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Venoarterial shunting from inferior vena cava to left atrium in atrial septal defects with normal right heart pressures
Venoarterial Cava
Shunting
to Left Atrium with
Normal
from
Inferior
in Atria1
Right
Heart
Vena
Septal
Defects
Pressures
Report of Two Cases* WILLIAM KALPH
K.
L. WINTERS, JR., M.D., F.A.c.c., TYSON,
FELIX CORTES, M.D., MICHAEL MCDONOUGH,
Philadelphia,
Pennsylvania
but disclosed, in addition, arterial unsaturation resulting from an interatrial communication traversed by the cardiac catheter. The boy had been well until
T
HE majority of uncomplicated atria1 septal defects manifest left to right shunting. However, right to left intracardiac shunting, when it occurs in atria1 septal defect, need not be associated with pulmonary hypertension or pulmonary valvular stenosis. Occasionally a peculiar developmental or anatomic derangement of the positioning of the atria1 opening of the inferior or superior cava may permit drainage of a part of all of the caval flow to the left atrium producing cyanosis of varying degree with or without respiratory embarrassment. Two such cases of drainage of a portion of the inferior cava flow into the left atrium are preOne was unrecognized at the time of sented. successful surgical correction of a congenital pulmonary valvular stenosis. An atria1 septal defect came to be suspected in the second patient with the appearance of cyanosis, dyspnea and evidence for intracardiac venoarterial shunting after a pneurnonectomy for bronchogenic carcinoma. The importance of blood gas tension studies and selective dye-dilution or cineangiographic technics to study inferior and superior cavai flow in confirming this diagnosis is enlphasized.
December 5, when he complained of severe fatigue and dyspnea. His mother then noted cyanosis. A heart defect had been known to exist since age 5, but he had been otherwise asymptomatic. At the time of operation, a grade 3/6 harsh, ejection, basal systolic murmur was present with diminished Pp and a left parasternal systolic lift. An electrocardiogram showed right atria1 enlargement, marked right axis deviation and right ventricular hypertrophy. Chest roentgenogram demonstrated right atria1 prominence, enlarged pulmonary artery segment and diminished intrapulmonary vasculature. The hemoglobin was 22.4 gm., hematocrit 75%. Following a successful closed pulmonary valvotomy, the postoperative course was uneventful. He ~elasreadmitted on April 9, 1962, for re-evaluation because of a persistent cardiac murmur and cyanosis. Since surgery there had been considerable improvement in exercise tolerance and much less dyspnea. On examination, there remained nail-bed cyanosis and clubbing of fingers and toes, a systolic thrill in the second left intercostal space with a grade 5/6 ejection systolic murmur, and a short, early diastolic, decrescendo murmur. The latter was thought to represent pulmonary valvular insufficiency commonly following closed pulmonary valvotomy. The electrocardiogram still showed right axis deviation, right ventricular hypertrophy (less than preoperatively) and incomplete right bundle branch block. On chest roentgenogram the heart size and configuration were unchanged. Right atria1 prominence and large pulmonary artery segment persisted. Hemoglobin was 20.7 gm.%. Cardiac catheterization was again performed April 12
CASE REPORTS
This 17 year old white boy underwent a closed pulmonary valvotomy at St. Christopher’s Hospital for Children in Philadelphia on Dec. 12, 1959, for pulmonary valvular stenosis. Catheterization studies (Table I) performed December 17 confirmed the presence of pulmonary valvular stenosis CASE
1.
* From the Departments of Medicine and Surgery, Temple University Medical study was supported in part by U. S. Public Health Service. Grant HE 06313. VOLUME
19, FEBRUARY
M.D.,
M.D., HOWARD BAIER, M.D., JOSE GIMENEZ, M.D. and JULIO C. DAVILA, ~hl.~., I’.A.c.c.
t 967
293
Center,
Philadelphia,
Pa.
This
Winters
294
Chsc
----12/17/57--Pressure (mm. Hg) SVC
1.
Catheterization
Chriiac
-_ 02 Content (vol.‘:;)
et al.
w--4/12/62---Pressure (mm. Hg)
Data _--_----5 0.2 Content (vol.‘:;,)
18.7
20.7 22.7 22.1 21.4
IVC RI\
H L M
1iv PA LA LV BA H = high;
16/3 (8) 230/O 12/8 8 105/8 115/76 L = low;
17.; 17.1 16.4 16.0 15.9 18.3 23.2 (78’&)
a = 15 v=7 30/o-5 22/7 19/7 115/75
02 Content (\wl.“; ) ~~~~ .____
I(l.2 v = 3 (2)
22.5 19.3 70.5
10/4 11/5 8/3(3)
19.0 19.2 20.0
20.8 21.5
26.7
/7 /J63__~_. .__.~~_
PreSsWe (mm. Ifg)
(96c/;)
120/84
25.9
(87l;;)
M = mid.
(‘Table I). The atria1 septal defect was easily entered from the right saphenous vein. Right ventricular pressure was now normal. A selective cineangiogram with injection into the left atrium outlined the atria1 septal defect. The interpretation of this finding in relation to the cyanosis is not clear from hospital records. In retrosL>ect, arterial-venous admixture at the atria1 level would adequately explain the cyanosis. He was admitted to ‘Temple University Hospital for further study of the persistent cyanosis on March 7,
1963. He had remained completely asymptomatic, requiring no medication and working regularly 40 hours a week as a sewing machine operator. On examination there was obvious nail-bed cyanosis. There remained the previously noted systolic thrill in the second left intercostal space, and systolic and diastolic murmurs along the upper left sternal border. Laboratory Studies: The electrocardiogram showed right axis deviation and right bundle branch block (Fig. 1). Chest roentgenogram (Fig. 2) disclosed an enlarged pulmonary artery segment, but \vas other-
FIG. 1. Case 1. Preoperative electrocardiogram demonstrates an incomplete right bundle branch block pattern with rightward deviation of the terminal portion of the QRS complex.
gram Mar. 8,1963,
FIG. 2.
Case 1.
