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Neuroradiology
Intracerebral Venous Angioma
1
Lyle R. Wendling, M.D.,2 James S. Moore, Jr., M.D., Stephen A. Kieffer, M.D.,3 Herbert I. Goldberg, M.D., and Richard E. Latchaw, M.D.4 Intracerebral venous angioma is a rare congenital vascular malformation of the brain. Three cases are reported, all of which had strikingly similar angiographic findings in the venous phase, viz., a local network of small medullary veins which converge centrally into a single large venous channel which courses transcerebrally to reach the superficial venous system. No gross abnormalities are seen in the arterial phase with the usual techniques. However, magnification delineated enlarged arterial branches supplying the periphery of the malformation in 2 of the 3 cases. A poorly marginated homogeneous blush and early filling of the draining veins were also seen in these 2 patients. The findings in the venous phase agree with those described in previous isolated case reports and appear to be highly suggestive of this rare malformation. INDEX TERMS: Angioma. Brain, abnormalities. Cerebral Angiography. Magnification • Malformations, arteriovenous Radiology 119:141-147, April 1976
is an unusual vascular malformation seldom found in the spinal cord and even more rarely in the brain. On both gross and microscopic anatomic examination, this lesion quite closely resembles the more common arteriovenous malformation, except that arteries are not to be found in increased number or size in the region of the malformation (9, 12). Angiographic demonstration of an intracerebral venous angioma was first reported by Wolf et a/. in 1967 (14), and only 3 other cases with angiographic evaluation have been described in the intervening years (2, 4, 5). We have recently encountered 3 patients in whom cerebral angiography demonstrated a unique appearance which may be highly suggestive of this rare malformation.
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CASE REPORTS CASE I. A 28-year-old black man was admitted to the Minneapolis Veterans Administration Hospital because of grand mal seizures one to two times per week over the past four years. Previous EEG and CSF studies were normal. On the day of admission, the patient had three grand mal seizures. General physical examination was unremarkable, but neurological examination revealed a mild left-sided hyperreflexia. Skull x rays were normal. The dynamic portion of a 99mTc brain scan demonstrated an early appearing area of increased radioactivity in the right inferior frontal region which seemed to drain into the superior sagittal sinus and wash out in the venous phase (Fig. 1, A). Static views were normal. A right common carotid angiogram (simultaneous biplane study, 1.8 times magnification) demonstrated no gross arterial abnormality. However, on careful inspection, several slightly enlarged tertiary branches of the middle cerebral artery were identified in the inferomedial portion of the right frontal lobe. These branches appeared to penetrate the substance of the brain and supply the malformation on its periphery (Fig. 1, B). In the late arterial and capillary phases, a
poorly marginated homogeneous blush was evident in the inferomedial aspect of the right frontal lobe (Fig. 1, C). Almost simultaneously, a myriad of small medullary veins appeared in the area of the blush. In the venous phase, these small vessels converged centrally into a single large vein which traversed the substance of the frontal pole to its lateral surface and then drained upward to empty into the superior sagittal sinus (Fig. 1, D and E). On opening the dura at operation, a large cortical vein was identified which disappeared into the substance of the right frontal lobe. A cortical incision was made and the large vein was followed into an area of increased vascularity which grossly appeared to represent an arteriovenous malformation. Dissection was carried out around the enlarged vessels, and a right frontal lobectomy to the tip of the frontal horn was performed. Histologic examination of the excised frontal lobe showed numerous dilated thick-walled vascular structures separated by neural parenchyma. The wall thickening was due to increased collagenous tissue. Special stains for elastic tissue showed no elastic laminae in the vessel walls, confirming that these were in fact veins (Fig. 1, F). No arteries were identified within the malformation. CASE II. A 49-year-old black man presented at the Philadelphia General Hospital with a one-year history of generalized seizures with no focal component. The seizures typically occurred about 24 hours after discontinuance of heavy ethanol intake. The patient had sustained head trauma two years earlier but was not knocked unconscious from this episode. There were no positive findings on physical or neurological examination, and an EEG and CSF studies were normal. A 99mTc brain scan was also normal, but only static images were obtained. A left common carotid angiogram demonstrated no gross abnormality in the early arterial phase. In the late arterial phase, a faint, poorly marginated blush was noted in the posterior frontal parasagittal region, and an early filling vein ascended from the region of the blush to empty into the superior sagittal sinus (Fig. 2, A). In the capillary phase, numerous small medullary veins were evident in the region of the blush and appeared to drain into the ascending vein which was densely opacified ,(Fig. 2, B).
