RADIOLOGY Coronary Neovascularity and Fistula Formation A Sign of Mural Thrombus RENATE L. SOULEN, M.D., JULIUS H. GROLLMAN, JR., M.D., DONALD PAGLIA, M.D., AND THOMAS KREULEN, M.D. SUMMARY Fifteen patients have shown neovascularity in the left heart during selective coronary arteriography, with associated fistulous communication to a cardiac chamber in ten. In nine the abnormalities were adjacent to and within ventricular mural thrombi, associated with ventricular aneurysms in seven and congestive cardiomyopathy in two. In six patients with mitral stenosis and atrial fibrillation the angiographic changes related to left atrial thrombi.
Histologic study of two atrial thrombi showed revascularization patterns in keeping both with the angiographic findings and with an intermediate stage in the evolution of mural thrombus. Though myxomas can produce a similar appearance, clinical and additional angiographic features should permit differentiation in most instances between this infrequent tumor and the far more common mural thrombus.
CORONARY NEOVASCULARITY and fistula formation are infrequent abnormalities usually attributed to neoplasm and congenital anomaly, respectively. Our experience with fifteen patients indicates that mural thrombus may stimulate both these abnormalities, and that they may be demonstrated by selective coronary arteriography and confirmed histologically.
with the atrial chamber (fig. 1) was associated in five, with sufficient contrast medium entering the chamber to outline filling defects in four patients; angiographic diagnosis of thrombus was inferential in the remaining two. The key angiographic findings in this group are summarized in table 3. Four of these six patients have come to surgery and the presence of thrombus was confirmed in each. Detailed histologic studies were made of the thrombus in two patients; the other specimens were not examined beyond confirming the thrombotic nature of the clot and excluding myxoma. Histologic sections through the left atrial appendage of one of these patients (fig. 2) revealed fenestration of the lumen by interconnecting septa composed of mature collagenous fibrous tissue.These septa enclosed channels of varying size which were lined by distinct endothelium and were interpreted as representing complete organization and recanalization of a mural thrombus. The excised mural thrombus of another patient was grossly semi-gelatinous with an outer surface which was irregular, granular and variegated red and tan. The cut surface had a pitted appearance with irregular laminations (fig. 3). Microscopically, it consisted almost entirely of acellular proteinaceous material, with a fibrillar pattern in some areas, which was undergoing peripheral organization. Electron microscopy demonstrated only fibrin. Proliferative fibroblasts, capillaries, and mature vessels penetrated well into the fibrinous mass (fig. 4). In addition to these vessels, a large portion of the thrombus was fenestrated by numerous irregular and fusiform channels which lacked endothelial lining cells but frequently contained fresh blood (fig. 5). Neither stellate cells nor histochemical reactions suggestive of myxoma were apparent.
Material Fifteen patients have shown neovascularity in the left heart during selective coronary arteriography, with associated fistulous communications to a cardiac chamber in ten. The clinical diagnosis and evidence for mural thrombus in each of these patients is summarized in table 1. Nine patients exhibited abnormal vascular blushing in the left ventricle during coronary arteriography. Ventriculography demonstrated filling defects, consistent with mural thrombus, in the same area as the blush in eight of these. Mural thrombus was not identified with certainty in the single plane right anterior oblique ventriculogram of the remaining patient whose vascular blush occurred in the region of a posterior aneurysm. Seven patients had ventricular aneurysms while two had congestive cardiomyopathy. In five patients a fistulous communication with the left ventricular cavity was associated with abnormal vascularization of portions of the filling defect. The key angiographic findings in these patients are listed in table 2. Surgical proof of mural thrombus was available only in a patient with massive embolus to the aortic bifurcation. Unfortunately, no histologic studies of the clot were obtained. Six patients, all with mitral stenosis and atrial fibrillation, demonstrated neovascularity and blushes in the region of the left atrium and/or its appendage. Fistulous communication