Preoperative posteroonterior chest roentgeno-
shows slight prominence
of pulmonary
artery segment. THE
AMERICAN
JOURNAL
OF CARDIOLOGY
Venoarterial
Shunting
in Atria1
Septal
2 ‘I 5
Ikfects
%I iL
LRA
7 0
I
71115
I 2:
set POSTop WC to FA
SCC
FIG. 3. Case 1. Dyp-ddu&n curws. Indocyanine green (5 mg.) was injected into supcriol vena cava (SVC), low right atrium (LRA), inferior vena cave (IVC) preoperatively and inferior vena cava postoperatively. Note early appearance of dye at femoral artery salllplinq site (F.4) related most closely to injection into the inferior venn cava prcoperativcly and absent postoperatively.
wisr normal. Hemoglobin was 21.5 gm., hematocrit 637;. An arterial blood sample obtained with the patient breathing room air was 93.6yc saturated with a l)O:! of 71.5, pCO:! 44.5, and pH 7.463. After breathing 100% oxygen for 10 minutes, the saturation rose to 97.3yo, but the 1’02 rose only to 97.5, and pCO? dropped to 35. The pH remained 7.455. Ci~~liczc-cutheterization was repeated on May 9 (Table I). Dye-dilution studies (Fig. 3) performed by injecting ?J mg. Cardio-Green” into the superior vena cava, right atrium, inferior vena cava, right ventricle and left atrium I\-ith sampling at a femoral artery indicated a right to left shunt into the left atrium related predominantly to flow from the inferior vena cava through the previously diagnosed atria1 septal defect. C’ineangiograpl~~ confirmed the location and direction of the shunt. The defect was subsequently closed during cardiopulmonary bypass on May 14. Postoperative dye-dilution studies and cineangiocardiograms demonstrated an intact atrial septum (Fig. 3). At the time of disVOI.UME
19. FEBRUARY
1967
charge, the hemoglobin was 11.3 gm. and hematocrit 35yc. He has remained well without further cyanosis. Postoperative catheterization studies have not as yet been performed. CASE 2. A 52 year old mushroom groxver was first admitted to ‘l‘emple University Medical Center in June 1963, complaining of hoarseness of one year’s duration. He denied any history of dyspnca on exertion, palpitations, ankle edema, or any symptoms referable to the cardiopulmonary system. Physical examination of the heart and lungs was within normal limits. At this time, the electrocardiogram was normal and a chest roentgenogram demonstrated a normal cardiac silhouette. On bronchoscopy, a carcinoma of the right vocal cord was found for Lvhich a partial laryngectomy was performed. The postoperative course was uncomplicated, and the patient \\.a~ discharged to be followed-up as an outpatient. The second hospifal admission occurred in October 1963, when on a routine postoperative chest film a
Winters
et al.
FIG. 4. Case 2. Chest roentgenograms. A, preoperative filnl demonstrates complete obstruction of the right upper lobe bronchus with partial atalectasis. The trachea is displaced to the right. The minor fissurr is elevated. A hilar mass is seen producing a convex bulge at the hilum in contrast to the concave contour of the minor fissure. The heart and pulmonary vascular markings are normal. B, postoperative film shows marked shift of the trachea and mediastinum to the right. The left lung is hyperlucent. The heart cannot be defined.
mass was found in the right hilum (Fig. 4A). ‘The electrocardiogram remained normal, as did a chest roentgenogram for cardiac silhouette and pulmonary vascular markings. Bronchoscopy and cytologic study of the sputum indicated a carcinoma in the right upper lobe. A right pneumonectomy was performed, and at operation the tumor was found to have invaded the wall of the superior vena cava but was not obstructing flow. A portion of the superior vena cava was resected and replaced by a 7 cm. Teflon8 graft. The postoperative course was uncomplicated, and the patient was discharged two weeks after surgery. He continued to improve at home and was fully ambulatory until three months after discharge, when he began to experience some dyspnea occurring only when he changed from the recumbent to the standing position. After standing for a few minutes, the dyspnea disappeared, and he could walk without difficulty. He was thought to be in moderate congestive heart failure and was treated with digitalis but did not improve. These symptoms continued to progress until January 1964, when he was hospitalized at Temple University Hospital for a period of five weeks to determine the cause of this dyspnea. At the time, the patient was comfortable in the recumbent position, but as he attempted to stand or sit up, he would become extremely short of breath and cyanotic.
Assuming the recumbent position relieved the symptoms immediately. Onphysical examination the blood pressure was 120/80 mm. Hg and the weight 125 lb. The patient was thin and appeared chronically ill. The neck veins were not distended. Tracheal deviation toward the right was present, and the breath sounds were normal in the left chest. The left hemithorax was slightly hyper-resonant. Examination of the heart was unremarkable ; there was normal sinus rhythm at a rate of 80/min. Examination of the abdomen was within normal limits. The peripheral arterial pulses were normal and equal bilaterally. The chest roentgenogram (Fig. 4B) showed a mediastinal shift and deviation of the trachea into the right chest. Some herniation of the left lung into the right chest anteriorly was also present. The cardiovascular silhouette was normal. Chest x-ray examination and fluoroscopy were performed with the patient in both the supine and erect positions, but no abnormalities were found to explain the dyspnea. Bronchoscopy revealed a normal tracheobronchial tree. Right heart catheterization was performed to obtain a pulmonary angiogram. Right atria1 and right venA biplane venous tricular pressures were normal. angiogram was obtained with the patient first in the recumbent and then the sitting position by injection of Renovist@ into the left antecubital vein. Pictures THE
AMERICAN
JOURNAL
OF
CARDIOLOGY
Venoarterial
Shunting
r[‘ARL.E II (hsr
2. .\rterial HloodGas Determinations
,.-
-Sirrinp 2 min.
34 95 10 7 57 32 91
8 7 491 .o 5 6
7 435 x2 0
31 8 100 7.442 126 4 30 0 9x 6 92 7 419 448
~-~~ 7 min. O?
7 513 47.7 25.8 X8 25 7.520 334 24.4
7.50 49.1 27.7 no.2
29 7.469 85.0 33.8 96.4 9.1
7.452 “. 421 37.1 100
75
were taken at a rate of 2/see. for seven seconds. Right heart chambers were well visualized and were normal in size with no trace of a right to left shunt. Laboratory studies wre as follows: P uptake 3370 in 24 hours, hemoglobin 16 gm.%, hematocrit 49, \\hite blood cells 9,400 with a normal differential. Crinary excretion of 17 ketosteroids was 417 mg. for 24 hours. Urinalysis, fasting blood sugar and serum electrolytes were normal. ‘/‘he elect?-ocardiogram at this time revealed right axis deviation with questionable P wave abnormalities suggestive of pulmonary disease. There was clockwise rotation of the heart in its longitudinal axis and a tendency to low voltage. External spirometr,v demonstrated vital capacity to be 40 per cent and maximal breathing capacity 45 per cent of predicted value, with a normal timed vital capacity. rirterial blood gas studies were performed with the patient breathing room air and then 100% oxygen in the supine position and immediately after standing (‘l’able II). These studies revealed a slightly decreased arterial blood ~02 and pCO2 with normal arterial saturation in the supine position. On assumption of the erect posture, unsaturation of the arterial blood appeared which was not correctable by breathing 1007, oxygen. This was interpreted as being due to an abnormal ventilation-perfusion ratio in the remaining lung. A marked increase in minute ventilation appeared, resulting in a decrease in arterial pCO2. No effective treatment was found, and the patient was once again sent home to be followed as an outpatient. His condition continued to deteriorate at home, necessitating readmission in April 1964 for more complete evaluation. At this time the patient was cyanotic in the recumbent position and was unable to sit up in bed. The chest roentgenogram and electrocardiogram revealed no essential change. The hemoglobin had risen to 19 gm. and the hematocrit to 57%. VOLCME.
