
The American
Journal of CARDIOLOGY
Volume 31
517
PARTIAL
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
seen on the chest roentgenogram, which was first described by Dotter et a1.4 The abnormal vein receives tributaries from a variable number of right lung lobes. The dye curves obtained in Case 5 after right pulmonary arterial injection and systemic arterial sampling showed a small first peak, followed by a large second peak of the left to right shunt, suggesting that a large part, but not all, of the right lung drained anomalously in this patient. The scimitar sign may occur alone (Case 6) or may be associated tiith a variety of congenital bronchovascular and cardiac anomalies (Case 5).12 The various pathologic changes in the right lung include a diminution in size of the right lung, commonly due to absence of the right middle lobe. Bronchial abnormalities include abnormal distribution, accessory
ET AL.
bronchi and cystic bronchial changes. Other aberrations include a hypoplastic right pulmonary artery, partial arterial supply from the systemic circulation to the pulmonary tree, diaphragmatic defects and congenital cardiac and extrathoracic lesions. A pulmonary angiogram is perhaps the most useful diagnostic procedure in this condition since it outlines the size and distribution of the right pulmonary artery, and displays the anomalous vein along with its tributaries. The aortic phase occasionally helps delineate anomalous systemic arterial supply of the lower right pulmonary lobe from the descending thoracic aorta. Acknowledgment We thank Mrs. Thelma Gottlieb for valuable in the preparation of this manuscript.
assistance
References 1. Swan HJC, Burchell HB, Wood EH: Differential diagnosis at cardiac catheterization of anomalous pulmonary venous drainage related to atrial septal defects or abnormal venous connections. Proc Staff Meet Mayo Clinic 28:452-462, 1953 2. Edwards JE: Pathologic and developmental considerations in anomalous pulmonary venous connection. Proc Staff Meet Mayo Clinic 28:441-452, 1953 3. Neil1 CA: Development of pulmonary veins: with reference to the embryology of anomalies of- pulmonary venous return. Pediatrics 18:880-887, 1956 4. Dotter CT, Hardisty NM, Steinberg I: Anomalous right pulmonary vein entering the inferior vena cava: two cases diagnosed during life by angiocardiography and cardiac catheterization. Amer J bled Sci 218:31-36, 1949 5. Grishman, A, Poppel MH, Simpson RS, et al: The roentgenographic and angiocardiographic aspects of (1) aberrant insertion of pulmonary veins associated with interatrial septal defect and (2) congenital arteriovenous aneurysm of the lung. Amer J Roentgen 62:500-508,1949 6. Samet P, Bernstein WH, Kramer C, et al: Indicator-dilution curves in congenital cardiac lesions involving the ventricles and great vessels. Amer J Cardiol 10:83-92, 1962 7. Maramba LC, Narula OS, Hildner FJ, et al: Mitral stenosis in a patient with a congenital communication between the systemic and pulmonary venous beds. Chest 57:336-339, 1970 8. Swan HJC, Hetzel PS, Wood EH: Quantitative estimation by indicator-dilution technics of the contribution of blood from each lung to the left-to-right shunt in atrial septal defect. Circulation 14:212-220, 1956 9. Semet P, Fierer EM, Bernstein WH: Anomalous pulmonary venous drainage. Diagnostic value of bronchospirometry. Amer J Med 25: 654-658, 1958 10. Neill, CA, Ferencz C, Sebiston DC, et al: The familial oc-
518
April 1973
The American
Journal of CARDIOLOGY