Discussion Radiologically demonstrable neovascularity is a well recognized feature of many neoplasms and, less frequently, of inflammatory masses and reparative processes. It is the granulation tissue of the latter two which produces the new vessels with hypervascularity in the arterial phase, and blushes or stains during the capillary and venous phases of angiography.1 The histologic evolution of mural thrombi has been extensively studied by Mitchell and Schwartz2 and,
From the Departments of Radiology and Medicine, Temple University Health Sciences Center, Philadelphia, Pennsylvania and the Departments of Radiological Sciences and Pathology, UCLA Center for the Health Sciences, Los Angeles, California. Presented in part at the 48th annual Scientific Session of the American Heart Association, Anaheim, California, 1975. Address for reprints: Renate L. Soulen, M.D., Department of Radiology, Temple University Health Sciences Center, Philadelphia, Pennsylvania. Received May 4, 1977; revision accepted May 30, 1977. 663
CIRCULATION
664
TABLE 1. Fifteen Patients with Neovascularization Attributed to Thrombus Total
nurnber
Diagnosis
Left ventricular aneurysm Congestive cardiomyopathy Mitral stenosis with atrial fibrillation
Evidence for presence of thrombus
of patients Embolization
Angiographic filling defect Surgery
7
2
6
1
2
0
2
0
6
5
4
4
VOL 56, No 4, OCTOBER 1977
more recently, by Salyer and his associates.3 Both groups describe an initial stage of platelet and leukocyte rich masses, an intermediate stage of invasion by vascular channels and mesenchymal cells from the underlying endocardium, and a late stage of collagen and elastic fiber formation as the thrombus is converted to a thick fibrous plaque covered with endothelium. Farrer-Brown, in microradiographs of postmortem specimens injected with contrast medium, demonstrated the neovascularity of such granulation tissue extending from the trabeculae carneae into mural thrombus.' It is, therefore, reasonable to expect that selective coronary arteriography might also demonstrate these
FIGURE 1. Selective coronary arteriograms in a patient with surgically confirmed large left atrial thrombus. A) Selective left coronary injection in slight RA 0 showing neovascularity (curved arrow) and beginning pooling (white arrow) in the left atrium and blush within the left atrial appendage (black arrow). B) Later frame of same injection showing persistent blush and pooling. C) Selective right coronary injection in steeper RA 0 showing early puddling of contrast within the left atrium from enlarged atrial branches (arrows). D) Later frame from same injection with pooled contrast outlining a large irregular filling defect (arrows).
CORONARY NEOVASCULARITY IN THROMBUS/Soulen et al. TAB3LE 2. Angiographic Fiindings in Patients with Ventricular AVeovascularization Left ventriculogram
Patient
1. 34 M
2. 68 M 3. 47 F 4. 36 F 5. 63 F 6. 73 M
7. 54 M
Coronary arteriogram
Enlarged, diffusely hypo- AN and F; otherwise
kinetic; apical clot Enlarged, diff usely hypokinetic; apical clot Aiiterolateral arid apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral anid apical aneurysm with apical clot Aniterolateral arid apical aneurysm with apical clot Posterior aneurysm
TABLE 3. Angiographic Findings in Patients with Left Atrial
Neovascularization Patient
4. 63 F 5. 65 F
Atrial branch LCA
6. 58 F
Atrial branch LCA
2. 57 F
AN and F; LAD stenosis
3. 59 F
AN and F; LAD occlusion
Coronary supply
Atrial branches of both RCA and LCA Atrial branches of both RCA and LCA Atrial branches of both RCA and LCA Atrial branch LCA
1. 72 F
normal AN; otherwise normal
AN and F; LAD stenosis
Abbreviations: N neovascularity; RCA LCA left coronary artery; F fistula; LA\ auricular appendage. =
=
AN; LAD occlusion
665
=
Abnormalities shown
N and F in LA and LAA N and F in LA and LAA N, blush, and F in LA N, blush, and F in LAA N, blush, and F in LAA N and blush in LA rigIt
coronary artery;
left atrium; LAA
=
left
AN; LAD stenosis and occlusion
changes and that this intermediate stage of mural thrombus evolution will be seen more frequently as the performance of coronary arteriography continues to increase. The histologic appearance of our cases is in agreement with this concept. Salyer describes extension of mural thrombus material into Thebesian veins draining into the chambers. Granulation tissue within and recanalization of such thrombus may account for the fistulous communication demonstrated in 10 of our 15 patients. One would not expect such angiographic changes in either the early or late stages, which could explain the many thrombi seen only as filling defects within a cardiac chamber, particularly the left ventricle.
