- Email: [email protected]
Reverse alveolar circulation in patients with cyanotic congenital heart disease
Reverse alveolar circulation in patients with cyanotic congenital heart disease Theodore H. Stanley, M.D.,* and Willem J. Kolff, M.D., Ph.D.,** Salt Lake City, Utah, and San Antonio, Texas
Although it has been shown experimentally that a reversed alveolar circulation, that is, pulmonary vein to alveolar capillary to pulmonary artery blood flow, will result in oxygen uptake and carbon dioxide exchange, 1, ~ a disease state with this type of circulation and the significance of such a flow have not been described. Patients with cyanotic congenital heart disease have increased bronchial artery blood flows which have been shown to participate in respiratory gas exchange. e-;; While it has been assumed that the pathway of bronchial flow in these patients is via a bronchial artery to pulmonary artery to alveolar capillary route, respiratory exchange could also be achieved via one of two other routes: (I) bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery or (2) bronchial artery to alveolar capillary to pulmonary artery. The surgical repair of tricuspid atresia in 2 patients with functioning Glenn anastomoses (superior vena cava to right pulmonary artery) enabled us to measure proximal right pulmonary artery (PRPA) oxygen tensions and to determine whether From the Divisions of Anesthesiology and Artificial Organs,
University of Utah College of Medicine, Salt Lake City, Utah 84112, and the Division of Anesthesiology, Wilford Hall, USAF Medical Center, San Antonio, Texas 78236. Received for publication March 28, 1973. • Assistant Professor of Anesthesiology and Assistant Research Professor of Surgery, University of Utah, College of Medicine. •• Professor of Surgery and Chairman, Division of Artificial Organs, University of Utah, College of Medicine.
16
a reverse circulation takes place in these patients. Methods
The 2 children were Caucasian boys, 10 and 12 years of age. Both had previously undergone palliative Glenn and left BlalockTaussig procedures in order to increase arterial oxygenation, but they were now outgrowing the shunts as witnessed by a decreasing exercise tolerance and arterial oxygen tensions in the range of 35 to 40 mm. Hg. Both were small (23 and 28 kilograms), obviously cyanotic children in no distress. Their preoperative hemoglobin values were 21.2 and 19.8 Gm. per cent, respectively and both were receiving digoxin. Premedication consisted of 0.4 mg. of morphine sulfate administered intramuscularly 90 minutes before the scheduled surgery. When the patients arrived in the operating room, two large-bore intravenous lines were started in the arms and a No. 16 gauge central venous pressure catheter was placed in the antecubital fossa and threaded through the Glenn anastomosis into the PRPA. This position was confirmed at surgery. Anesthesia was slowly induced with 100 to 200 mg. of sodium thiopental and maintained with 0.5 to 2 per cent halothane and 98 to 100 per cent oxygen. The patients were then paralyzed with 1.5 mg. per kilogram of succinylcholine and intubated. Subsequent paralysis was maintained with periodic 3 to 6 mg. increments
Volume 66
Reverse alveolar circulation
Number 1
17
July, 1973
of d-tubocurarine. After intubation, a catheter was inserted in the radial artery for pressure measurements and blood sampling. The surgical procedure has been previiously reported." In patients with the Glenn anastomosis, the procedure entails a diversion of all of the inferior vena cava blood to the left lung via the creation of a shunt between the right atrium and the main pulmonary artery (which merely perfuses the left lung). In short, the right atrium is used to propel inferior vena caval blood through the left lung. To facilitate this function, the right atrium is provided