currence of hypoplastic right lung with systemic arterial supply and venous drainage. “Scimitar syndrome”. Bull Johns Hopkins Hosp 107:1-15, 1960 11. Frye RL, Krebs M, Rahimtoola SH, Ongley PA, et al: Partial anomalous pulmonary venous connection without atrial septal defect. Amer J Cardiol 22:242-250, 1968 12. Kiely 8, Filler J, Stone S, et al: Syndrome of anomalous venous drainage of the right lung to the inferior vena cava: review of 67 reported cases and three new cases in chilz dren. Amer J Cardiol20: 102-l 16, 1967 13. Snellen HA, van lngen HC, Hoefsmit E CH M: Patterns of anomalous pulmonary venous drainage. Circulation 38:4563,1968 14. Brody H: Drainage of pulmonary veins into right side of heart. Arch Path (Chicago) 33:221-240, 1942 15. Knutson JRB, Taylor BE, Pruitt RD, et al: Anomalous pulmonary venous drainage diagnosed by catheterization of the right side of the heart: report of 3 cases. Proc Staff Meet Mayo Clin 25:52-59, 1950 16. Adler LN, Berger RL, Starkey GWB, et al: Anomalous pulmonary venous drainage associated with mitral stenosis. Report of a case successfully repaired. New Eng J Med 270:166-172, 1964 17. Halpern BL, Murray GC, Conti CR, et al: Continuous murmur due to the combination of rheumatic mitral stenosis and a rare type of anomalous pulmonary venous drainage. Circulation 42:165-l 70, 1970 18. Keith JD, Rowe RD, Vlad P: Heart Disease in Infancy and Childhood, second edition. New York, Macmillan, 1967, p 499-509 19. Kirklin JW, Ellis RH, Ward EH: Treatment of anomalous venous connections in association with internal communications. Surgery 39:389-398, 1956
Volume 31
Partial Ammalaus PulmonaryVenous Connection and Drainage EUGENE MASCARENHAS. ROGER P. JAVIER, MD PHILIP
SAMET,
MD,
MD
FACC
Miami. Florida
The clinical, diagnostic and pathophysiologic features of types of partial anomalous pulmonary venous connection age seen in 6 adult patients are presented. This distinct entity is perhaps more commonly prevalent than has been believed. It may be associated with other cardiac and anomalies and also with acquired rheumatic valve disease.
5 different and drainanatomic previously pulmonary
A pulmonary vein is said to be anomalously connected when it fails to communicate normally with the left atrium and instead connects to the right side of the heart, that is, right atrium, coronary sinus or the venae cavae or their tributaries. Partial anomalous pulmonary venous connection is said to be present when some, but not all, pulmonary veins are aberrantly connected. The term “connection” is used to define an anatomic relation and “drainage” to indicate its physiologic effect.’ The embryologic basis2*3 for these pulmonary venous aberrations is well recognized. However, this anomaly remained a pathologic curiosity until 1949 when Dotter et a1.4 and Irishman the clinical diagnosis by roentgenography, cardiac et al.” reported catheterization and angiography. Advances in surgical techniques have now made these anomalies at least potentially correctable. Opt imal preoperative planning requires accurate determination of the sites of anomalous connection, evaluation of the magnitude of shunt flow and presence of associated cardiac lesions. The purpose of this paper is to present the clinical and diagnostic features of 5 different types of partial anomalous pulmonary venous connection
seen
in 6 adult
patients.
Methods All patients were evaluated hy a clinical history, physical examination, electrocardiogramS radiography and fluoroscopy. Right heart catheterization and attempts to enter the anomalous pulmonary veins and to cross an atrial septal defect were made in each patient. I,eft heart transseptal catheterization was carried out in :! patients. Blood oxygen determinations were obtained in 4 cases. Standard angiographic methods were adopted to visualize aberrant vessels and their connections. Differential bronchospirometry was performed in 1 case. I,eft to right shunt flow was determined by the nitrous oxide method in 3 patients. lndocyanine green dye-dilution curves were recorded” in 4 patients and ascorhate indicator dilution curves in 1 patient.
Results From the Division of Cardiology, Department of Internal Medicine, Mount Sinai Hospital of Greater Miami and the University of Miami Medical School. Miami. Fla. Manuscriot received May 9. 1972; revised manuscript received Au&st 15. 1972. accepted Sebtemhm37 _“.
_.
,
IQ73 .-SC.
Address for reprints: Eugene Mascarenhas. MD, Mount Sinai Hospital. 4300 Alton Rd.. Miami Beach, Fla. 33140.