Indeed Grollman et al. first described coronary arteriographic evidence of neovascularity, blush and subsequent washout into the left ventricle in seven patients with mural thrombus associated with ventricular aneurysms5 and Standen reported similar changes in the left atrium of a patient with mitral stenosis, atrial fibrillation and a large atrial thrombus.6 However, "tumor vascularity" has also been reported in a left atrial myxoma7 and more recently we have seen a second such case. This is not surprising in light of the histologic similarity of myxomas and organizing thrombi.3' I The coronary arteriographic features do not distinguish these two lesions. Myxoma is characterized by mobility of the mass, a pedunculated configuration, and origin from the area of the fossa ovalis. An immobile filling defect which occludes the atrial appendage, particularly in a fibrillating patient with mitral stenosis, favors the diagnosis of thrombus. In addition to the markedly different clinical presentation, the neovascularity and fistulous communication seen in thrombi are distinguished from congenital coronary fistulae angiographically by the small size of the new vessels,
FIGURE 2. Low power cross-section of left atrial appendage, elastic stain. The dark band indicated by the arrows is the elastica of the endocardium. The atrial lumen is fenestrated by totally organized recanalized thrombus.
FIGURE 3. Cut surface of mural thrombus showing indistinct lines of Zahn and dark blood-filled channels.
8. 55 F
9. 73 M
AN and F; LAI) and OM stenoses
Posterior neovascularity; OM stenosis
Abbreviations: AN = apical neovascularity; LAD descending; F fistula; OM obtuse marginal.
=
left anterior
=
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VOL 56, No 4, OCTOBER 1977
AS
4~~~~~xa FIGURE 4. Organization of mural thrombus. A well en
dorhelialized. vsepn etaedepyiothfbrn sms.
FIGURE 5. Mural thrombus with many nonendothelialized channels containing fresh blood. An organizing vessel with maturing endothelium is indicated by the arrow.
predilection for left chambers, associated chamber filling defects with blushes, and absence of hemodynamically significant shunts. We believe thrombi account for the fistulae in two of the three patients reported by Arani et al.9 Coronary atherosclerosis per se has been proposed as a cause of acquired coronary fistula by King and Schoonmaker.'0 We have not seen neovascularity associated with coronary atherosclerosis in the absence of mural thrombus, and attribute the fistula in their patient to the large atrial thrombus found at surgery. The absence of coronary atherosclerosis in both our cases of congestive cardiomyopathy and in four of the patients with mitral disease also argues against such a pathogenesis. In conclusion, coronary arteriography in the presence of a mural thrombus may show neovascularity to the region of the thrombus, contrast blush within the thrombus, and fistulous communication with the cardiac chamber in which the thrombus adheres. These angiographic abnormalities correlate well with the histologic findings of penetration by vascular channels from the underlying endocardium and most likely represent an intermediate stage in the evolution of the thrombus. Although a myxoma can produce a similar appearance, clinical and additional angiographic findings should permit differentiation in most instances between this
infrequent tumor and the far more common mural thrombus.
References 1. Doppman JL, Fried LC, DiChiro G: Absent constrictive response of wound vessels to intra-arterial vasopressors: Angiographic observations. Radiology 93: 57, 1969 2. Mitchell JRA, Schwartz CJ: Arterial Disease. Oxford, Blackwell Scientific Publications Ltd, 1965, pp 151-154 3. Salyer WR, Page DL, Hutchins GM: The development of cardiac myxomas and papillary endocardial lesions from mural thrombus. Am Heart J 89: 4, 1975 4. Farrer-Brown G: Normal and diseased vascular pattern of myocardium of human heart. II. Pattern seen with fibrosis of the left ventricular free wall. Br Heart J 30: 537, 1968 5. Grollman JH Jr, Hoffman RB, Price JE Jr, O'Reilly RJ, Lilley JM, Herman NP: Abnormal vascularity in left ventricular mural thrombus demonstrated by selective coronary arteriography. Radiology 113: 591, 1974 6. Standen JR: "Tumor vascularity" in left atrial thrombus demonstrated by selective coronary arteriography. Radiology 116: 549, 1975 7. Marshall WH Jr, Steiner RM, Wexler L: "Tumor vascularity" in left atrial myxoma demonstrated by selective coronary arteriography. Radiology 93: 815, 1969 8. Salyer WR, Salyer DC: Myxoma-like features of organizing thrombi in arteries and veins Arch Pathol 99: 307, 1975 9* Arani DT, Greene DG, Klocke JJ: Coronary artery fistula emptying into left heart chambers. Circulation 54 (suppl 11): II-39, 1976 10. King SB III, Schoonmaker FW: Coronary artery to left atrial fistula in association with severe atherosclerosis and mitral stenosis: Report of surgical repair. Chest 67: 361, 1975
Histologic study of two atrial thrombi showed revascularization patterns in keeping both with the angiographic findings and with an intermediate stage in the evolution of mural thrombus. Though myxomas can produce a similar appearance, clinical and additional angiographic features should permit differentiation in most instances between this infrequent tumor and the far more common mural thrombus.
