Diagnostic Radiology
branch to the apical segment of the right upper lobe which was not visualized. The capillary phase showed lack of perfusion in this segment. There was normal pulmonary venous return to the left atrium. In the levo phase the pulmonary artery branch to the right apex, observed on coronary arteriography to arise from the left circumflex artery, was visualized. A lung scan also showed lack of perfusion in the apical segment of the right upper lobe. At surgery the bronchial artery arising from the left circumflex artery was isolated; it was noted to anastomose with the segmental pulmonary artery to the apical segment of the right upper lobe, which was ligated. The patient recovered uneventfully, and experienced a dramatic disappearance of his angina. A follow-up radiograph revealed infarction of the right apical pulmonary segment. The patient refused recatheterization.
Pulmonary Steal Syndrome: An Unusual Case of Coronary-Bronchial Pulmonary Artery Communication 1 Hugo Spindola-Franco, M.D., Arthur Weisel, M.D., and Abner J. Delman, M.D. The authors report a patient with angina pectoris in whom selective left coronary angiography demonstrated that the pulmonary artery branch to an apical lung segment was supplied by a bronchial collateral vessel which arose from the left circumflex artery. The anatomic and physiological developmental mechanisms, and the clinical implications, are discussed. Relief of the patient's angina following ligation of the pulmonary artery branch indicated the development of a form of pulmonary steal syndrome. INDEX TERMS: Arteries, bronchial. (Coronary artery, fistula communicating with pulmonary artery, 5 [ 4].1843) • Coronary vessels. Pulmonary arteries, abnormalities
DISCUSSION
Anastomoses between the coronary arteries and extracardiac vessels have been recognized since the beginning of the nineteenth century (1). These include anastomoses with bronchial, internal mammary, pericardial and anterior mediastinal arteries as well as superior and inferior phrenic, intercostal and esophageal branches of the aorta. Moberg (2) demonstrated connections between the bronchial and coronary arteries in all subjects, regardless of age and independent of atherosclerosis. These pathways usually become functionally significant only when a gradient exists between the two arterial systems, generally associated with arteriosclerotic coronary artery disease which may produce a pressure gradient, causing blood flow from the bronchial to the coronary arteries (3). These anastomotic pathways may also become functionally significant in an opposite direction in patients with pulmonary disease (4). Viamonte et al. (5) suggested that decreased perfusion in the bronchial vascular bed is a response to tumor or inflammation in the bronchial wall, producing decreased pressure in the bronchial system and reversed blood flow from coronary to bronchial arteries. Another mechanism for increased blood flow through the bronchial collateral vessels is demonstrated in this patient. The demonstrated malformation of a pulmonary artery branch to a single pulmonary segment, with no evidence of continuity between the main pulmonary artery and the otherwise normally formed branch vessel, may represent an isolated congenital anomaly. It also may have developed secondary to a localized intrauterine or acquired pulmonary infection. Embryologically, such an isolated congenital malformation of the pulmonary arterial system can be explained by a localized defect in the development of a distal segment of one of the paired sixth aortic arches which produce the pulmonary arterial branches. An infectious process could produce the same result byc causing inflammation, stenosis and eventually occlusion of a segmental pulmonary artery. The result in either case would be decreased perfusion pressure in the pulmonary vascular bed of the affected pulmonary segment. A pressure gradient would then exist between the bronchial arterial system and the pulmonary vascular bed. The rich anastomotic system between the coronary and bronchial vessels (2, 3, 6, 7), and between the bronchial and pulmonary vessels (bronchopulmonary anastomoses) (8), may be responsible for blood flow from a higher pressure coronary arterial system to a lower pressure pulmonary arterial system,
Radiology 126:25-27, January 1978
collateral pathway from the left circumflex coronary artery to the pulmonary artery branch supplying the apical segment of the right upper lobe via a bronchial artery, was demonstrated by selective left coronary angiography (Fig. 1) in a patient with typical angina. Lack of direct perfusion of this lung segment by the pulmonary arterial circulation was confirmed by radionuclide lung scan and pulmonary angiography (Fig. 2). The patient's angina disappeared following ligation of the pulmonary artery branch. We present developmental mechanisms for both the demonstrated collateral pathway and the form of pulmonary steal syndrome which could explain the angina pectoris.