with two aortic or pulmonary valve homografts: One is inserted into the inferior vena cava at its junction with the right atrium, to prevent blood reflux into the inferior vena cava during atrial systole; the other is used as an anastomosis between the right atrial appendage and the main pulmonary artery so that, during atrial diastole, there is no reflux from the left pulmonary artery into the right atrium. The operation is performed through a median sternotomy with cardiopulmonary bypass. Bypass was accomplished in both of our patients by a diversion of blood from the superior and inferior venae cavae to a Bentley bubble oxygenator and a Sarns roller pump, with reintroduction of the arterialized blood into the femoral artery. Extracorporeal flow rates and radial arterial blood pressures were recorded every 15 minutes during bypass. Although blood from the superior vena cava was no longer flowing through the lungs, our catheter remained in the PRPA for pressure measurement and blood sampling. During bypass, the lungs were semiinflated with 100 per cent oxygen or 100 per cent nitrous oxide at a steady endotracheal tube pressure of 8 to 10 em. of water. Arterial and proximal right pulmonary artery blood samples were slowly drawn at 5 minute intervals for analysis of oxygen tension. Oxygen tensions were determined on an Instrumentation Laboratories digital acid-base analyzer. Corrections for temperature difference between the patient and the analyzer were incorporated into the
reported results. Both patients lost heat during the surgical procedure; by the time bypass was started their temperatures were 32 to 33° C. as measured by an esophageal temperature probe (Yellow Springs Instrument Co., Yellow Springs, Ohio). This temperature was maintained during bypass with the use of a heat exchanger in the extracorporeal circuit. Results While the patients were breathing 98 to 100 per cent oxygen, after the induction of anesthesia, arterial oxygen tension averaged between 60 and 70 mm. Hg and PRPA oxygen tension between 26 and 34 mm. Hg in both patients. Mean PRPA blood pressures were between 8 and 15 mm. Hg. With the surgical opening of the chest, arterial oxygen tension improved to a range between 70 and 80 mm. Hg and PRPA oxygen tension to between 34 and 38 mm. Hg. Mean PRPA blood pressures did not change. Five minutes after the start of total heart-lung bypass, with the lungs inflated with 100 per cent oxygen, arterial oxygen tension was 176 mm. Hg and PRPA oxygen tension was 99 mm. Hg (Table I). Ten minutes later, arterial oxygen tension was essentially the same at 189 mm. Hg, but PRPA oxygen tension was now 235 mm. Hg. After 30 minutes, although arterial oxygen tension had not changed, PRPA oxygen tension had risen to 350 mm. Hg. At this point, the lungs were ventilated with 100 per cent nitrous oxide at 8 L. per minute for 5 minutes and then allowed to remain in the semi-inflated state with nitrous oxide as the inflating gas. After 5 minutes of exposure to nitrous oxide, both arterial and PRPA oxygen tensions were 200 mm. Hg. Fifteen minutes later, arterial oxygen tension was 190 and PRPA oxygen tension was 155 mm. Hg. After 30 minutes of exposure to nitrous oxide, although arterial oxygen tension was essentially unchanged, that of the PRPA was 138 mm. Hg. During bypass, mean PRPA and arterial blood pressures were relatively stable, averaging 18 ± 5 and 60 ± 11 mm. Hg, respectively.
The Journal of
18
Stanley and Kolff
Thoracic and Cardiovascular Surgery
Table I. Arterial and proximal right pulmonary artery (PRPA) oxygen tensions during cardiopulmonary bypass in 2 patients with tricuspid atresia Time of exposure to inflating gas Inflating gas
Oxygen Oxygen Oxygen Nitrous Nitrous Nitrous
(100 per cent) (100 per cent) (100 per cent) oxide (100 per cent) oxide (100 per cent) oxide (100 per cent)
(min.)