CORONARY NEOVASCULARITY and fistula formation are infrequent abnormalities usually attributed to neoplasm and congenital anomaly, respectively. Our experience with fifteen patients indicates that mural thrombus may stimulate both these abnormalities, and that they may be demonstrated by selective coronary arteriography and confirmed histologically.
with the atrial chamber (fig. 1) was associated in five, with sufficient contrast medium entering the chamber to outline filling defects in four patients; angiographic diagnosis of thrombus was inferential in the remaining two. The key angiographic findings in this group are summarized in table 3. Four of these six patients have come to surgery and the presence of thrombus was confirmed in each. Detailed histologic studies were made of the thrombus in two patients; the other specimens were not examined beyond confirming the thrombotic nature of the clot and excluding myxoma. Histologic sections through the left atrial appendage of one of these patients (fig. 2) revealed fenestration of the lumen by interconnecting septa composed of mature collagenous fibrous tissue.These septa enclosed channels of varying size which were lined by distinct endothelium and were interpreted as representing complete organization and recanalization of a mural thrombus. The excised mural thrombus of another patient was grossly semi-gelatinous with an outer surface which was irregular, granular and variegated red and tan. The cut surface had a pitted appearance with irregular laminations (fig. 3). Microscopically, it consisted almost entirely of acellular proteinaceous material, with a fibrillar pattern in some areas, which was undergoing peripheral organization. Electron microscopy demonstrated only fibrin. Proliferative fibroblasts, capillaries, and mature vessels penetrated well into the fibrinous mass (fig. 4). In addition to these vessels, a large portion of the thrombus was fenestrated by numerous irregular and fusiform channels which lacked endothelial lining cells but frequently contained fresh blood (fig. 5). Neither stellate cells nor histochemical reactions suggestive of myxoma were apparent.
Material Fifteen patients have shown neovascularity in the left heart during selective coronary arteriography, with associated fistulous communications to a cardiac chamber in ten. The clinical diagnosis and evidence for mural thrombus in each of these patients is summarized in table 1. Nine patients exhibited abnormal vascular blushing in the left ventricle during coronary arteriography. Ventriculography demonstrated filling defects, consistent with mural thrombus, in the same area as the blush in eight of these. Mural thrombus was not identified with certainty in the single plane right anterior oblique ventriculogram of the remaining patient whose vascular blush occurred in the region of a posterior aneurysm. Seven patients had ventricular aneurysms while two had congestive cardiomyopathy. In five patients a fistulous communication with the left ventricular cavity was associated with abnormal vascularization of portions of the filling defect. The key angiographic findings in these patients are listed in table 2. Surgical proof of mural thrombus was available only in a patient with massive embolus to the aortic bifurcation. Unfortunately, no histologic studies of the clot were obtained. Six patients, all with mitral stenosis and atrial fibrillation, demonstrated neovascularity and blushes in the region of the left atrium and/or its appendage. Fistulous communication
Discussion Radiologically demonstrable neovascularity is a well recognized feature of many neoplasms and, less frequently, of inflammatory masses and reparative processes. It is the granulation tissue of the latter two which produces the new vessels with hypervascularity in the arterial phase, and blushes or stains during the capillary and venous phases of angiography.1 The histologic evolution of mural thrombi has been extensively studied by Mitchell and Schwartz2 and,