19:
FEBRUARY
1967
in Atria1 Septal
1Iefects
297
Arterial gas tension studies revealed a decrease in arterial PO:! on room air in the recumbent position. The ~02 did not rise as expected on 1005; oxygen (Table II). On assuming the upright position, p0~ decreased drastically, pCOz decreased as the minute ventilation increased. The patient became extremely dyspneic, precluding further stlrdies on lOOy;l oxygen in this position. Right heart catheterization was again performed. The intracardiac pressures remained normal on the right side. Dye-dilution curves obtained by injecting 5 mg. of Cardio-Green into the superior vena cava and right atrium revealed early systemic appearance of dye indicative of right to left shunting of blood (Fig. 5). Injection into the inferior vena cava revealed a larger amount of shunting and was highly suggestive of predominant shunting of blood from the inferior vena cava into the left atrium. Right ventricular injection of dye revealed a normal dye-dilution curve. A cineangiogram at this time confirmed these findings and a diagnosis of atria1 septal defect of the secundum type, with right to left shunting of blood from r.he inferior vena cava to left atrium, was made Closure of the atria1 sepal defect was performed on June 3, 1964, under endotracheal anesthesia, utilizing cardiopulmonary bypass. At the time of operation it was noted that the heart had rotated in such a
way that the inferior vena cava was emptying nearly directly into the atria1 septal defect. The appearance of right to left shunting was attributed to a mediastinal shift following the pneumonectomy in a patient with a small, asymptomatic atria1 secundum defect previously unrecognized. Cardiac catheterization was performed two weeks after surgical intervention. At this time, all studies were within normal limits and dye-dilution curves and rhe cineangiogram revealed no evidence of any intracardiac shunting of blood. The marked mediastinal shift to the right was still observed on chext x-ray examination. ‘The patient has remained \vell with normal hemoglobin and hematocrit. Cathererization studies one year postoperatively confirmed the complete closure of the defect. DISCUSSION
The occurrence of arterial anoxemia and polycythemia in uncomplicated atria1 septal defect is infrequent but may occur with the proper anatomic setting. In the absence of right ventricular diastolic hypertension, the left to right pressure gradient across an atria1 septal defect has been shown to persist during the entire cardiac cycle, or for all but a short period before or during atria1 systole.‘J Thus, under these conditions, to provide sufficient mixing of unsaturated with saturated blood to produce arterial unsaturation, it has been postulated that large secundum defects must be present forming a common chamber.3 Under
298
Winters
et al. SVC to FA
t
t
31 sec.
I!
0
2t2
32t
sec.
IVC to FA
t
t
t
t
0
16
22
32
t sec.
0
t
16
tt 30
34 sec.
5. Case 2. Dye-dilution ~urue. Indocyanine green (5 mg.) was injected into right ventrick (RV), superior vena cava (SVC), right atrium (RA) and inferior vena cava (IVC) preoperatively. Note early appearance of dye at femoral artery sampling site (FA) most closely related to injection into the inferior vena cava and absence of this early curve after injection into the right ventricle. FIG.
other conditions with smaller defects, it is postulated that at some period in the cardiac cycle, presumably during atria1 diastole, the shunt is reversed because of brief changes in the However, Seizer and Lewis5 pressure gradient.4 in a review in 1949 of 180 proved cases of atria1 defect were unable to find any apparent relation between the size of the defect and the They astutely postulated presence of cyanosis. the mechanism of cyanosis to be a directional flow of venous blood into the left auricle under a specific set of anatomic conditions; namely, if one of the venae cavae were so oriented as to permit a stream of blood to be directed into the left atrium during a period when a pressure gradient might be absent or reversed. This need not interfere with the major left to right shunt during the remainder of the cardiac cycle. Such streaming occurs in fetal circulation with inferior caval blood directed through the foramen ovale and superior caval blood through the tricuspid valve. It is not unreasonable to presume that this occurs after birth. Indeed, this type of flow was demonstrated angiocardiographically by Lind and Wegeliu@ in 3 infants. The atria1 septal defect in these patients was not
identifiable when the injection \vas nlade into the superior vena cava but was readily apparent when the injection was made from the inferior cava. Swan, Burchell and Wood’ reported On 9 patients with atria1 septal defects exhibiting right to left shunting by the dye-dilution technic (T-1824). In 5 of these cases the shunt was demonstrable only from the inferior vena cava and in several was not accompanied by s)-stemic Those arterial oxygen unsaturation at rest. cases of shunts demonstrable from the superior vena cava were complicated by other problems. They point to the anatomic relation of the inThe limbus ferior vena cava to the fossa ovalis. of the fossa ovalis straddles the atria1 orifice of the inferior vena cava so that a portion of the inflow from the inferior cava impinges directly on the floor of the fossa ovalis; thus blood from the inferior cava could pass equally \vcll into By the left atrium if a secundurn defect existed. selective dye-dilution studies they could demonstrate whether the defect lay in closer relation Quantito the inferior or superior vena cava. tation of the right to left shunt is possible, although Swan et al.5 rightly point to potential THE
AMERICAN
JOURNAL
OF CARDIOI.OGY
Venoarterial
Shunting
crrorx produced by the complex dilution and ltlisinq proresscs which are not readily quantitatcd. 111 (:asc 1 reported here, a successful closed prlllnonary valvotomy for congenital puhnonary stcllosis \vas accomplished but was followed by The cause for this was persistence of cyanosis. Arterial unsaturation in severe not rccoynized. pullnonary stenosis related to right to left sh(lntine through a patent foramen ovale or associated atria1 septal defect is not uncommon. B\lt persistence of this shunting in the face of normal right heart pressures following surgery, as demonstrated in Table I, should raise the qrlestion of an additional defect. Oakley and associates” recently reported on 6 cases of cono;cnital plllmonary valvular stenosis exhibiting postoperative arterial unsaturation. These patients all exhibited abnormal right ventricular function as evidenced by either systolic or diastolic hypertension. The postoperative arterial unsattlration was demonstrated to be due to right to left shunting at the atria1 level by curves and atcoomasir-blue dye-dilution tribtlted to persistence of abnormal right ventricular compliance. It is not clear, however, lvhether anatomic relation of the inferior or srlperior ca1.a to the left atrium may have played a part. They do emphasize the importance of searching for interatrial communications in patients \vith pl&nonary valvular stenosis so that the>. Inay be closed. This procedure may prevent the complication of postoperative cyanosis occllrriilg in those patients whose right ventricular ft~nction remains abnormal despite correction Case 1 reported here of the \-al\-lllar problem. did not demonstrate residual abnormal right \~rntrict&lr function in terms of pressure abnorrnalit!.. The relation of the inferior vena ca\.al flo\v to the left atrium became quite clear after dye-dillltion curves were obtained by inicctions into various portions of the right heart (Fir. .3). Cineangiography then visually confirtllcd the anatomic relation. This case reselllblcs the 3 reported by Gallaher and his grorlp” in 1963, which also exhibited normal right \.cntriclllar function as manifested by Right to left shunting nor11la1 presstIres. through an atria1 septal defect from the inferior \.cna cava was demonstrated by angiocardiograph!. in 2 patients and confirmed at operation in the third. C;U(, _7 \vas an intriguing problem of rapidly proprcssing respiratory embarrassment related to the lIpright position which followed a right VOI IXI:
1 ‘).