1 From the Departments of Radiology (L. W., J. M., S. K.), Minneapolis Veterans Administration Hospital and University of Minnesota Health Sciences Center, Minneapolis, Minn., Philadelphia General Hospital (H. G.), Philadelphia, Pa., and United States Air Force Hospital (R. L.), Travis Air Force Base, Calif. Accepted for publication in October 1975. Presented at the Thirteenth Annual Meeting of the American Society of Neuroradiology, Vancouver, B.C., June 4-7, 1975. 2 Formerly Fellow in Neuroradiology (NINDS Traineeship 5T01-NS-05422). Present address: Department of Radiology, Sacred Heart Medical Center, Spokane, Wash. 3 Present address: Department of Radiology, State University of New York, Upstate Medical Center, Syracuse, N.Y. 4 Present address: Department of Radiology, University of Minnesota Health Sciences Center, Minneapolis, Minn. shan
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Fig. 1. CASE I. A. 99mTc brain scan. The dynamic portion of the study (upper row) demonstrates increased radioactivity in the right inferior frontal region (single arrow) which drains early into the superior sagittal sinus (double arrows). The static images (lower row) are normal. B. Right common carotid arteriogram, midarterial phase, lateral view, 1.8 times magnification. There are several slightly enlarged peripheral branches of the middle cerebral artery in the inferior frontal region (arrows). These branch arteries cross several other larger middle cerebral branches, indicating that they lie within the substance of the frontal lobe. With the exception of the lenticulostriate arteries, such penetrating branches are normally not visualized, even with magnification. C. Same study, late arterial phase, anteroposterior view. There is a poorly marginated heterogeneous blush in the inferomedial aspect of the right frontal lobe (arrows). D. Same study, midvenous phase, anteroposterior view. A spoke-like network of smaller veins (arrows) converges centrally into a single large vein (crossed arrows) which courses inferiorly and laterally to reach the floor of the anterior cranial fossa and then ascends medially to drain into the superior sagittal sinus. On careful inspection, the converging smaller veins can be identified on Figure 1, C in the midst of the blush. E. Same study, midvenous phase, lateral view. The centripetally draining venous network outlines the extent of the malformation. F. Low power photomicrograph of the excised specimen from the inferomedial right frontal lobe; Verhoeff's elastic tissue stain. Smaller thin-walled vascular channels (2) are separated by normal neural tissue. These channels drain into a much larger caliber vessel which is also thin-walled ( 1). No elastic tissue is demonstrated in the walls of the visualized vessels.
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Fig. 2. CASE II. A. Left common carotid angiogram, late arterial phase, lateral view. There is a faint, poorly defined blush in the posterior frontal parasagittal region. An early filling vein (arrow) ascends from the area of the blush toward the superior sagittal sinus. B. Same study, capillary phase, lateral view. Numerous smaller veins are evident in the region of the blush and appear to drain into the larger ascending vein which is now more densely opacified. C. Repeat injection, early arterial phase, coned-down lateral view, 5 times magnification. Several small branches arise from the callosomarginal artery in this region. These smaller arteries circumscribe the area of blush seen in Fig. 2, A. D. Same study, late arterial phase, lateral view, 5 times magnification. A myriad of small venous channels converges into the large ascending vein. (From Goldberg HI: Clinical cerebral magnification angiography and angiotomography: lesions of the perforating arteries. [In j Small Vessel Angiography, Hilal S, ed. St. Louis, Moseby, 1973. By permission of the authors and publisher.)