Case 1
Case 2
Arterial Po, I PRPA Po, (111m. Hg) (mm. Hg)
5 15 30 5 20 30
The findings during bypass in the second patient were similar. Bypass PRPA and arterial blood pressures averaged 16 ± 4 and 58 ± 9 mm. Hg, respectively. Five minutes after the start of bypass, arterial and PRPA oxygen tensions were 138. and 78 mm. Hg, respectively (Table I). Ten minutes later, arterial oxygen tension equalled 120 mm. Hg, and PRPA oxygen tension was 190 mm. Hg. After 30 minutes of bypass, arterial oxygen tension was 145 mm. Hg while PRPA oxygen tension had risen to 345 mm. Hg. Five minutes after nitrous oxide was begun, arterial oxygen tension was still 145 mm. Hg, but that of the PRPA equalled 191 mm. Hg. By 20 minutes, although arterial oxygen tension had been increased to 150 mm. Hg, PRPA oxygen tension was 110 mm. Hg. After 30 minutes of exposure to nitrous oxide, PRPA oxygen tension had dropped to 89 mm. Hg. Discussion
Bronchial artery .o pulmonary artery anastomoses are known to exist in the normal lung but are functionally closed in the absence of disease.' Many stimuli have been shown to encourage both the opening of these pre-existing channels and the development of new bronchial collaterals.v 8-10 One of the most profound of these stimuli is the presence of cyanotic congenital heart disease with decreased pulmonary artery flow.3 Collateral blood flow as high as 2 L. per square meter per minute or 5 L. per minute, approaching 75 per cent of total cardiac output, has been reported in these condi-
176 189 189 200 190 187
99 235 350 200 155 138
Arterial Po, (111111. Hg)
138 120 145 145 150 151
I PRPA
Po, (mm. Hg)
78 190 345 191 110 89
tions. It has been noted that large-lumen channels anastomose with the pulmonary artery at the precapillary level and that this expanded blood flow participates in gas exchange at the alveolar level. These findings suggest that the major pathway of bronchial flow in these patients is via a bronchial artery to pulmonary artery to alveolar capillary route." While this may be so, the simultaneous existence of many anastomoses between the bronchial artery and pulmonary vein and between the bronchial artery and alveolar capillaries implies that respiratory exchange and a major blood flow pattern could exist via either of two routes: (1) bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery or (2) bronchial artery to alveolar capillary to pulmonary artery. Indeed, Liebow and colleagues" showed that Diodrast, injected into the bronchial arteries, opacifies the pulmonary veins before the pulmonary arteries. In this study, PRPA oxygen tension during bypass was as much as 200 mm. Hg higher than arterialized blood flowing directly from the heart-lung machine. Since the lungs of the patients were filled with 100 per cent oxygen, such degrees of pulmonary artery oxygenation could have been achieved only via reverse pulmonary blood flow with alveolar oxygen uptake, probably from either a bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery route or a bronchial artery to alveolar capillary to pulmonary artery route. Although suction from the aspiration of
Volume 66
Reverse alveolar circulation
Number 1 July, 1973
blood through the PRPA catheter could artificially cause a reverse alveolar blood flow by decreasing pulmonary artery pressure below that of the left atrium, we doubt that this occurred, for the suction required to fill the syringe and the volume of blood taken at each sampling (3 ml.) were minimal. Changing the lung-inflating gas from 100 per cent oxygen to 100 per cent nitrous oxide resulted in a progressive decrease of PRP A oxygen tensions to levels below those of arterial blood, confirming that alveolar gas exchange was the mechanism by which PRPA oxygen tensions were being changed, Because of many unknowns-i.e., blood volume in the right lung, the flow rate of bronchial artery blood directly into the pulmonary artery via precapillary anastomosis with the latter, and the flow rates of venous drainage away from the lung-it is impossible to estimate what fraction of the total bronchial artery flow traveled in a reverse direction to normal at the alveolar-capillary level. It is easy to see, however, that this is an intrinsically more efficient means of oxygen transfer in cyanotic congenital heart disease: It necessitates a double exposure of such blood to the alveolar air sacs, a backward flow past the alveoli to the pulmonary artery, and then a second exposure to the alveoli when the blood returns to the left heart. At present, it is difficult to say whether this type of flow actually occurs in the patient with cyanotic congenital heart disease when he is' neither anesthetized nor on heart-lung bypass. However, these stud-
19
ies do demonstrate that the capacity for reverse circulation with oxygenation does exist in these patients and suggests that this type of circulation may help to increase arterial oxygen saturation for them.