FEBRUARY
1767
in Atria1
Septal
I )efects
200
pnelnnonectolny for bronchogrnic carcillonla. The initial blood gas studies strongly stlggestrd right to left shtlnting of blood at either the cardiac or pulnlonary area (Table 11). But initial angiocardiographic stltdies attetllpting to locate the defect were ltnsucccssf~ll. Olrr suspicions centered initially on the superior caval graft inserted at the tlrne of operation to replace the portion of cava invaded by the carcinoma, but there was nothing in the operative technic to implicate an abnormal corn--Ï munication between this graft and the left atriuin. A subsequent survey of the inferior and superior cava flow by dye-dilution stttdies indicated right to left shunting at the atria1 level in close approximation to the inferior cava (Fig. 5.). Cineangiography obtained b) injecting contrast medium into the inferior cava confirmed the location and direction of shrmt. Over the four month period during which these studies were performed, cyanosis became an increasingly prominent finding, and respiratory embarrassment progressi\,cl\, increased until the patient was dyspneic recumbent as well as erect. This gradual deterioration was attributed in retrospect to progressive dislocation of the heart into the right chest with anglllation of the atria1 septum in such a manner to permit a greater degree of right to left shrmtins from the inferior vena cava directly into the secundum defect. The blood gas studies delllonstrate the inadequacy of arterial oxygen saturation as a measure of response to breathing lOOo/, oxygen. In Table II, normal arterial oxygen saturation is attained on April 34, 1964, with the patient breathing lOO%, oxygen while supine, but the p0~ response is clearl!. and markedly diminished. This is the Illajor clrre to an abnormal venoarterial shllnt, the exact nature of which was deterlrlined only by selective dye-dilution studies. Our experience illustrates the importance of blood gas studies in problenls of c).anosis or respiratory distress. Failure to improve pOn by breathing 100% oxygen for seven or Inore minutes strongly suggests right to left shunting either in the lungs or heart. Appropriate indicator-dilution technics and cineangiographb may then be employed to localize flu,ther the area of shunt. SUMMARY
Two unusual cases of atria1 septal defect are presented with right to left shunting occllrring from fllnctional drainage of the inferior I-ena
300
Winters
cava into the left atrium. The first had been unrecognized in a teenage boy who previously had undergone successful closed pulmonary valvotomy for congenital pulmonary valvular The second occurred following a right stenosis. pneumonectomy for bronchogenic carcinoma in a man with a previously undetected atria1 septal defect. The respiratory embarrassment developing postoperatively was related to dislocation of the heart resulting in an anatomic shift of the atria1 septum so that the inferior cava emptied directly into the septum secundum defect. Both patients had normal right heart pressures, and in each the diagnosis was established by selective dye-dilution curves and confirmed Blood gas studies by selective cineangiography. were instrumental in the second case in pointing toward a right to left shunt subsequently conThe imporfirmed by dye-dilution studies. tance of blood pH, pCO2, and ~02 studies and selective indicator-dilution studies in the evaluation of patients with unexplained cyanosis or respiratory distress is emphasized. REFERENCES 1. LITTLE, R. C., OPDYKE, D. F. and HAWLEY, J. G. Dynamics
of experimental
atria1 septal
Am. J. Physiol., 158: 241, 1949.
defects.
et al. 2. BRANNON,E. S., WEENS, 1-I. S. and
WARREN,
.J. N.
Atria1 septal defect: Study of hemodynamics by Am. the technique of right heart catheterization.
3.
J. M. Sc., 210: 480, 1345. B. E., GERACI, J.
E., POLLACK, A. A., BURCHELL, 1-T. B. and WOOD, E. H. Interatrial tnixing of blood and pulmonary circulatory dynamics in atria1 septal defects. Pm. Staff Meet.
TAYLOR,
Mayo Clin., 23: 500, 1948. 4. SOULIE, P., JOLY, F., CARLOTTI, J. and SICOT, J. R. Arch. mal. Les communications interauriculaires. mew, 43: 97, 1950. 5. SELXER, A. and LEWIS, A. E. The occurrence of chronic
cyanosis in cases of atria1 septal defect.
Am. J. M. SC., 218: 516,1949. 6. LIND, J. and WEGELIUS, C. children.
Atria1 septal defects in An angiocardiographic study. Circula-
tion, 7: 819, 1953. 7.
H. J. C., BURCHELL, H. B. and WOOD, E. H. The presence of venoarterial shunts in patients with interatrial communications. Circulation, 10 :
SWAN,
705,1954. 8. SWAN, H. J. C., ZAPATA DIAZ, J. and WOOD, E. H. Dye dilution curves in cyanotic congenital heart disease. Circulation, 8: 70, 1953. 9. OAKLEY, C. M., BRAIMBRIDGE, M. V., BEN,TALL, H. H. and CLELAND, W. P. Reversed interatrial shunt following complete relief of pulmonary valvular stenosis. Bit. Heart J., 26: 662, 1964. 10. GALLAHER, M. E., SPERLING, D. R., GWINN, J. L., MOYER, B. W. and FYLER, D. C. Functional drainage of the inferior vena cava into the left ilm. J. Cardial., 12: 561, atrium--- three cases.