A
CASE REPORT A 53-year-old hypertensive man was admitted for evaluation of angina (relieved by nitroglycerin) of increasing frequency and severity of four years' duration. Other drug therapy for the angina and hypertension was also used, e.g., Inderal, Aldomet. The only significant abnormality discovered on the admission examination was a grade IIVI systolic murmur at the lower left sternal border. A chest radiograph was normal (Fig. 3). Electrocardiographic changes were compatible with a previous inferior wall infarction. Cardiac catheterization revealed the left ventricular end diastolic pressure to be moderately elevated both pre- (22-24 mm Hg) and postangiography (21-24 mm Hg). Ventricular and aortic valve systolic gradients were absent. The post premature ventricular contraction response was normal. The cardiac index was 3.2 L/min/m 2 . Biplane left ventriculography revealed a mildly hyperkinetic ventricle. The papillary muscles were hypertrophied. There was no evidence of mitral insufficiency. Ventriculographic analysis showed: ejection fraction 79.800%; LV volume 112.633 ml; stroke volume 89.881 ml; stroke volume index 44.973 ml/rn'', Selective coronary opacification (Fig. 1) revealed minimal atherosclerotic changes in the mid left anterior descending artery. The left circumflex artery proper was small and nondominant. The left atrial circumflex branch gave rise to a tortuous vessel which anastomosed with the pulmonary arterial branch supplying the apical segment of the right upper lobe. An area of stenosis was present at the site of the anastomosis. We felt that the vessel arising from the left circumflex artery was a variety of bronchial artery providing collateral flow from the coronary arterial system to the pulmonary artery branch. Insignificant nonobstructive changes were seen in the right coronary artery. A pulmonary angiogram was then performed (Fig. 2); the pulmonary artery and its branches were normal, except for the pulmonary artery
~om the Departments of Radiology and Medicine (Cardiology), Montefiore Hospital and Medical Center, Albert Einstein College of Medicine of Yeshiva University. Accepted for publication in June 1977. emt
25
26
HUGO SPINDOLA-FRANCO AND OTHERS
via a bronchial collateral pathway. This is a tenable explanation for the hemodynamics in our patient. It is unlikely that the right pulmonary apical segment in our patient represents a form of pulmonary sequestration. The systemic arterial supply and the venous drainage via the pulmonary veins are typical of intralobar sequestration. However, even in the absence of confirmation of normal bronchial struc-
January 1978
tures, it is believed that sequestration is unlikely on the basis of the normal pulmonary arterial branching pattern in the pulmonary segment, its apical location, and the coronary to bronchial arterial pathways supplying it. Examples of communications between the coronary arteries and the pulmonary circulation are well documented. In all but one case the communications are from the coronary arteries
Fig. 1. Selective left coronary angiogram. A. Nonsubtracted angiogram shows a large left atrial circumflex artery communicating with the apical pulmonary artery branch of right upper lobe, via a bronchial collateral. B. Subtracted angiogram clearly shows the coronary bronchial anastomosis (arrow) and the pulmonary bronchial anastomosis (arrow). Note the large caliber of the left atrial circumflex artery compared to the left anterior descending artery.
Fig. 2. Pulmonary angiogram fails to opacify the apical pulmonary artery branch which opacified during left coronary angiography.
Fig. 3. Chest radiograph shows retrospectively a large vessel to the apical segment of the right upper lobe (arrows).