REFERENCES
2 3 4
5
6 7 8
9 10
Houle, D. B., Campbell, G. S., and Visscher, M. B.: Retrograde and Forward Perfusion of Isolated Canine Lung Lobes, Proc. Soc. Exp. BioI. Med. 97: 892, 1958. Stanley, T. H.: Unpublished data. Bing, R. J., Vandam, L. D., and Gray, F. D.: Physiological Studies in Congenital Heart Disease, Johns Hopkins Med. J. 80: 121, 1947. Landrigan, P. R., Purkis, I. E., Roy, D. E., and Cudkowicz, L.: Cardio-respiratory Studies in a Patient With an Absent Left Pulmonary Artery, Thorax 18: 77, 1963. Liebow, A. A., Hales, M. R., and Bloomer, W. E.: Relation of Bronchial to Pulmonary Vascular Tree, in Adams, W. R., and Veith, I., editors: Pulmonary Circulation, New York, 1958, Grune & Stratton, Inc. Fontan, F., and Baudet, E.: Surgical Repair of Tricuspid Atresia, Thorax 26: 240, 1971. Hutchin, P., Terzi, R. G. G., and Peters, R. M.: Bronchial-Pulmonary Artery Reverse Flow, Ann. Thorac. Surg. 4: 391, 1967. Alley, R. D., Stranahan, A., Kausel, H., Formel, P., and Van Mierop, L. H. S.: Demonstration of Bronchial-Pulmonary Artery Reverse Flow in Suppurative Pulmonary Disease, Clin. Res. 6: 41, 1958. Cudkowicz, L., and Armstrong, J. 8.: The Blood Supply of Malignant Pulmonary Neoplasms, Thorax 8: 152, 1953. Hanes, P., and Heath, D.: The Human Pulmonary Circulation, Baltimore, 1962, The Williams & Wilkins Company.
Although it has been shown experimentally that a reversed alveolar circulation, that is, pulmonary vein to alveolar capillary to pulmonary artery blood flow, will result in oxygen uptake and carbon dioxide exchange, 1, ~ a disease state with this type of circulation and the significance of such a flow have not been described. Patients with cyanotic congenital heart disease have increased bronchial artery blood flows which have been shown to participate in respiratory gas exchange. e-;; While it has been assumed that the pathway of bronchial flow in these patients is via a bronchial artery to pulmonary artery to alveolar capillary route, respiratory exchange could also be achieved via one of two other routes: (I) bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery or (2) bronchial artery to alveolar capillary to pulmonary artery. The surgical repair of tricuspid atresia in 2 patients with functioning Glenn anastomoses (superior vena cava to right pulmonary artery) enabled us to measure proximal right pulmonary artery (PRPA) oxygen tensions and to determine whether From the Divisions of Anesthesiology and Artificial Organs,
University of Utah College of Medicine, Salt Lake City, Utah 84112, and the Division of Anesthesiology, Wilford Hall, USAF Medical Center, San Antonio, Texas 78236. Received for publication March 28, 1973. • Assistant Professor of Anesthesiology and Assistant Research Professor of Surgery, University of Utah, College of Medicine. •• Professor of Surgery and Chairman, Division of Artificial Organs, University of Utah, College of Medicine.