From the Departments of Radiology and Medicine, Temple University Health Sciences Center, Philadelphia, Pennsylvania and the Departments of Radiological Sciences and Pathology, UCLA Center for the Health Sciences, Los Angeles, California. Presented in part at the 48th annual Scientific Session of the American Heart Association, Anaheim, California, 1975. Address for reprints: Renate L. Soulen, M.D., Department of Radiology, Temple University Health Sciences Center, Philadelphia, Pennsylvania. Received May 4, 1977; revision accepted May 30, 1977. 663
CIRCULATION
664
TABLE 1. Fifteen Patients with Neovascularization Attributed to Thrombus Total
nurnber
Diagnosis
Left ventricular aneurysm Congestive cardiomyopathy Mitral stenosis with atrial fibrillation
Evidence for presence of thrombus
of patients Embolization
Angiographic filling defect Surgery
7
2
6
1
2
0
2
0
6
5
4
4
VOL 56, No 4, OCTOBER 1977
more recently, by Salyer and his associates.3 Both groups describe an initial stage of platelet and leukocyte rich masses, an intermediate stage of invasion by vascular channels and mesenchymal cells from the underlying endocardium, and a late stage of collagen and elastic fiber formation as the thrombus is converted to a thick fibrous plaque covered with endothelium. Farrer-Brown, in microradiographs of postmortem specimens injected with contrast medium, demonstrated the neovascularity of such granulation tissue extending from the trabeculae carneae into mural thrombus.' It is, therefore, reasonable to expect that selective coronary arteriography might also demonstrate these
FIGURE 1. Selective coronary arteriograms in a patient with surgically confirmed large left atrial thrombus. A) Selective left coronary injection in slight RA 0 showing neovascularity (curved arrow) and beginning pooling (white arrow) in the left atrium and blush within the left atrial appendage (black arrow). B) Later frame of same injection showing persistent blush and pooling. C) Selective right coronary injection in steeper RA 0 showing early puddling of contrast within the left atrium from enlarged atrial branches (arrows). D) Later frame from same injection with pooled contrast outlining a large irregular filling defect (arrows).
CORONARY NEOVASCULARITY IN THROMBUS/Soulen et al. TAB3LE 2. Angiographic Fiindings in Patients with Ventricular AVeovascularization Left ventriculogram
Patient
1. 34 M
2. 68 M 3. 47 F 4. 36 F 5. 63 F 6. 73 M
7. 54 M
Coronary arteriogram
Enlarged, diffusely hypo- AN and F; otherwise
kinetic; apical clot Enlarged, diff usely hypokinetic; apical clot Aiiterolateral arid apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral and apical aneurysm with apical clot Anterolateral anid apical aneurysm with apical clot Aniterolateral arid apical aneurysm with apical clot Posterior aneurysm
TABLE 3. Angiographic Findings in Patients with Left Atrial
Neovascularization Patient
4. 63 F 5. 65 F
Atrial branch LCA
6. 58 F
Atrial branch LCA
2. 57 F
AN and F; LAD stenosis
3. 59 F
AN and F; LAD occlusion
Coronary supply
Atrial branches of both RCA and LCA Atrial branches of both RCA and LCA Atrial branches of both RCA and LCA Atrial branch LCA
1. 72 F
normal AN; otherwise normal
AN and F; LAD stenosis
Abbreviations: N neovascularity; RCA LCA left coronary artery; F fistula; LA\ auricular appendage. =
=
AN; LAD occlusion
665
=
Abnormalities shown
N and F in LA and LAA N and F in LA and LAA N, blush, and F in LA N, blush, and F in LAA N, blush, and F in LAA N and blush in LA rigIt
coronary artery;
left atrium; LAA
=
left
AN; LAD stenosis and occlusion
changes and that this intermediate stage of mural thrombus evolution will be seen more frequently as the performance of coronary arteriography continues to increase. The histologic appearance of our cases is in agreement with this concept. Salyer describes extension of mural thrombus material into Thebesian veins draining into the chambers. Granulation tissue within and recanalization of such thrombus may account for the fistulous communication demonstrated in 10 of our 15 patients. One would not expect such angiographic changes in either the early or late stages, which could explain the many thrombi seen only as filling defects within a cardiac chamber, particularly the left ventricle.