Vol. 126
27
PULMONARY STEAL SYNDROME
to either the main pulmonary trunk or to a cardiac chamber; these direct communications have been referred to as coronary arteriovenous fistulae. In the single exception (9), a communication is demonstrated between the left coronary artery and a peripheral branch of the right pulmonary artery. Examination of the patient's coronary angiogram reveals a long, tortuous vessel arising from a branch of the left coronary artery, and ending in a peripheral pulmonary arterial branch supplying an inferior segment of the right lower lobe. An area of stenosis is noted in the tortuous vessel at its junction with the pulmonary artery (bronchopulmonary anastomosis). These findings are reminiscent of our own; both cases show unusual coronary to bronchial to pulmonary arterial collateral pathways, rather than direct communications. This pathway deserves recognition as a distinct entity, separate from coronary arteriovenous fistula, and probably of a different etiology. The shunting of blood from the coronary to the pulmonary circulation, directly (coronary to main pulmonary trunk) or indirectly (coronary to bronchial to pulmonary arterial branch), produces a "pulmonary steal syndrome", a term which describes specifically a shunting of blood from the coronary to the pulmonary circulation. This differs from a coronary steal, in which blood is diverted from one myocardial compartment to another (10, 11), and is also to be differentiated from a "bronchial steal", observed in patients with pulmonary inflammatory disease, in which blood is shunted from a coronary artery to the bronchial circulation (4). A pulmonary steal could decrease myocardial perfusion, resulting in ischemic changes in the myocardium supplied by the involved coronary artery. Therefore, surgical ligation of such a demonstrated shunt pathway appears justified for the symptomatic relief of chest pain, if no other cause for angina can be demonstrated. The disappearance of angina in our patient, following ligation of the involved segmental pulmonary artery, strongly supports the pulmonary steal hypothesis.
Diagnostic Radiology
REFERENCES 1. Von Haller A: First lines of physiology. 1st American Edition, p 35, 1803. Wearn JT, Harvey Lecture, 243-270,1939-1940. (Cited by Moberg A. Anastomoses between extracardiac vessels and coronary arteries.) Acta Med Scand (Suppl. 485):5-26, Stockholm 1968 2. Moberg A: Anastomoses between extracardiac vessels and coronary arteries. I. Via bronchial arteries. II. Via internal mammary arteries. Acta Radiol Diag 6:177-192,263-272, Mar-May 1967 3. Bjork L: Angiographic demonstration of extracardial anastomoses to the coronary arteries. Radiology 87:274-277, Aug 1966 4. Smith SC, Adams DF, Herman MV, et al: Coronary-to-bronchial anastomoses: an in vivo demonstration by selective coronary arteriography. Radiology 104:289-290, Aug 1972 5. Viamonte M Jr, Parks RE, Smoak WM III: Guided catheterization of the bronchial arteries. Radiology 85:205-229, Aug 1965 6. Petelenz T: Extracoronary shunts with coronary arteries in man. Cardiologia 47:323-336. 1965 7. Bjork L: Anastomoses between the coronary and bronchial arteries. Acta Radiol (Diag) 4:93-96, Jan 1966 8. Pump KK: Distribution of bronchial arteries in the human lung. Chest 62:447-451, Oct 1972 9. Macchi RJ. Fabregas RA, Chianelli HO, et al: Anomalous communication of the left coronary artery with a peripheral branch of the right pulmonary artery. Chest 69:565-568, Apr 1976 10. Winburg MM, Howe BB. Weis HR: Effect of nitroglycerin and dipyridamole on epicardial and endocardial oxygen tension-Further evidence for redistribution of myocardial blood flow. J Pharmacol Exper Therap 176:184-199, Jan 1971 11. Spindola-Franco H, Codini MA: Paradoxical effect of nitroglycerin on left ventricular wall motion in coronary artery disease. Invest Radiol 11:392, Sep-Oct 1976
Hugo Spindola-Franco,M.D. Montefiore Hospital and Medical Center 111 East 21Oth Street Bronx, New York, N.Y. 10467
branch to the apical segment of the right upper lobe which was not visualized. The capillary phase showed lack of perfusion in this segment. There was normal pulmonary venous return to the left atrium. In the levo phase the pulmonary artery branch to the right apex, observed on coronary arteriography to arise from the left circumflex artery, was visualized. A lung scan also showed lack of perfusion in the apical segment of the right upper lobe. At surgery the bronchial artery arising from the left circumflex artery was isolated; it was noted to anastomose with the segmental pulmonary artery to the apical segment of the right upper lobe, which was ligated. The patient recovered uneventfully, and experienced a dramatic disappearance of his angina. A follow-up radiograph revealed infarction of the right apical pulmonary segment. The patient refused recatheterization.