16
a reverse circulation takes place in these patients. Methods
The 2 children were Caucasian boys, 10 and 12 years of age. Both had previously undergone palliative Glenn and left BlalockTaussig procedures in order to increase arterial oxygenation, but they were now outgrowing the shunts as witnessed by a decreasing exercise tolerance and arterial oxygen tensions in the range of 35 to 40 mm. Hg. Both were small (23 and 28 kilograms), obviously cyanotic children in no distress. Their preoperative hemoglobin values were 21.2 and 19.8 Gm. per cent, respectively and both were receiving digoxin. Premedication consisted of 0.4 mg. of morphine sulfate administered intramuscularly 90 minutes before the scheduled surgery. When the patients arrived in the operating room, two large-bore intravenous lines were started in the arms and a No. 16 gauge central venous pressure catheter was placed in the antecubital fossa and threaded through the Glenn anastomosis into the PRPA. This position was confirmed at surgery. Anesthesia was slowly induced with 100 to 200 mg. of sodium thiopental and maintained with 0.5 to 2 per cent halothane and 98 to 100 per cent oxygen. The patients were then paralyzed with 1.5 mg. per kilogram of succinylcholine and intubated. Subsequent paralysis was maintained with periodic 3 to 6 mg. increments
Volume 66
Reverse alveolar circulation
Number 1
17
July, 1973
of d-tubocurarine. After intubation, a catheter was inserted in the radial artery for pressure measurements and blood sampling. The surgical procedure has been previiously reported." In patients with the Glenn anastomosis, the procedure entails a diversion of all of the inferior vena cava blood to the left lung via the creation of a shunt between the right atrium and the main pulmonary artery (which merely perfuses the left lung). In short, the right atrium is used to propel inferior vena caval blood through the left lung. To facilitate this function, the right atrium is provided with two aortic or pulmonary valve homografts: One is inserted into the inferior vena cava at its junction with the right atrium, to prevent blood reflux into the inferior vena cava during atrial systole; the other is used as an anastomosis between the right atrial appendage and the main pulmonary artery so that, during atrial diastole, there is no reflux from the left pulmonary artery into the right atrium. The operation is performed through a median sternotomy with cardiopulmonary bypass. Bypass was accomplished in both of our patients by a diversion of blood from the superior and inferior venae cavae to a Bentley bubble oxygenator and a Sarns roller pump, with reintroduction of the arterialized blood into the femoral artery. Extracorporeal flow rates and radial arterial blood pressures were recorded every 15 minutes during bypass. Although blood from the superior vena cava was no longer flowing through the lungs, our catheter remained in the PRPA for pressure measurement and blood sampling. During bypass, the lungs were semiinflated with 100 per cent oxygen or 100 per cent nitrous oxide at a steady endotracheal tube pressure of 8 to 10 em. of water. Arterial and proximal right pulmonary artery blood samples were slowly drawn at 5 minute intervals for analysis of oxygen tension. Oxygen tensions were determined on an Instrumentation Laboratories digital acid-base analyzer. Corrections for temperature difference between the patient and the analyzer were incorporated into the
reported results. Both patients lost heat during the surgical procedure; by the time bypass was started their temperatures were 32 to 33° C. as measured by an esophageal temperature probe (Yellow Springs Instrument Co., Yellow Springs, Ohio). This temperature was maintained during bypass with the use of a heat exchanger in the extracorporeal circuit. Results While the patients were breathing 98 to 100 per cent oxygen, after the induction of anesthesia, arterial oxygen tension averaged between 60 and 70 mm. Hg and PRPA oxygen tension between 26 and 34 mm. Hg in both patients. Mean PRPA blood pressures were between 8 and 15 mm. Hg. With the surgical opening of the chest, arterial oxygen tension improved to a range between 70 and 80 mm. Hg and PRPA oxygen tension to between 34 and 38 mm. Hg. Mean PRPA blood pressures did not change. Five minutes after the start of total heart-lung bypass, with the lungs inflated with 100 per cent oxygen, arterial oxygen tension was 176 mm. Hg and PRPA oxygen tension was 99 mm. Hg (Table I). Ten minutes later, arterial oxygen tension was essentially the same at 189 mm. Hg, but PRPA oxygen tension was now 235 mm. Hg. After 30 minutes, although arterial oxygen tension had not changed, PRPA oxygen tension had risen to 350 mm. Hg. At this point, the lungs were ventilated with 100 per cent nitrous oxide at 8 L. per minute for 5 minutes and then allowed to remain in the semi-inflated state with nitrous oxide as the inflating gas. After 5 minutes of exposure to nitrous oxide, both arterial and PRPA oxygen tensions were 200 mm. Hg. Fifteen minutes later, arterial oxygen tension was 190 and PRPA oxygen tension was 155 mm. Hg. After 30 minutes of exposure to nitrous oxide, although arterial oxygen tension was essentially unchanged, that of the PRPA was 138 mm. Hg. During bypass, mean PRPA and arterial blood pressures were relatively stable, averaging 18 ± 5 and 60 ± 11 mm. Hg, respectively.