1963.
THE AMERICAN JOURNAL OF CARDIOLOGY
Shunting
to Left Atrium with
Normal
from
Inferior
in Atria1
Right
Heart
Vena
Septal
Defects
Pressures
Report of Two Cases* WILLIAM KALPH
K.
L. WINTERS, JR., M.D., F.A.c.c., TYSON,
FELIX CORTES, M.D., MICHAEL MCDONOUGH,
Philadelphia,
Pennsylvania
but disclosed, in addition, arterial unsaturation resulting from an interatrial communication traversed by the cardiac catheter. The boy had been well until
T
HE majority of uncomplicated atria1 septal defects manifest left to right shunting. However, right to left intracardiac shunting, when it occurs in atria1 septal defect, need not be associated with pulmonary hypertension or pulmonary valvular stenosis. Occasionally a peculiar developmental or anatomic derangement of the positioning of the atria1 opening of the inferior or superior cava may permit drainage of a part of all of the caval flow to the left atrium producing cyanosis of varying degree with or without respiratory embarrassment. Two such cases of drainage of a portion of the inferior cava flow into the left atrium are preOne was unrecognized at the time of sented. successful surgical correction of a congenital pulmonary valvular stenosis. An atria1 septal defect came to be suspected in the second patient with the appearance of cyanosis, dyspnea and evidence for intracardiac venoarterial shunting after a pneurnonectomy for bronchogenic carcinoma. The importance of blood gas tension studies and selective dye-dilution or cineangiographic technics to study inferior and superior cavai flow in confirming this diagnosis is enlphasized.
December 5, when he complained of severe fatigue and dyspnea. His mother then noted cyanosis. A heart defect had been known to exist since age 5, but he had been otherwise asymptomatic. At the time of operation, a grade 3/6 harsh, ejection, basal systolic murmur was present with diminished Pp and a left parasternal systolic lift. An electrocardiogram showed right atria1 enlargement, marked right axis deviation and right ventricular hypertrophy. Chest roentgenogram demonstrated right atria1 prominence, enlarged pulmonary artery segment and diminished intrapulmonary vasculature. The hemoglobin was 22.4 gm., hematocrit 75%. Following a successful closed pulmonary valvotomy, the postoperative course was uneventful. He ~elasreadmitted on April 9, 1962, for re-evaluation because of a persistent cardiac murmur and cyanosis. Since surgery there had been considerable improvement in exercise tolerance and much less dyspnea. On examination, there remained nail-bed cyanosis and clubbing of fingers and toes, a systolic thrill in the second left intercostal space with a grade 5/6 ejection systolic murmur, and a short, early diastolic, decrescendo murmur. The latter was thought to represent pulmonary valvular insufficiency commonly following closed pulmonary valvotomy. The electrocardiogram still showed right axis deviation, right ventricular hypertrophy (less than preoperatively) and incomplete right bundle branch block. On chest roentgenogram the heart size and configuration were unchanged. Right atria1 prominence and large pulmonary artery segment persisted. Hemoglobin was 20.7 gm.%. Cardiac catheterization was again performed April 12
CASE REPORTS
This 17 year old white boy underwent a closed pulmonary valvotomy at St. Christopher’s Hospital for Children in Philadelphia on Dec. 12, 1959, for pulmonary valvular stenosis. Catheterization studies (Table I) performed December 17 confirmed the presence of pulmonary valvular stenosis CASE
1.
* From the Departments of Medicine and Surgery, Temple University Medical study was supported in part by U. S. Public Health Service. Grant HE 06313. VOLUME
19, FEBRUARY
M.D.,
M.D., HOWARD BAIER, M.D., JOSE GIMENEZ, M.D. and JULIO C. DAVILA, ~hl.~., I’.A.c.c.
t 967
293
Center,
Philadelphia,
Pa.
This
Winters
294
Chsc
----12/17/57--Pressure (mm. Hg) SVC
1.
Catheterization
Chriiac
-_ 02 Content (vol.‘:;)
et al.
w--4/12/62---Pressure (mm. Hg)
Data _--_----5 0.2 Content (vol.‘:;,)
18.7
20.7 22.7 22.1 21.4
IVC RI\
H L M
1iv PA LA LV BA H = high;
16/3 (8) 230/O 12/8 8 105/8 115/76 L = low;
17.; 17.1 16.4 16.0 15.9 18.3 23.2 (78’&)
a = 15 v=7 30/o-5 22/7 19/7 115/75
02 Content (\wl.“; ) ~~~~ .____
I(l.2 v = 3 (2)
22.5 19.3 70.5
10/4 11/5 8/3(3)
19.0 19.2 20.0
20.8 21.5
26.7
/7 /J63__~_. .__.~~_
PreSsWe (mm. Ifg)
(96c/;)
120/84
25.9
(87l;;)
M = mid.
(‘Table I). The atria1 septal defect was easily entered from the right saphenous vein. Right ventricular pressure was now normal. A selective cineangiogram with injection into the left atrium outlined the atria1 septal defect. The interpretation of this finding in relation to the cyanosis is not clear from hospital records. In retrosL>ect, arterial-venous admixture at the atria1 level would adequately explain the cyanosis. He was admitted to ‘Temple University Hospital for further study of the persistent cyanosis on March 7,
1963. He had remained completely asymptomatic, requiring no medication and working regularly 40 hours a week as a sewing machine operator. On examination there was obvious nail-bed cyanosis. There remained the previously noted systolic thrill in the second left intercostal space, and systolic and diastolic murmurs along the upper left sternal border. Laboratory Studies: The electrocardiogram showed right axis deviation and right bundle branch block (Fig. 1). Chest roentgenogram (Fig. 2) disclosed an enlarged pulmonary artery segment, but \vas other-
FIG. 1. Case 1. Preoperative electrocardiogram demonstrates an incomplete right bundle branch block pattern with rightward deviation of the terminal portion of the QRS complex.
gram Mar. 8,1963,
FIG. 2.
Case 1.