Pulmonary Steal Syndrome: An Unusual Case of Coronary-Bronchial Pulmonary Artery Communication 1 Hugo Spindola-Franco, M.D., Arthur Weisel, M.D., and Abner J. Delman, M.D. The authors report a patient with angina pectoris in whom selective left coronary angiography demonstrated that the pulmonary artery branch to an apical lung segment was supplied by a bronchial collateral vessel which arose from the left circumflex artery. The anatomic and physiological developmental mechanisms, and the clinical implications, are discussed. Relief of the patient's angina following ligation of the pulmonary artery branch indicated the development of a form of pulmonary steal syndrome. INDEX TERMS: Arteries, bronchial. (Coronary artery, fistula communicating with pulmonary artery, 5 [ 4].1843) • Coronary vessels. Pulmonary arteries, abnormalities
DISCUSSION
Anastomoses between the coronary arteries and extracardiac vessels have been recognized since the beginning of the nineteenth century (1). These include anastomoses with bronchial, internal mammary, pericardial and anterior mediastinal arteries as well as superior and inferior phrenic, intercostal and esophageal branches of the aorta. Moberg (2) demonstrated connections between the bronchial and coronary arteries in all subjects, regardless of age and independent of atherosclerosis. These pathways usually become functionally significant only when a gradient exists between the two arterial systems, generally associated with arteriosclerotic coronary artery disease which may produce a pressure gradient, causing blood flow from the bronchial to the coronary arteries (3). These anastomotic pathways may also become functionally significant in an opposite direction in patients with pulmonary disease (4). Viamonte et al. (5) suggested that decreased perfusion in the bronchial vascular bed is a response to tumor or inflammation in the bronchial wall, producing decreased pressure in the bronchial system and reversed blood flow from coronary to bronchial arteries. Another mechanism for increased blood flow through the bronchial collateral vessels is demonstrated in this patient. The demonstrated malformation of a pulmonary artery branch to a single pulmonary segment, with no evidence of continuity between the main pulmonary artery and the otherwise normally formed branch vessel, may represent an isolated congenital anomaly. It also may have developed secondary to a localized intrauterine or acquired pulmonary infection. Embryologically, such an isolated congenital malformation of the pulmonary arterial system can be explained by a localized defect in the development of a distal segment of one of the paired sixth aortic arches which produce the pulmonary arterial branches. An infectious process could produce the same result byc causing inflammation, stenosis and eventually occlusion of a segmental pulmonary artery. The result in either case would be decreased perfusion pressure in the pulmonary vascular bed of the affected pulmonary segment. A pressure gradient would then exist between the bronchial arterial system and the pulmonary vascular bed. The rich anastomotic system between the coronary and bronchial vessels (2, 3, 6, 7), and between the bronchial and pulmonary vessels (bronchopulmonary anastomoses) (8), may be responsible for blood flow from a higher pressure coronary arterial system to a lower pressure pulmonary arterial system,
Radiology 126:25-27, January 1978
collateral pathway from the left circumflex coronary artery to the pulmonary artery branch supplying the apical segment of the right upper lobe via a bronchial artery, was demonstrated by selective left coronary angiography (Fig. 1) in a patient with typical angina. Lack of direct perfusion of this lung segment by the pulmonary arterial circulation was confirmed by radionuclide lung scan and pulmonary angiography (Fig. 2). The patient's angina disappeared following ligation of the pulmonary artery branch. We present developmental mechanisms for both the demonstrated collateral pathway and the form of pulmonary steal syndrome which could explain the angina pectoris.