512
April 1973
The clinical, patients presented
with
electrocardiographic partial
in Table
anomalous
I. The
and
radiologic features of the 6 venous connection are findings are shown in Table
pulmonary
hemodynamic
II. Case I. Anomalous drainage of the left superior pulmonary vein (LSPV) into the left innominate vein: A 31 year old housewife was referred to us in March 19,X3 for evaluation of a heart murmur that was first detected at age 1:). She had had no cardiovascular symptoms even during 3
The American Journal of CARDIOLOGY
Volume 31
PARTIAL
TABLE
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
I
Clinical,
Electrocardiographic
and Radiologic
in 6 Patients with Partial Anomalous
Features
Pulmonary
Venous Connection
Physical Signs
Case
Age
no.
Race/Sex
1
N/P
31
2
C/P
54
3 4
C/F
5
C/F C/M
41 la 30
6
C/M
35
C = Caucasian;
Symptoms
(yr)
Thrill
Cardiac neurosis, heart murmur Dyspnea Fatigue Effort dyspnea Recurrent bronchitis Asymptomatic
N = negro;
IRBBB
+
Chest Rosntgenogram
Accentuated P2
Grade
Location
-
316
ULSB
Normal
-
+
316
IRBBB
+
+
-
+ -
316
Mitral area ULSB ULSB -
IRBBB IRBBB ST-T wave
+ + -
+ + -
+
ULSB
changes IRBBB
Systolic Murmur
416
216
= incomplete
right
bundle
branch
block; ULSB
ECG
= upper
left sternal
Heart Size
Increased Pulmonary Vascularity
Anomalous Vein
+ border.
presence of a left to right shunt. Dye curves were then obtained after selective injection of dye into the right and left pulmonary arteries with simultaneous sampling from the femoral artery and right atrium (Fig. 1). The curves after right pulmonary arterial injection were normal; those after left pulmonary arterial injection revealed a left to right shunt and an early right atria1 appearance time. Constant left pulmonary arterial injection with serial sampling from the right heart chambers and at different sites in the superior vena cava localized the anomalous draining site to the left innominate vein (Fig. 2). Fifty cubic centimeters of contrast material injected into the left pulmonary artery subsequently outlined an anomalous left superior pulmonary vein, 2 cm in diameter, traversing the medial left upper lung field, overlapping the aorta and joining the left innominate vein (Fig. 3). The degree of shunt flow was calculated to be approximately 28 percent by the use of the nitrous oxide method. Case 2. Communication of left superior pulmonary vein and innominate vein by way of a persistent left superior vena cava in a patient with rheumatic mitral
uncomplicated pregnancies. For the past 5 years she showed marked concern over her heart murmur. Examination of the cardiovascular system was essentially normal, except for a grade 3/6 ejection systolic murmur along the left sternal border (Table I). The electrochest cardiac fluoroscopic examination, cardiogram, roentgenogram and right heart pressures were all found to be normal (Table II). Blood oxygen determinations during right heart catheterization revealed that the oxygen content of blood in the inferior vena cava (13.2 vol percent) was less than the oxygen content in the right atrium (15.5 vol percent) and superior vena cava (15.3 vol percent). The findings of this reverse relation in oxygen content alerted us to the presence of a left to right shunt. Since blood of high oxygen content was found in the superior vena cava with no significant step-up in the right atrium, it was considered probable that the interatrial septum was intact and that an anomalous pulmonary vein drained into the superior vena cava or its tributaries. Injection of indocyanine green dye into the main pulmonary artery and sampling in the femoral artery confirmed the
TABLE
ET AL.
II
Hemodynamic
Data and Oxygen Studies in 6 Patients with Partial Anomalous
Case
IVC or SVC
no.