Preoperative posteroonterior chest roentgeno-
shows slight prominence
of pulmonary
artery segment. THE
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Venoarterial
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2 ‘I 5
Ikfects
%I iL
LRA
7 0
I
71115
I 2:
set POSTop WC to FA
SCC
FIG. 3. Case 1. Dyp-ddu&n curws. Indocyanine green (5 mg.) was injected into supcriol vena cava (SVC), low right atrium (LRA), inferior vena cave (IVC) preoperatively and inferior vena cava postoperatively. Note early appearance of dye at femoral artery salllplinq site (F.4) related most closely to injection into the inferior venn cava prcoperativcly and absent postoperatively.
wisr normal. Hemoglobin was 21.5 gm., hematocrit 637;. An arterial blood sample obtained with the patient breathing room air was 93.6yc saturated with a l)O:! of 71.5, pCO:! 44.5, and pH 7.463. After breathing 100% oxygen for 10 minutes, the saturation rose to 97.3yo, but the 1’02 rose only to 97.5, and pCO? dropped to 35. The pH remained 7.455. Ci~~liczc-cutheterization was repeated on May 9 (Table I). Dye-dilution studies (Fig. 3) performed by injecting ?J mg. Cardio-Green” into the superior vena cava, right atrium, inferior vena cava, right ventricle and left atrium I\-ith sampling at a femoral artery indicated a right to left shunt into the left atrium related predominantly to flow from the inferior vena cava through the previously diagnosed atria1 septal defect. C’ineangiograpl~~ confirmed the location and direction of the shunt. The defect was subsequently closed during cardiopulmonary bypass on May 14. Postoperative dye-dilution studies and cineangiocardiograms demonstrated an intact atrial septum (Fig. 3). At the time of disVOI.UME
19. FEBRUARY
1967
charge, the hemoglobin was 11.3 gm. and hematocrit 35yc. He has remained well without further cyanosis. Postoperative catheterization studies have not as yet been performed. CASE 2. A 52 year old mushroom groxver was first admitted to ‘l‘emple University Medical Center in June 1963, complaining of hoarseness of one year’s duration. He denied any history of dyspnca on exertion, palpitations, ankle edema, or any symptoms referable to the cardiopulmonary system. Physical examination of the heart and lungs was within normal limits. At this time, the electrocardiogram was normal and a chest roentgenogram demonstrated a normal cardiac silhouette. On bronchoscopy, a carcinoma of the right vocal cord was found for Lvhich a partial laryngectomy was performed. The postoperative course was uncomplicated, and the patient \\.a~ discharged to be followed-up as an outpatient. The second hospifal admission occurred in October 1963, when on a routine postoperative chest film a
Winters
et al.
FIG. 4. Case 2. Chest roentgenograms. A, preoperative filnl demonstrates complete obstruction of the right upper lobe bronchus with partial atalectasis. The trachea is displaced to the right. The minor fissurr is elevated. A hilar mass is seen producing a convex bulge at the hilum in contrast to the concave contour of the minor fissure. The heart and pulmonary vascular markings are normal. B, postoperative film shows marked shift of the trachea and mediastinum to the right. The left lung is hyperlucent. The heart cannot be defined.
mass was found in the right hilum (Fig. 4A). ‘The electrocardiogram remained normal, as did a chest roentgenogram for cardiac silhouette and pulmonary vascular markings. Bronchoscopy and cytologic study of the sputum indicated a carcinoma in the right upper lobe. A right pneumonectomy was performed, and at operation the tumor was found to have invaded the wall of the superior vena cava but was not obstructing flow. A portion of the superior vena cava was resected and replaced by a 7 cm. Teflon8 graft. The postoperative course was uncomplicated, and the patient was discharged two weeks after surgery. He continued to improve at home and was fully ambulatory until three months after discharge, when he began to experience some dyspnea occurring only when he changed from the recumbent to the standing position. After standing for a few minutes, the dyspnea disappeared, and he could walk without difficulty. He was thought to be in moderate congestive heart failure and was treated with digitalis but did not improve. These symptoms continued to progress until January 1964, when he was hospitalized at Temple University Hospital for a period of five weeks to determine the cause of this dyspnea. At the time, the patient was comfortable in the recumbent position, but as he attempted to stand or sit up, he would become extremely short of breath and cyanotic.
Assuming the recumbent position relieved the symptoms immediately. Onphysical examination the blood pressure was 120/80 mm. Hg and the weight 125 lb. The patient was thin and appeared chronically ill. The neck veins were not distended. Tracheal deviation toward the right was present, and the breath sounds were normal in the left chest. The left hemithorax was slightly hyper-resonant. Examination of the heart was unremarkable ; there was normal sinus rhythm at a rate of 80/min. Examination of the abdomen was within normal limits. The peripheral arterial pulses were normal and equal bilaterally. The chest roentgenogram (Fig. 4B) showed a mediastinal shift and deviation of the trachea into the right chest. Some herniation of the left lung into the right chest anteriorly was also present. The cardiovascular silhouette was normal. Chest x-ray examination and fluoroscopy were performed with the patient in both the supine and erect positions, but no abnormalities were found to explain the dyspnea. Bronchoscopy revealed a normal tracheobronchial tree. Right heart catheterization was performed to obtain a pulmonary angiogram. Right atria1 and right venA biplane venous tricular pressures were normal. angiogram was obtained with the patient first in the recumbent and then the sitting position by injection of Renovist@ into the left antecubital vein. Pictures THE
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Venoarterial
Shunting
r[‘ARL.E II (hsr
2. .\rterial HloodGas Determinations
,.-
-Sirrinp 2 min.
34 95 10 7 57 32 91
8 7 491 .o 5 6
7 435 x2 0
31 8 100 7.442 126 4 30 0 9x 6 92 7 419 448
~-~~ 7 min. O?
7 513 47.7 25.8 X8 25 7.520 334 24.4
7.50 49.1 27.7 no.2
29 7.469 85.0 33.8 96.4 9.1
7.452 “. 421 37.1 100
75
were taken at a rate of 2/see. for seven seconds. Right heart chambers were well visualized and were normal in size with no trace of a right to left shunt. Laboratory studies wre as follows: P uptake 3370 in 24 hours, hemoglobin 16 gm.%, hematocrit 49, \\hite blood cells 9,400 with a normal differential. Crinary excretion of 17 ketosteroids was 417 mg. for 24 hours. Urinalysis, fasting blood sugar and serum electrolytes were normal. ‘/‘he elect?-ocardiogram at this time revealed right axis deviation with questionable P wave abnormalities suggestive of pulmonary disease. There was clockwise rotation of the heart in its longitudinal axis and a tendency to low voltage. External spirometr,v demonstrated vital capacity to be 40 per cent and maximal breathing capacity 45 per cent of predicted value, with a normal timed vital capacity. rirterial blood gas studies were performed with the patient breathing room air and then 100% oxygen in the supine position and immediately after standing (‘l’able II). These studies revealed a slightly decreased arterial blood ~02 and pCO2 with normal arterial saturation in the supine position. On assumption of the erect posture, unsaturation of the arterial blood appeared which was not correctable by breathing 1007, oxygen. This was interpreted as being due to an abnormal ventilation-perfusion ratio in the remaining lung. A marked increase in minute ventilation appeared, resulting in a decrease in arterial pCO2. No effective treatment was found, and the patient was once again sent home to be followed as an outpatient. His condition continued to deteriorate at home, necessitating readmission in April 1964 for more complete evaluation. At this time the patient was cyanotic in the recumbent position and was unable to sit up in bed. The chest roentgenogram and electrocardiogram revealed no essential change. The hemoglobin had risen to 19 gm. and the hematocrit to 57%. VOLCME.