The Journal of
18
Stanley and Kolff
Thoracic and Cardiovascular Surgery
Table I. Arterial and proximal right pulmonary artery (PRPA) oxygen tensions during cardiopulmonary bypass in 2 patients with tricuspid atresia Time of exposure to inflating gas Inflating gas
Oxygen Oxygen Oxygen Nitrous Nitrous Nitrous
(100 per cent) (100 per cent) (100 per cent) oxide (100 per cent) oxide (100 per cent) oxide (100 per cent)
(min.)
Case 1
Case 2
Arterial Po, I PRPA Po, (111m. Hg) (mm. Hg)
5 15 30 5 20 30
The findings during bypass in the second patient were similar. Bypass PRPA and arterial blood pressures averaged 16 ± 4 and 58 ± 9 mm. Hg, respectively. Five minutes after the start of bypass, arterial and PRPA oxygen tensions were 138. and 78 mm. Hg, respectively (Table I). Ten minutes later, arterial oxygen tension equalled 120 mm. Hg, and PRPA oxygen tension was 190 mm. Hg. After 30 minutes of bypass, arterial oxygen tension was 145 mm. Hg while PRPA oxygen tension had risen to 345 mm. Hg. Five minutes after nitrous oxide was begun, arterial oxygen tension was still 145 mm. Hg, but that of the PRPA equalled 191 mm. Hg. By 20 minutes, although arterial oxygen tension had been increased to 150 mm. Hg, PRPA oxygen tension was 110 mm. Hg. After 30 minutes of exposure to nitrous oxide, PRPA oxygen tension had dropped to 89 mm. Hg. Discussion
Bronchial artery .o pulmonary artery anastomoses are known to exist in the normal lung but are functionally closed in the absence of disease.' Many stimuli have been shown to encourage both the opening of these pre-existing channels and the development of new bronchial collaterals.v 8-10 One of the most profound of these stimuli is the presence of cyanotic congenital heart disease with decreased pulmonary artery flow.3 Collateral blood flow as high as 2 L. per square meter per minute or 5 L. per minute, approaching 75 per cent of total cardiac output, has been reported in these condi-
176 189 189 200 190 187
99 235 350 200 155 138
Arterial Po, (111111. Hg)
138 120 145 145 150 151
I PRPA
Po, (mm. Hg)
78 190 345 191 110 89
tions. It has been noted that large-lumen channels anastomose with the pulmonary artery at the precapillary level and that this expanded blood flow participates in gas exchange at the alveolar level. These findings suggest that the major pathway of bronchial flow in these patients is via a bronchial artery to pulmonary artery to alveolar capillary route." While this may be so, the simultaneous existence of many anastomoses between the bronchial artery and pulmonary vein and between the bronchial artery and alveolar capillaries implies that respiratory exchange and a major blood flow pattern could exist via either of two routes: (1) bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery or (2) bronchial artery to alveolar capillary to pulmonary artery. Indeed, Liebow and colleagues" showed that Diodrast, injected into the bronchial arteries, opacifies the pulmonary veins before the pulmonary arteries. In this study, PRPA oxygen tension during bypass was as much as 200 mm. Hg higher than arterialized blood flowing directly from the heart-lung machine. Since the lungs of the patients were filled with 100 per cent oxygen, such degrees of pulmonary artery oxygenation could have been achieved only via reverse pulmonary blood flow with alveolar oxygen uptake, probably from either a bronchial artery to pulmonary vein to alveolar capillary to pulmonary artery route or a bronchial artery to alveolar capillary to pulmonary artery route. Although suction from the aspiration of