A
CASE REPORT A 53-year-old hypertensive man was admitted for evaluation of angina (relieved by nitroglycerin) of increasing frequency and severity of four years' duration. Other drug therapy for the angina and hypertension was also used, e.g., Inderal, Aldomet. The only significant abnormality discovered on the admission examination was a grade IIVI systolic murmur at the lower left sternal border. A chest radiograph was normal (Fig. 3). Electrocardiographic changes were compatible with a previous inferior wall infarction. Cardiac catheterization revealed the left ventricular end diastolic pressure to be moderately elevated both pre- (22-24 mm Hg) and postangiography (21-24 mm Hg). Ventricular and aortic valve systolic gradients were absent. The post premature ventricular contraction response was normal. The cardiac index was 3.2 L/min/m 2 . Biplane left ventriculography revealed a mildly hyperkinetic ventricle. The papillary muscles were hypertrophied. There was no evidence of mitral insufficiency. Ventriculographic analysis showed: ejection fraction 79.800%; LV volume 112.633 ml; stroke volume 89.881 ml; stroke volume index 44.973 ml/rn'', Selective coronary opacification (Fig. 1) revealed minimal atherosclerotic changes in the mid left anterior descending artery. The left circumflex artery proper was small and nondominant. The left atrial circumflex branch gave rise to a tortuous vessel which anastomosed with the pulmonary arterial branch supplying the apical segment of the right upper lobe. An area of stenosis was present at the site of the anastomosis. We felt that the vessel arising from the left circumflex artery was a variety of bronchial artery providing collateral flow from the coronary arterial system to the pulmonary artery branch. Insignificant nonobstructive changes were seen in the right coronary artery. A pulmonary angiogram was then performed (Fig. 2); the pulmonary artery and its branches were normal, except for the pulmonary artery
~om the Departments of Radiology and Medicine (Cardiology), Montefiore Hospital and Medical Center, Albert Einstein College of Medicine of Yeshiva University. Accepted for publication in June 1977. emt
25
26
HUGO SPINDOLA-FRANCO AND OTHERS
via a bronchial collateral pathway. This is a tenable explanation for the hemodynamics in our patient. It is unlikely that the right pulmonary apical segment in our patient represents a form of pulmonary sequestration. The systemic arterial supply and the venous drainage via the pulmonary veins are typical of intralobar sequestration. However, even in the absence of confirmation of normal bronchial struc-
January 1978
tures, it is believed that sequestration is unlikely on the basis of the normal pulmonary arterial branching pattern in the pulmonary segment, its apical location, and the coronary to bronchial arterial pathways supplying it. Examples of communications between the coronary arteries and the pulmonary circulation are well documented. In all but one case the communications are from the coronary arteries
Fig. 1. Selective left coronary angiogram. A. Nonsubtracted angiogram shows a large left atrial circumflex artery communicating with the apical pulmonary artery branch of right upper lobe, via a bronchial collateral. B. Subtracted angiogram clearly shows the coronary bronchial anastomosis (arrow) and the pulmonary bronchial anastomosis (arrow). Note the large caliber of the left atrial circumflex artery compared to the left anterior descending artery.
Fig. 2. Pulmonary angiogram fails to opacify the apical pulmonary artery branch which opacified during left coronary angiography.
Fig. 3. Chest radiograph shows retrospectively a large vessel to the apical segment of the right upper lobe (arrows).