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Fig. 3. CASE III. A. 99mTc image, dynamic portion. The arterial phase (upper left) is normal. In the early phase (upper right), there is an area of increased radioactivity in the left frontal region (arrows) which persists into the late venous phase (lower row of images). The static images (not displayed) were normal. B. Left internal carotid angiogram, midarteriaJ phase, lateral view. No abnormality is evident. C. Same study (capillary phase, lateral view) is normal. D. Same study, midvenous phase, lateral view. Numerous small venous channels drain inferiorly and centrally into a larger venous channel which ascends to empty into the superior sagittal sinus.
A repeat injection was made, and serial films were obtained at 5 times magnification. In the early arterial phase, prior to the appearance of any blush, a callosomarginal branch of the anterior cerebral artery in the posterior frontal parasagittal region gave rise to several small tributaries which appeared to supply the vascular lesion at its periphery (Fig. 2, C). In the late arterial phase, a network of medullary veins is more clearly identified on the magnification study;
these veins are dilated, irreqular, tortuous, and drain centrally into the large ascending cortical vein (Fig. 2, D). The patient was placed on seizure control medications and discharged without operation. His subsequent clinical course over a three-year period has been stable. CASE
III.
A 24-year-old white man was hospitalized for a minor
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surgical procedure on an extremity. Thirty minutes before the procedure was to begin, he was given 0.2 ml intradermal test injection of lidocaine in the operating room. This was followed immediately by a generalized seizure. Follow-up evaluation revealed a patient who had been in excellent health until the recent incident. There was no history of previous seizures or drug allergies. His general physical and neurological examinations were normal. Skull x rays and EEG were normal. He was transferred to the United States Air Force Hospital at Travis Air Force Base, California, for furtherevaluation. On the dynamic study, a 99mTc brain scan demonstrated an area of increased uptake in the left frontal region in the early portion of the venous phase, with a lesser degree of uptake on subsequent routine anddelayed static views (Fig. 3, A). A selective left internal carotid angiogram demonstrated no gross abnormality in the arterial or capillary phases (Fig. 3, B and C). In the venous phase, numerous small but dilated medullary veins drained centrally into a single large channel which courses transcerebrally to reach the cortical surface and then posteriorly to drain into the superior sagittal sinus (Fig. 3, D). No surgical intervention was undertaken. Results of the follow-up examination six months later, including EEG and brain scan, were unchanged from the previous admission.
PATHOLOGY AND CLASSIFICATION
With the exception of arteriovenous malformations, vascular malformations of the brain are rare. Courville found only 5 venous angiomas and 18 capillary telangiectases in a series of 30,000 autopsies (3). Russell and Rubinstein (12) classify vascular malformations of the central nervous system as follows: 1.
2.
3.
Capillary telangiectasis: a collection of abnormally dilated capillaries which lack any smooth muscle or elastic tissues in their walls. The individual capillaries are separated by normal interstitial neural tissues. This lesion is typically small, solitary, and asymptomatic. Cavernous angioma: a well-circumscribed, compact honeycomb-like mass of large sinusoidal vascular spaces. These lesions vary considerably in size from one millimeter up to several centimeters (9) and are occasionally symptomatic due to associated hemorrhage or seizures. The individual vessels resemble capillaries, without muscle or elastic tissue, and there is no intervening brain parenchyma. Thromboses and punctate calcifications are common (13). Arteriovenous malformation: by far, the most common type of vascular malformation. These lesions consist of a tortuous mass of dilated, elongated, and thickened arteries and veins which may vary in size from a few millimeters ("cryptic") to a mass many centimeters in diameter. The arteries show altered lamination of elastic fibers with areas of segmental dilatation. The intervening brain parenchyma between the vessels usually degenerates with time due to hemorrhage and/or vascular insufficiency from thrombosis or arteriosclerosis (9, 10).