Volume 66
Reverse alveolar circulation
Number 1 July, 1973
blood through the PRPA catheter could artificially cause a reverse alveolar blood flow by decreasing pulmonary artery pressure below that of the left atrium, we doubt that this occurred, for the suction required to fill the syringe and the volume of blood taken at each sampling (3 ml.) were minimal. Changing the lung-inflating gas from 100 per cent oxygen to 100 per cent nitrous oxide resulted in a progressive decrease of PRP A oxygen tensions to levels below those of arterial blood, confirming that alveolar gas exchange was the mechanism by which PRPA oxygen tensions were being changed, Because of many unknowns-i.e., blood volume in the right lung, the flow rate of bronchial artery blood directly into the pulmonary artery via precapillary anastomosis with the latter, and the flow rates of venous drainage away from the lung-it is impossible to estimate what fraction of the total bronchial artery flow traveled in a reverse direction to normal at the alveolar-capillary level. It is easy to see, however, that this is an intrinsically more efficient means of oxygen transfer in cyanotic congenital heart disease: It necessitates a double exposure of such blood to the alveolar air sacs, a backward flow past the alveoli to the pulmonary artery, and then a second exposure to the alveoli when the blood returns to the left heart. At present, it is difficult to say whether this type of flow actually occurs in the patient with cyanotic congenital heart disease when he is' neither anesthetized nor on heart-lung bypass. However, these stud-
19
ies do demonstrate that the capacity for reverse circulation with oxygenation does exist in these patients and suggests that this type of circulation may help to increase arterial oxygen saturation for them.
REFERENCES
2 3 4
5
6 7 8
9 10
Houle, D. B., Campbell, G. S., and Visscher, M. B.: Retrograde and Forward Perfusion of Isolated Canine Lung Lobes, Proc. Soc. Exp. BioI. Med. 97: 892, 1958. Stanley, T. H.: Unpublished data. Bing, R. J., Vandam, L. D., and Gray, F. D.: Physiological Studies in Congenital Heart Disease, Johns Hopkins Med. J. 80: 121, 1947. Landrigan, P. R., Purkis, I. E., Roy, D. E., and Cudkowicz, L.: Cardio-respiratory Studies in a Patient With an Absent Left Pulmonary Artery, Thorax 18: 77, 1963. Liebow, A. A., Hales, M. R., and Bloomer, W. E.: Relation of Bronchial to Pulmonary Vascular Tree, in Adams, W. R., and Veith, I., editors: Pulmonary Circulation, New York, 1958, Grune & Stratton, Inc. Fontan, F., and Baudet, E.: Surgical Repair of Tricuspid Atresia, Thorax 26: 240, 1971. Hutchin, P., Terzi, R. G. G., and Peters, R. M.: Bronchial-Pulmonary Artery Reverse Flow, Ann. Thorac. Surg. 4: 391, 1967. Alley, R. D., Stranahan, A., Kausel, H., Formel, P., and Van Mierop, L. H. S.: Demonstration of Bronchial-Pulmonary Artery Reverse Flow in Suppurative Pulmonary Disease, Clin. Res. 6: 41, 1958. Cudkowicz, L., and Armstrong, J. 8.: The Blood Supply of Malignant Pulmonary Neoplasms, Thorax 8: 152, 1953. Hanes, P., and Heath, D.: The Human Pulmonary Circulation, Baltimore, 1962, The Williams & Wilkins Company.