02
RA
02
P
-__ OaC
RV
PA
P
02
Pulmonary
Pulmonary
LA
P
Venous Connections
o*c
P
Vein 02
Systemic Artery 02
P
Shunt
Asso-
flow No
ciated Cardiac Lesions
Me;hod
13.2*; 15.3 -
15.5 -
-2 5
15.0 -
20/O 37/Z
15.1 -
1718 36119
-
17
-
17.5 -
14cria5 124175
28% -
-
-
-
la.9
130185
45%
MS Ml ASD
13.4*; 15.2
16.4
1
16.9
24/Z
16.9
22113
12.3 -
16.3 -
4 1
16.7 -
2214 2212
17.4 -
1817 18/6
18.0 -
-
la.2 -
la.2 -
121170 110165
-
ASD -
19.2*; 15.8
17.8
2
17.8
2315
la.3
20/10
-
-
20.1
20.5
110166
36%
-
* Inferior vena cava. ASD = atrial septal defect; IVC = inferior vena cava; LA = left atrium; Ml = mitral insufficiency; MS = mitral stenosis; O2 = oxygen content (%); P = pressure (mm Hg); PA = pulmonary artery; RA = right atrium; RV = right ventricle; SVC = superior vena cava.
April 1973
The American Journal of CARDIOLOGY
Volume 31
513
PARTIAL
RPA
ANOMALOUS
to FA
and
PULMONARY
RA
VENOUS
CONNECTION-MASCARENHAS
LPA
to FA
and
ET AL.
RA
FIGURE 1. Case 1. Anomalous pulmonary venous connection and drainage of the left upper lobe pulmonary vein to the left innominate vein with an intact interatrial septum. Localization of the site of the left to right shunt by selective right (RPA) and left (LPA) pulmonary arterial injection. Simultaneous samplings from the femoral artery (FA) and right atrium (RA) reveals a left to right shunt after injection into the left but not the right pulmonary artery, The appearance times are corrected for the dead space volumes of the respective sampling systems.
5.8:.
L PA
TO SVC
2”ABOVE
R A
L PA
TO S VC
4”ABOVE
R A
Mid - point In /action
miwh
FIGURE 3. Case 1. Angiographic demonstration of anomalous left superior pulmonary venous (LSPV) drainage into the left innominate vein (IV).
514
April 1973
The American
Journal of CARDIOLOGY
FIGURE 2. Case 1. The left to right shunt after left pulmonary arterial injection is evident in the superior vena cava after sampling 2 inches above the right atrium but not 4 inches above this chamber.
m(nat IIi I
valve disease7: A 54 year old white married woman with rheumatic valvular heart disease was referred to us for hemodynamic evaluation in March 1965 because of progressively increasing dyspnea over the past 10 years (Tables I and II). The pertinent hemodynamic abnormalities were moderate mitral valve stenosis (left atrial-left ventricular mean diastolic gradient 8 mm Hg), mild mitral and tricuspid valvular insufficiency and mild pulmonary hypertension. At transseptal left heart catheterization injection of indocyanine green dye into the left atrium with right heart sampling from the pulmonary artery, right ventricle and right atrium revealed an early appearance time in each chamber, suggesting a left to right shunt. An early appearance time was also observed by sampling the superior vena cava, but not in the high right jugular system. Left atria1 and left ventricular cineangiograms showed no interatrial or interventricular septal defects. The site of the left to right shunt was not clearly established at the time of this study. During open heart surgery moderately severe mitral valve stenosis was noted. The dependent portion of the
Volume 31
PARTIAL
S.V.C.
FIGURE injection
to
L.B.A.
(G-6-4WIW”tR.A.)
ANOMALOUS
PULMONARY
Low R.A. to L.B.A.
(G-6-42)
VENOUS
CONNECTION-MASCARENHAS
1.v.c. t0
L.B.A.
(~-6-42)
ET AL.
(~“AR.A.)
4. Case 3. Sinus venosus type of atrial septal defect. Systemic arterial sampling after inferior vena caval (C) and right atrial (B) reveals a small right to left shunt. However, the shunt is best noted after injection into the superior vena cava (A).