Vol. 126
27
PULMONARY STEAL SYNDROME
to either the main pulmonary trunk or to a cardiac chamber; these direct communications have been referred to as coronary arteriovenous fistulae. In the single exception (9), a communication is demonstrated between the left coronary artery and a peripheral branch of the right pulmonary artery. Examination of the patient's coronary angiogram reveals a long, tortuous vessel arising from a branch of the left coronary artery, and ending in a peripheral pulmonary arterial branch supplying an inferior segment of the right lower lobe. An area of stenosis is noted in the tortuous vessel at its junction with the pulmonary artery (bronchopulmonary anastomosis). These findings are reminiscent of our own; both cases show unusual coronary to bronchial to pulmonary arterial collateral pathways, rather than direct communications. This pathway deserves recognition as a distinct entity, separate from coronary arteriovenous fistula, and probably of a different etiology. The shunting of blood from the coronary to the pulmonary circulation, directly (coronary to main pulmonary trunk) or indirectly (coronary to bronchial to pulmonary arterial branch), produces a "pulmonary steal syndrome", a term which describes specifically a shunting of blood from the coronary to the pulmonary circulation. This differs from a coronary steal, in which blood is diverted from one myocardial compartment to another (10, 11), and is also to be differentiated from a "bronchial steal", observed in patients with pulmonary inflammatory disease, in which blood is shunted from a coronary artery to the bronchial circulation (4). A pulmonary steal could decrease myocardial perfusion, resulting in ischemic changes in the myocardium supplied by the involved coronary artery. Therefore, surgical ligation of such a demonstrated shunt pathway appears justified for the symptomatic relief of chest pain, if no other cause for angina can be demonstrated. The disappearance of angina in our patient, following ligation of the involved segmental pulmonary artery, strongly supports the pulmonary steal hypothesis.
Diagnostic Radiology
REFERENCES 1. Von Haller A: First lines of physiology. 1st American Edition, p 35, 1803. Wearn JT, Harvey Lecture, 243-270,1939-1940. (Cited by Moberg A. Anastomoses between extracardiac vessels and coronary arteries.) Acta Med Scand (Suppl. 485):5-26, Stockholm 1968 2. Moberg A: Anastomoses between extracardiac vessels and coronary arteries. I. Via bronchial arteries. II. Via internal mammary arteries. Acta Radiol Diag 6:177-192,263-272, Mar-May 1967 3. Bjork L: Angiographic demonstration of extracardial anastomoses to the coronary arteries. Radiology 87:274-277, Aug 1966 4. Smith SC, Adams DF, Herman MV, et al: Coronary-to-bronchial anastomoses: an in vivo demonstration by selective coronary arteriography. Radiology 104:289-290, Aug 1972 5. Viamonte M Jr, Parks RE, Smoak WM III: Guided catheterization of the bronchial arteries. Radiology 85:205-229, Aug 1965 6. Petelenz T: Extracoronary shunts with coronary arteries in man. Cardiologia 47:323-336. 1965 7. Bjork L: Anastomoses between the coronary and bronchial arteries. Acta Radiol (Diag) 4:93-96, Jan 1966 8. Pump KK: Distribution of bronchial arteries in the human lung. Chest 62:447-451, Oct 1972 9. Macchi RJ. Fabregas RA, Chianelli HO, et al: Anomalous communication of the left coronary artery with a peripheral branch of the right pulmonary artery. Chest 69:565-568, Apr 1976 10. Winburg MM, Howe BB. Weis HR: Effect of nitroglycerin and dipyridamole on epicardial and endocardial oxygen tension-Further evidence for redistribution of myocardial blood flow. J Pharmacol Exper Therap 176:184-199, Jan 1971 11. Spindola-Franco H, Codini MA: Paradoxical effect of nitroglycerin on left ventricular wall motion in coronary artery disease. Invest Radiol 11:392, Sep-Oct 1976
Hugo Spindola-Franco,M.D. Montefiore Hospital and Medical Center 111 East 21Oth Street Bronx, New York, N.Y. 10467