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1967
in Atria1 Septal
1Iefects
297
Arterial gas tension studies revealed a decrease in arterial PO:! on room air in the recumbent position. The ~02 did not rise as expected on 1005; oxygen (Table II). On assuming the upright position, p0~ decreased drastically, pCOz decreased as the minute ventilation increased. The patient became extremely dyspneic, precluding further stlrdies on lOOy;l oxygen in this position. Right heart catheterization was again performed. The intracardiac pressures remained normal on the right side. Dye-dilution curves obtained by injecting 5 mg. of Cardio-Green into the superior vena cava and right atrium revealed early systemic appearance of dye indicative of right to left shunting of blood (Fig. 5). Injection into the inferior vena cava revealed a larger amount of shunting and was highly suggestive of predominant shunting of blood from the inferior vena cava into the left atrium. Right ventricular injection of dye revealed a normal dye-dilution curve. A cineangiogram at this time confirmed these findings and a diagnosis of atria1 septal defect of the secundum type, with right to left shunting of blood from r.he inferior vena cava to left atrium, was made Closure of the atria1 sepal defect was performed on June 3, 1964, under endotracheal anesthesia, utilizing cardiopulmonary bypass. At the time of operation it was noted that the heart had rotated in such a
way that the inferior vena cava was emptying nearly directly into the atria1 septal defect. The appearance of right to left shunting was attributed to a mediastinal shift following the pneumonectomy in a patient with a small, asymptomatic atria1 secundum defect previously unrecognized. Cardiac catheterization was performed two weeks after surgical intervention. At this time, all studies were within normal limits and dye-dilution curves and rhe cineangiogram revealed no evidence of any intracardiac shunting of blood. The marked mediastinal shift to the right was still observed on chext x-ray examination. ‘The patient has remained \vell with normal hemoglobin and hematocrit. Cathererization studies one year postoperatively confirmed the complete closure of the defect. DISCUSSION
The occurrence of arterial anoxemia and polycythemia in uncomplicated atria1 septal defect is infrequent but may occur with the proper anatomic setting. In the absence of right ventricular diastolic hypertension, the left to right pressure gradient across an atria1 septal defect has been shown to persist during the entire cardiac cycle, or for all but a short period before or during atria1 systole.‘J Thus, under these conditions, to provide sufficient mixing of unsaturated with saturated blood to produce arterial unsaturation, it has been postulated that large secundum defects must be present forming a common chamber.3 Under
298
Winters
et al. SVC to FA
t
t
31 sec.
I!
0
2t2
32t
sec.
IVC to FA
t
t
t
t
0
16
22
32
t sec.
0
t
16
tt 30
34 sec.
5. Case 2. Dye-dilution ~urue. Indocyanine green (5 mg.) was injected into right ventrick (RV), superior vena cava (SVC), right atrium (RA) and inferior vena cava (IVC) preoperatively. Note early appearance of dye at femoral artery sampling site (FA) most closely related to injection into the inferior vena cava and absence of this early curve after injection into the right ventricle. FIG.
other conditions with smaller defects, it is postulated that at some period in the cardiac cycle, presumably during atria1 diastole, the shunt is reversed because of brief changes in the However, Seizer and Lewis5 pressure gradient.4 in a review in 1949 of 180 proved cases of atria1 defect were unable to find any apparent relation between the size of the defect and the They astutely postulated presence of cyanosis. the mechanism of cyanosis to be a directional flow of venous blood into the left auricle under a specific set of anatomic conditions; namely, if one of the venae cavae were so oriented as to permit a stream of blood to be directed into the left atrium during a period when a pressure gradient might be absent or reversed. This need not interfere with the major left to right shunt during the remainder of the cardiac cycle. Such streaming occurs in fetal circulation with inferior caval blood directed through the foramen ovale and superior caval blood through the tricuspid valve. It is not unreasonable to presume that this occurs after birth. Indeed, this type of flow was demonstrated angiocardiographically by Lind and Wegeliu@ in 3 infants. The atria1 septal defect in these patients was not
identifiable when the injection \vas nlade into the superior vena cava but was readily apparent when the injection was made from the inferior cava. Swan, Burchell and Wood’ reported On 9 patients with atria1 septal defects exhibiting right to left shunting by the dye-dilution technic (T-1824). In 5 of these cases the shunt was demonstrable only from the inferior vena cava and in several was not accompanied by s)-stemic Those arterial oxygen unsaturation at rest. cases of shunts demonstrable from the superior vena cava were complicated by other problems. They point to the anatomic relation of the inThe limbus ferior vena cava to the fossa ovalis. of the fossa ovalis straddles the atria1 orifice of the inferior vena cava so that a portion of the inflow from the inferior cava impinges directly on the floor of the fossa ovalis; thus blood from the inferior cava could pass equally \vcll into By the left atrium if a secundurn defect existed. selective dye-dilution studies they could demonstrate whether the defect lay in closer relation Quantito the inferior or superior vena cava. tation of the right to left shunt is possible, although Swan et al.5 rightly point to potential THE
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Venoarterial
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crrorx produced by the complex dilution and ltlisinq proresscs which are not readily quantitatcd. 111 (:asc 1 reported here, a successful closed prlllnonary valvotomy for congenital puhnonary stcllosis \vas accomplished but was followed by The cause for this was persistence of cyanosis. Arterial unsaturation in severe not rccoynized. pullnonary stenosis related to right to left sh(lntine through a patent foramen ovale or associated atria1 septal defect is not uncommon. B\lt persistence of this shunting in the face of normal right heart pressures following surgery, as demonstrated in Table I, should raise the qrlestion of an additional defect. Oakley and associates” recently reported on 6 cases of cono;cnital plllmonary valvular stenosis exhibiting postoperative arterial unsaturation. These patients all exhibited abnormal right ventricular function as evidenced by either systolic or diastolic hypertension. The postoperative arterial unsattlration was demonstrated to be due to right to left shunting at the atria1 level by curves and atcoomasir-blue dye-dilution tribtlted to persistence of abnormal right ventricular compliance. It is not clear, however, lvhether anatomic relation of the inferior or srlperior ca1.a to the left atrium may have played a part. They do emphasize the importance of searching for interatrial communications in patients \vith pl&nonary valvular stenosis so that the>. Inay be closed. This procedure may prevent the complication of postoperative cyanosis occllrriilg in those patients whose right ventricular ft~nction remains abnormal despite correction Case 1 reported here of the \-al\-lllar problem. did not demonstrate residual abnormal right \~rntrict&lr function in terms of pressure abnorrnalit!.. The relation of the inferior vena ca\.al flo\v to the left atrium became quite clear after dye-dillltion curves were obtained by inicctions into various portions of the right heart (Fir. .3). Cineangiography then visually confirtllcd the anatomic relation. This case reselllblcs the 3 reported by Gallaher and his grorlp” in 1963, which also exhibited normal right \.cntriclllar function as manifested by Right to left shunting nor11la1 presstIres. through an atria1 septal defect from the inferior \.cna cava was demonstrated by angiocardiograph!. in 2 patients and confirmed at operation in the third. C;U(, _7 \vas an intriguing problem of rapidly proprcssing respiratory embarrassment related to the lIpright position which followed a right VOI IXI:
1 ‘).