left atrium showed a brisk flow of unoxygenated blood in the area of the left superior pulmonary vein. Insufflation of the lung failed to change the color of the blood. The heart and mediastinum were rotated to the right, and a large vein (left superior vena cava) on the left side was seen to communicate with the normally placed left superior pulmonary vein. After the left superior vena cava was ligated, the flow of unoxygenated blood ceased. A mitral valvuloplasty was performed, and the patient was discharged after an uneventful hospital course. On restudy 6 months postoperatively the left to right shunt was no longer demonstrable. Case 3. Drainage of right pulmonary veins into the right atrium with an atria1 septal defect (sinus venosus type): A cardiac murmur was first detected in a 41 year
old white woman at age 4 years. For the past three years she had been experiencing paroxysmal attacks of atria1 fibrillation. The salient features on examination in 1960 were right ventricular and pulmonary arterial pulsations. The second heart sound was widely split, varied little with respiration, and the pulmonic component was accentuated. A grade 3/6 ejection systolic murmur was best heard over the pulmonic area. Fluoroscopic examination of the chest showed an enlarged heart (right atrium and right ventricle) and a very prominent pulmonary arterial segment with increased pulmonary vascular markings but no hilar dance. The electrocardiogram showed incomplete right bundle branch block (QRS duration 0.11 second). Intracardiac right heart pressures were normal. (Table II). Blood oxygen studies revealed a significant oxygen step-up at the atria1 level. The catheter tip could not be passed either into an anomalous pulmonary vein or into the left atrium by way of an atria1 septal defect. Indocyanine curves obtained after selective injections into the right and left pulmonary artery with systemic arterial sampling showed a greater magnitude of left to right shunt flow after right rather than left pulmonary arterial injection. Such preferential flow is not pathognomonic of an atria1 septal defect with partial anomalous pulmonary venous return from the right lung, and since it can also occur in an ostium secundum atria1 septal defect with normal pulmonary venous connections.8 Indocyanine green dye curves after inferior and superior venae caval injection with systemic arterial sampling were carried out.
A larger right to left than from the inferior This finding favors a defect with anomalous the right lung rather atria1 septal defect.
shunt from the superior vena cava vena cava was noted. (Figure 4.) sinus venosus type of atria1 septal pulmonary venous connection from than an ostium secundum type of
Case 4. Drainage of right pulmonary veins into the right atrium with an atria1 septal defect (sinus venosus type): An 18 year old white girl9 had noted mild, nonprogressive exertional dyspnea for many years and was first seen by us in 1957. The clinical, fluoroscopic and electrocardiographic features (Table I) suggested a diagnosis of atria1 septal defect or anomalous pulmonary venous drainage, or both. On cardiac catheterization (Table II), the catheter tip was easily manipulated from the caudal superior vena cava and right atrium into the right pulmonary veins establishing the diagnosis of anomalous connection of right pulmonary veins. However, the catheter tip could not be manipulated through an atria1 septal defect, and the presence of this additional lesion could not be ruled out. To determine whether the entire right pulmonary venous drainage was into the right atrium, bronchospirometry was performed. A Carlens catheter9 was passed into the trachea so as to separate the ventilatory pathways of the right and left lungs. Different gas mixtures were then applied to the 2 lungs and serial measurements of arterial blood oxygen saturation were made. On room air the arterial oxygen saturation was 94 percent. When pure nitrogen (oxygen content 0.16 percent) was given to the right lung (the site of the anomalous pulmonary venous connection), and 24 percent oxygen to the left lung, the arterial oxygen saturation remained unchanged after 10 minutes. When the gas mixtures were reversed, arterial saturation decreased rapidly to 73 percent within 3 minutes. These findings together with the catheterization data, led to the diagnosis of virtually total unilateral (right-sided) anomalous venous connection and drainage. A second cardiac catheterization study was performed a year later. On this occasion the catheter tip was passed through an atria1 septal defect into the left atrium and left ventricle. At operation in 1961, the entire venous drainage of the right lung was noted to return to the right side of the heart, the superior pulmonary vein emptying into the
April 1973
The American Journal of CARDIOLOGY
Volume 31
515
PARTfAL
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
ET AL.