4.
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Venous angioma: the rarest of the types of vascular malformation, this lesion is characterized by large numbers of irregularly dilated venous channels. The walls of these vessels show irregular smooth muscle or connective tissue thickening but no elastic tissue. Both grossly and microscopically, a venous malformation resembles an arteriovenous malformation except that arteries are absent. In contrast to the cavernous angioma, the dilated vessels are separated by neural tissue (Fig. 1, F). ANGIOGRAPHIC FINDINGS
Cerebral angiograms have demonstrated a venous angioma (presumed or proved) in 7 patients, including the present series. In 6, the angiographic appearance was nearly identical. Most characteristic is the venous drainage pattern which has a caput medusae appearance: a myriad of small veins arise at the periphery of the deeply located lesion and converge centrally into a much larger vein. This large central vein follows a transcerebral course to reach a cortical surface, where it ascends to empty into larger cortical veins or a dural sinus (Figs. 1, C and D, 2, Band 0, and 3, C). Alternatively, the large transcerebral vein may drain into a subependymal vein in the wall of a lateral ventricle (2). Opacification of the venous network of the lesion may occur early, as in 2 of the 3 cases herein reported (Figs. 1, C; 2, B and D). Typically, the large central draining vein remains opacified through the late venous phase. A poorly marginated vascular blush was identified in the area of the lesion in the late arterial and capillary phases in 2 patients in this report (Figs. 1, C and 2, A) but has not been described in previous reports. In the arterial phase, no abnormalities are identified on films made using the usual techniques, even with subtraction. However, magnification studies in 2 cases did demonstrate small perforating arteries in the area of the malformation. In CASE I, at 1.8 times magnification, small middle cerebral artery branches are seen to cross larger branches, suggesting that the small branches are perforating into the substance of the brain (Fig. 1, B). In CASE II, at five times magnification, small cortical arteries at the periphery of the malformation are slightly enlarged and appear to be supplying the malformation (Fig. 2, C). Unless the malformation bleeds into the substance of the brain, it produces no vascular displacement. There was no angiographic evidence of mass effect in the 6 "typical" cases. A somewhat atypical angiographic pattern in a histologically proved venous angioma was reported by Wolf et al. (14). The patient had two intracerebral venous angiomas, only one of which was opacified at angiography. Two slightly enlarged branches of the middle cerebral artery supplied a collection of large irregular vessels. These vessels formed a disorganized collection
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which did not exhibit the centripetal drainage pattern described above. However, they did drain early into a large venous channel which coursed transcerebrally to reach the cortex and then ascended to empty into the superior sagittal sinus. The unopacified second malformation had bled, causing a large intracerebral hematoma which may have compressed and distorted the appearance of the opacified angioma.
DIFFERENTIAL DIAGNOSIS
The angiographic characteristics described above are, we believe, suggestive if not specific for the diagnosis of intracerebral venous angioma. They differ quite markedly from the more common arteriovenous malformation wherein grossly enlarged arteries supply the lesion and the venous drainage typically is more rapid through multiple venous channels arising and draining peripherally. In a venous angioma, the opacified veins drain centripetally into a common channel which then drains transcerebrally into either the superficial or deep venous systems. Cavernous angioma may present some difficulty in differential diagnosis. Roberson et al. (11) have described a case of cavernous angioma of the brain stem proved at autopsy in which angiography demonstrated a centripetal type of venous network remarkably similar in appearance to the lesions herein reported; however, they attributed the venous network not to the cavernous angioma but rather to associated "telangiectases." Liliequist (8) has recently reported 3 patients (one with histologic proof, the other two unproved) with cavernous angioma of the brain, all of whom demonstrated on angiography a capillary blush, early filling of dilated veins within the deeply seated lesions, and absence of enlarged feeding arteries. The pattern of venous drainage was centripetal but the radial arrangement of the venous network was not as striking as in Roberson's case or the patients with venous angioma herein reported. Jonutis et al. (6) described another patient with histologically proved intracerebral cavernous angioma in whom angiography demonstrated slightly enlarged feeding arteries, a capillary blush, and multiple draining veins without a centripetal pattern. Bogren et al. (1) also reported 2 cases of cavernous angioma with a prominent centripetal venous network evident on angiography, but this angiographic pattern was not present in their other 2 cases nor has it been confirmed by other authors (6, 11). On the basis of the histologically proved cases, there appears to be a considerable overlap in angiographic pattern between cavernous and venous angiomas. Carcinomatous or sarcomatous metastasis might mimic the peripheral arterial and centripetal venous patterns of venous angioma but such a lesion would likely be associated with considerably larger supplying arteries, irregular tumor vessels, and local mass effect. Occasionally, on angiography, a low grade glioma
April 1976
may demonstrate capillary blush and early filling veins without grossly enlarged feeding arteries. These tumors usually have a considerable mass effect and their venous drainage is centrifugal in contradistinction to venous angioma.