FEBRUARY
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in Atria1
Septal
I )efects
200
pnelnnonectolny for bronchogrnic carcillonla. The initial blood gas studies strongly stlggestrd right to left shtlnting of blood at either the cardiac or pulnlonary area (Table 11). But initial angiocardiographic stltdies attetllpting to locate the defect were ltnsucccssf~ll. Olrr suspicions centered initially on the superior caval graft inserted at the tlrne of operation to replace the portion of cava invaded by the carcinoma, but there was nothing in the operative technic to implicate an abnormal corn--Ï munication between this graft and the left atriuin. A subsequent survey of the inferior and superior cava flow by dye-dilution stttdies indicated right to left shunting at the atria1 level in close approximation to the inferior cava (Fig. 5.). Cineangiography obtained b) injecting contrast medium into the inferior cava confirmed the location and direction of shrmt. Over the four month period during which these studies were performed, cyanosis became an increasingly prominent finding, and respiratory embarrassment progressi\,cl\, increased until the patient was dyspneic recumbent as well as erect. This gradual deterioration was attributed in retrospect to progressive dislocation of the heart into the right chest with anglllation of the atria1 septum in such a manner to permit a greater degree of right to left shrmtins from the inferior vena cava directly into the secundum defect. The blood gas studies delllonstrate the inadequacy of arterial oxygen saturation as a measure of response to breathing lOOo/, oxygen. In Table II, normal arterial oxygen saturation is attained on April 34, 1964, with the patient breathing lOO%, oxygen while supine, but the p0~ response is clearl!. and markedly diminished. This is the Illajor clrre to an abnormal venoarterial shllnt, the exact nature of which was deterlrlined only by selective dye-dilution studies. Our experience illustrates the importance of blood gas studies in problenls of c).anosis or respiratory distress. Failure to improve pOn by breathing 100% oxygen for seven or Inore minutes strongly suggests right to left shunting either in the lungs or heart. Appropriate indicator-dilution technics and cineangiographb may then be employed to localize flu,ther the area of shunt. SUMMARY
Two unusual cases of atria1 septal defect are presented with right to left shunting occllrring from fllnctional drainage of the inferior I-ena
300
Winters
cava into the left atrium. The first had been unrecognized in a teenage boy who previously had undergone successful closed pulmonary valvotomy for congenital pulmonary valvular The second occurred following a right stenosis. pneumonectomy for bronchogenic carcinoma in a man with a previously undetected atria1 septal defect. The respiratory embarrassment developing postoperatively was related to dislocation of the heart resulting in an anatomic shift of the atria1 septum so that the inferior cava emptied directly into the septum secundum defect. Both patients had normal right heart pressures, and in each the diagnosis was established by selective dye-dilution curves and confirmed Blood gas studies by selective cineangiography. were instrumental in the second case in pointing toward a right to left shunt subsequently conThe imporfirmed by dye-dilution studies. tance of blood pH, pCO2, and ~02 studies and selective indicator-dilution studies in the evaluation of patients with unexplained cyanosis or respiratory distress is emphasized. REFERENCES 1. LITTLE, R. C., OPDYKE, D. F. and HAWLEY, J. G. Dynamics
of experimental
atria1 septal
Am. J. Physiol., 158: 241, 1949.
defects.
et al. 2. BRANNON,E. S., WEENS, 1-I. S. and
WARREN,
.J. N.
Atria1 septal defect: Study of hemodynamics by Am. the technique of right heart catheterization.
3.
J. M. Sc., 210: 480, 1345. B. E., GERACI, J.
E., POLLACK, A. A., BURCHELL, 1-T. B. and WOOD, E. H. Interatrial tnixing of blood and pulmonary circulatory dynamics in atria1 septal defects. Pm. Staff Meet.
TAYLOR,
Mayo Clin., 23: 500, 1948. 4. SOULIE, P., JOLY, F., CARLOTTI, J. and SICOT, J. R. Arch. mal. Les communications interauriculaires. mew, 43: 97, 1950. 5. SELXER, A. and LEWIS, A. E. The occurrence of chronic
cyanosis in cases of atria1 septal defect.
Am. J. M. SC., 218: 516,1949. 6. LIND, J. and WEGELIUS, C. children.
Atria1 septal defects in An angiocardiographic study. Circula-
tion, 7: 819, 1953. 7.
H. J. C., BURCHELL, H. B. and WOOD, E. H. The presence of venoarterial shunts in patients with interatrial communications. Circulation, 10 :
SWAN,
705,1954. 8. SWAN, H. J. C., ZAPATA DIAZ, J. and WOOD, E. H. Dye dilution curves in cyanotic congenital heart disease. Circulation, 8: 70, 1953. 9. OAKLEY, C. M., BRAIMBRIDGE, M. V., BEN,TALL, H. H. and CLELAND, W. P. Reversed interatrial shunt following complete relief of pulmonary valvular stenosis. Bit. Heart J., 26: 662, 1964. 10. GALLAHER, M. E., SPERLING, D. R., GWINN, J. L., MOYER, B. W. and FYLER, D. C. Functional drainage of the inferior vena cava into the left ilm. J. Cardial., 12: 561, atrium--- three cases.
1963.
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