calized. Auscultation of the heart was normal. A chest X-ray film showed the typical radiologic features of the “scimitar syndrome,“10 that is, (1) a scimitar-shaped density parallel to the right paracardiac border; (2) decreased right hemithorax; (3) shift of the cardiac shadow to the right; and (4) hypoplastic right pulmonary artery (Fig. 5). Cardiac catheterization revealed normal right heart pressures. Ascorbic acid dye curves with injection into each pulmonary artery with femoral arterial sampling detected a large left to right shunt after right pulmonary arterial injection. Injection of indocyanine green dye into the right pulmonary artery revealed an early right atria1 appearance time; when the tip of sampling catheter was positioned 3 inches below the diaphragm, a normally delayed appearance time was noted (Fig. 6). Pulmonary angiocardiograms demonstrated that the right pulmonary arterial tree was hypoplastic. The veins from the right lung joined to form a single large vessel adjacent to the right cardiac border and drained into the inferior vena cava 1 l/2 inches below the diaphragm. FIGURE 5. Case 5. “Scimitar syndrome.” The chest roentgenogram illustrates displacement of the cardiac silhouette to the right. A multibranching scimitar-shaped shadow is seen parallel to the right heart border and courses toward the diaphragm.
lower superior vena cava and the right inferior pulmonary vein into the upper right atrium. The lesions were appropriately corrected, and a 2 year follow-up evaluation showed no left to right shunt. Case
rior
5. Drainage
vena
cavae
of right pulmonary (scimitar syndrome):
veins into infeA 30 year old
white man complained of recurrent asthmatic bronchitis since age 10. Physical examination in 1965 revealed a mildly tachypneic patient. Diffuse rhonchi were heard over both lung fields. The right hemithorax was less expansile than the left. The cardiac impulse could not be lo-
I RPA
toFA
Case 6. Scimitar sign: A 35 year old asymptomatic man was referred to us in 1958 because a routine chest X-ray examination disclosed a scimitar-shaped opacity, parallel to the right heart border. Physical examination was essentially normal except for a Grade 3/6 ejection systolic murmur along the left sternal border. On cardiac catheterization oxygen content of the inferior vena caval blood (19.2 vol percent) was greater than that of blood samples obtained from the superior vena cava (15.8 vol percent) and right atrium (17.8 vol percent). The catheter tip was manipulated from the right atrium into the inferior vena cava and out into the right lower lung fields (Fig. 7). The oxygen content (20 vol percent) in this pulmonary vein matched the arterial oxygen content. The atria1 septum was ‘probed and felt to be intact. Shunt flow was calculated to be 36 percent of the total pulmonary blood flow.
andRA
, , RPA
toFA.andIVC
Mid-point Injection
7 set 1A T: 6.3-3.4 set
: I I I
FIGURE 6. Case 5. After right pulmonary arterial injection, the inferior vena cava 4 inches below the diaphragm.
516
April 1973
The American Journal of CARDIOLOGY
an early right atrial appearance
Volume 31
time is evident:
this finding
is not noted in
PARTIAL ANOMALOUS PULMONARY
VENOUS O~NNEOTI~N-MASCARENHAS
ET AL.
Discussion The development of new diagnostic techniques has increased the detection of partial anomalous pulmonary venous connection in a large number of patientsll-1s The detection in our laboratory of these various anomalies in 12 adult patients (6 described in this paper) within the last 14 years suggests that the condition is more common than has been previously believed.14 Although partial anomalous pulmonary venous connection constitutes a distinct anatomic entity, its clinical diagnosis may be difficult.ls The plain roentgenogram of the chest may be diagnostic, especially when the scimitar sign is visualized (Cases 5 and 6), whereas the electrocardiogram is not helpful in diagnosis. For diagnosis and precise localization of the lesion, reliance has to be placed on cardiac catheterization techniques, which include manipulation of the catheter into the anomalous vessels, oximetric studies, angiography and indicator dye-dilution techniques. Coexistence with mitral valve disease: The association of rheumatic mitral valve disease and partial anomalous pulmonary venous connection is being reported with increasing frequency.7J6J7 It has been estimated that approximately 1 of 350 subjectsI has anomalous pulmonary venous connections. The association of these 2 conditions was not suspected before cardiac catheterization in Case 2. However, a continuous murmur was heard in the left supraclavicular region and first 2 left interspaces in a similar case reported by Halpern et a1.17 This continuous murmur may prove to be a useful physical sign and should be sought for in patients with mitral valve disease. The communication between the persistent left superior vena cava and left superior pulmonary vein seen in our Case 