Indeed Grollman et al. first described coronary arteriographic evidence of neovascularity, blush and subsequent washout into the left ventricle in seven patients with mural thrombus associated with ventricular aneurysms5 and Standen reported similar changes in the left atrium of a patient with mitral stenosis, atrial fibrillation and a large atrial thrombus.6 However, "tumor vascularity" has also been reported in a left atrial myxoma7 and more recently we have seen a second such case. This is not surprising in light of the histologic similarity of myxomas and organizing thrombi.3' I The coronary arteriographic features do not distinguish these two lesions. Myxoma is characterized by mobility of the mass, a pedunculated configuration, and origin from the area of the fossa ovalis. An immobile filling defect which occludes the atrial appendage, particularly in a fibrillating patient with mitral stenosis, favors the diagnosis of thrombus. In addition to the markedly different clinical presentation, the neovascularity and fistulous communication seen in thrombi are distinguished from congenital coronary fistulae angiographically by the small size of the new vessels,
FIGURE 2. Low power cross-section of left atrial appendage, elastic stain. The dark band indicated by the arrows is the elastica of the endocardium. The atrial lumen is fenestrated by totally organized recanalized thrombus.
FIGURE 3. Cut surface of mural thrombus showing indistinct lines of Zahn and dark blood-filled channels.
8. 55 F
9. 73 M
AN and F; LAI) and OM stenoses
Posterior neovascularity; OM stenosis
Abbreviations: AN = apical neovascularity; LAD descending; F fistula; OM obtuse marginal.
=
left anterior
=
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AS
4~~~~~xa FIGURE 4. Organization of mural thrombus. A well en
dorhelialized. vsepn etaedepyiothfbrn sms.
FIGURE 5. Mural thrombus with many nonendothelialized channels containing fresh blood. An organizing vessel with maturing endothelium is indicated by the arrow.
predilection for left chambers, associated chamber filling defects with blushes, and absence of hemodynamically significant shunts. We believe thrombi account for the fistulae in two of the three patients reported by Arani et al.9 Coronary atherosclerosis per se has been proposed as a cause of acquired coronary fistula by King and Schoonmaker.'0 We have not seen neovascularity associated with coronary atherosclerosis in the absence of mural thrombus, and attribute the fistula in their patient to the large atrial thrombus found at surgery. The absence of coronary atherosclerosis in both our cases of congestive cardiomyopathy and in four of the patients with mitral disease also argues against such a pathogenesis. In conclusion, coronary arteriography in the presence of a mural thrombus may show neovascularity to the region of the thrombus, contrast blush within the thrombus, and fistulous communication with the cardiac chamber in which the thrombus adheres. These angiographic abnormalities correlate well with the histologic findings of penetration by vascular channels from the underlying endocardium and most likely represent an intermediate stage in the evolution of the thrombus. Although a myxoma can produce a similar appearance, clinical and additional angiographic findings should permit differentiation in most instances between this
infrequent tumor and the far more common mural thrombus.
References 1. Doppman JL, Fried LC, DiChiro G: Absent constrictive response of wound vessels to intra-arterial vasopressors: Angiographic observations. Radiology 93: 57, 1969 2. Mitchell JRA, Schwartz CJ: Arterial Disease. Oxford, Blackwell Scientific Publications Ltd, 1965, pp 151-154 3. Salyer WR, Page DL, Hutchins GM: The development of cardiac myxomas and papillary endocardial lesions from mural thrombus. Am Heart J 89: 4, 1975 4. Farrer-Brown G: Normal and diseased vascular pattern of myocardium of human heart. II. Pattern seen with fibrosis of the left ventricular free wall. Br Heart J 30: 537, 1968 5. Grollman JH Jr, Hoffman RB, Price JE Jr, O'Reilly RJ, Lilley JM, Herman NP: Abnormal vascularity in left ventricular mural thrombus demonstrated by selective coronary arteriography. Radiology 113: 591, 1974 6. Standen JR: "Tumor vascularity" in left atrial thrombus demonstrated by selective coronary arteriography. Radiology 116: 549, 1975 7. Marshall WH Jr, Steiner RM, Wexler L: "Tumor vascularity" in left atrial myxoma demonstrated by selective coronary arteriography. Radiology 93: 815, 1969 8. Salyer WR, Salyer DC: Myxoma-like features of organizing thrombi in arteries and veins Arch Pathol 99: 307, 1975 9* Arani DT, Greene DG, Klocke JJ: Coronary artery fistula emptying into left heart chambers. Circulation 54 (suppl 11): II-39, 1976 10. King SB III, Schoonmaker FW: Coronary artery to left atrial fistula in association with severe atherosclerosis and mitral stenosis: Report of surgical repair. Chest 67: 361, 1975