2 does not represent a true partial anomalous pulmonary venous connection as the left superior pulmonary vein connected normally with the left atrium. However, it does demonstrate how an acquired mitral valve lesion with consequent left atria1 hypertension may cause reversal of blood flow through a seemingly benign congenital communication, thus producing a left to right shunt. Coexistence with atria1 septal defect: Since 15 to 20 percent of all patients with an atria1 septal defect are said to have associated partial anomalous pulmonary venous connection,lg optimal preoperative planning requires that every effort be made to detect the coexistence of these lesions. Both of our patients with partial anomalous pulmonary venous connection and atria1 septal defect (Cases 3 and 4) had clinical, electrocardiographic and radiologic features of an atria1 septal defect. No clue to the associated anomalous pulmonary venous connections was found before cardiac catheterization. Since it may not always be possible to manipulate the catheter into an anomalous pulmonary vein and because entry into the pulmonary vein may occur after the catheter has crossed the interatrial septum and entered a normally connected pulmonary vein, indicator-dilution curves are required to establish the pres-
FIGURE 7. Case 6. Scimitar sign. The catheter tip is seen within the large anomalous pulmonary vein adjacent to the right heart border, which has been opacified with contrast material. The right heart catheter was observed to enter the anomalous vessel below the diaphragm from the inferior vena cava close to its connection with the right atrium.
ence of partial anomalous pulmonary venous connection in patients with atria1 septal defect. Dye curves are inscribed after injection of dye into the right atrium and venae cavae with systemic arterial sampling. In ostium secundum defects a right to left shunt (if present) is usually greater after dye injection into the inferior than into the superior vena cava; right to left shunt is often absent from the latter vessel. The finding of greater right to left shunt after superior than after inferior vena caval injection (Fig. 4) is strong evidence for a sinus venosus atria1 septal defect with partial anomalous pulmonary venous connection of the right upper and middle pulmonary lobes. In Case 4, the diagnosis of sinus venosus atria1 septal defect was established by cardiac catheterization. However, it was not possible by these methods to determine whether only part or all of the right lung drained anomalously. The question was resolved by differential bronchospirometry. This technique demonstrated that blood draining the right lung in this patient did not directly reach the periphery, but reached the systemic arterial blood only after circulation through the left lung. These data were confirmed at operation. The scimitar sign: Although partial anomalous pulmonary venous connection of the right lung into the superior vena cava or right atrium may often be associated with a patent interatrial septum, an atria1 septal defect is rarely seen when right lung veins drain into the inferior vena cava.12 The diagnosis of partial anomalous pulmonary venous connection of the right lung into the inferior vena cava in Cases 5 and 6 was made by the characteristic “scimitar sign”
April 1973
The American
Journal of CARDIOLOGY
Volume 31
517
PARTIAL
ANOMALOUS
PULMONARY
VENOUS
CONNECTION-MASCARENHAS
seen on the chest roentgenogram, which was first described by Dotter et a1.4 The abnormal vein receives tributaries from a variable number of right lung lobes. The dye curves obtained in Case 5 after right pulmonary arterial injection and systemic arterial sampling showed a small first peak, followed by a large second peak of the left to right shunt, suggesting that a large part, but not all, of the right lung drained anomalously in this patient. The scimitar sign may occur alone (Case 6) or may be associated tiith a variety of congenital bronchovascular and cardiac anomalies (Case 5).12 The various pathologic changes in the right lung include a diminution in size of the right lung, commonly due to absence of the right middle lobe. Bronchial abnormalities include abnormal distribution, accessory
ET AL.
bronchi and cystic bronchial changes. Other aberrations include a hypoplastic right pulmonary artery, partial arterial supply from the systemic circulation to the pulmonary tree, diaphragmatic defects and congenital cardiac and extrathoracic lesions. A pulmonary angiogram is perhaps the most useful diagnostic procedure in this condition since it outlines the size and distribution of the right pulmonary artery, and displays the anomalous vein along with its tributaries. The aortic phase occasionally helps delineate anomalous systemic arterial supply of the lower right pulmonary lobe from the descending thoracic aorta. Acknowledgment We thank Mrs. Thelma Gottlieb for valuable in the preparation of this manuscript.
assistance
References 1. Swan HJC, Burchell HB, Wood EH: Differential diagnosis at cardiac catheterization of anomalous pulmonary venous drainage related to atrial septal defects or abnormal venous connections. Proc Staff Meet Mayo Clinic 28:452-462, 1953 2. Edwards JE: Pathologic and developmental considerations in anomalous pulmonary venous connection. Proc Staff Meet Mayo Clinic 28:441-452, 1953 3. Neil1 CA: Development of pulmonary veins: with reference to the embryology of anomalies of- pulmonary venous return. Pediatrics 18:880-887, 1956 4. Dotter CT, Hardisty NM, Steinberg I: Anomalous right pulmonary vein entering the inferior vena cava: two cases diagnosed during life by angiocardiography and cardiac catheterization. Amer J bled Sci 218:31-36, 1949 5. Grishman, A, Poppel MH, Simpson RS, et al: The roentgenographic and angiocardiographic aspects of (1) aberrant insertion of pulmonary veins associated with interatrial septal defect and (2) congenital arteriovenous aneurysm of the lung. Amer J Roentgen 62:500-508,1949 6. Samet P, Bernstein WH, Kramer C, et al: Indicator-dilution curves in congenital cardiac lesions involving the ventricles and great vessels. Amer J Cardiol 10:83-92, 1962 7. Maramba LC, Narula OS, Hildner FJ, et al: Mitral stenosis in a patient with a congenital communication between the systemic and pulmonary venous beds. Chest 57:336-339, 1970 8. Swan HJC, Hetzel PS, Wood EH: Quantitative estimation by indicator-dilution technics of the contribution of blood from each lung to the left-to-right shunt in atrial septal defect. Circulation 14:212-220, 1956 9. Semet P, Fierer EM, Bernstein WH: Anomalous pulmonary venous drainage. Diagnostic value of bronchospirometry. Amer J Med 25: 654-658, 1958 10. Neill, CA, Ferencz C, Sebiston DC, et al: The familial oc-
518
April 1973
The American
Journal of CARDIOLOGY
currence of hypoplastic right lung with systemic arterial supply and venous drainage. “Scimitar syndrome”. Bull Johns Hopkins Hosp 107:1-15, 1960 11. Frye RL, Krebs M, Rahimtoola SH, Ongley PA, et al: Partial anomalous pulmonary venous connection without atrial septal defect. Amer J Cardiol 22:242-250, 1968 12. Kiely 8, Filler J, Stone S, et al: Syndrome of anomalous venous drainage of the right lung to the inferior vena cava: review of 67 reported cases and three new cases in chilz dren. Amer J Cardiol20: 102-l 16, 1967 13. Snellen HA, van lngen HC, Hoefsmit E CH M: Patterns of anomalous pulmonary venous drainage. Circulation 38:4563,1968 14. Brody H: Drainage of pulmonary veins into right side of heart. Arch Path (Chicago) 33:221-240, 1942 15. Knutson JRB, Taylor BE, Pruitt RD, et al: Anomalous pulmonary venous drainage diagnosed by catheterization of the right side of the heart: report of 3 cases. Proc Staff Meet Mayo Clin 25:52-59, 1950 16. Adler LN, Berger RL, Starkey GWB, et al: Anomalous pulmonary venous drainage associated with mitral stenosis. Report of a case successfully repaired. New Eng J Med 270:166-172, 1964 17. Halpern BL, Murray GC, Conti CR, et al: Continuous murmur due to the combination of rheumatic mitral stenosis and a rare type of anomalous pulmonary venous drainage. Circulation 42:165-l 70, 1970 18. Keith JD, Rowe RD, Vlad P: Heart Disease in Infancy and Childhood, second edition. New York, Macmillan, 1967, p 499-509 19. Kirklin JW, Ellis RH, Ward EH: Treatment of anomalous venous connections in association with internal communications. Surgery 39:389-398, 1956
Volume 31