DISCUSSION
Vascular malformations of the brain are congenital anomalies. The term "angioma," although widely used, is a misnomer since these lesions are not true neoplasms, i.e., they show no evidence of cellular proliferation. However, in their clinical and macroscopic features, they do somewhat resemble tumors in that they may grow (by dilatation of affected vessels) and inflict progressive destruction on the adjacent brain. In a 'broad sense, all vascular malformations of the brain must, by definition, be termed arteriovenous malformations, since the lesion must have an arterial supply. In the case of venous or cavernous angiomas, pathologists have been unable to demonstrate arteries in increased size or number in the malformation, and thus these lesions have been separated from the much larger group of arteriovenous malformations in which the arteries are indeed present in increased size and number. With magnification techniques, we have been able to demonstrate small peripheral arteries arising from major branches of the anterior and middle cerebral arteries, and coursing to the periphery of the venous malformation in 2 cases (Fig. 1, Band 2, C). These branches are not normally visualized without the aid of small focal spot magnification techniques. In the same 2 cases, a poorly defined blush and early filling medullary veins within that blush support the hypothesis that the supplying arteries are truly enlarged and that this lesion does represent an arteriovenous shunt. The lesion could therefore be considered a form of arteriovenous malformation with venous predominance. When treated surgically, the malformation is not usually excised en bloc, but rather the pathologist receives bits and fragments of tissue, typically without definite orientation as to exact location. The lack of arteries in the malformation on histologic examination may be related to the location of the feeding arteries on the periphery of the malformation and therefore outside the area of the pathologist's interest. The clinical aspects of this lesion usually relate to associated hemorrhage. In 1967, Wolf et al. accumulated 9 cases of venous angioma from the previous literature (14); in all 9, the diagnosis was made at autopsy following death from intracerebral and/or subarachnoid hemorrhage. Four patients have subsequently been reported in whom the diagnosis was suggested at angiography (2, 4, 5, 14). Of those 4 patients and the 3 in this report, only one has died from intracerebral hemorrhage (14). Of the remaining 6 cases, the presenting findings included generalized seizures in 3 and sub-
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arachnoid hemorrhage in 2; in one patient, the diagnosis was fortuitous and unrelated to his complaints. It is noteworthy that symptoms occurred under the age of 30 in 11 of the 16 patients. ACKNOWLEDGMENTS: The authors wish to acknowledge with grateful appreciation the assistance of Emmanuel Stadlan, M.D. (neuropathology) and Charles Weigent, M.D. (pathology), Minneapolis Veterans Administration Hospital, and Angeline Mastri, M.D. (neuropathology), University of Minnesota Hospitals, in the histologic evaluation of CASE I.
Department of Radiology Sacred Heart Medical Center West 101 Eighth Avenue Spokane, Wash. 99204
REFERENCES 1. Bogren H, Svalander C, Wickbom I: Angiography in intracranial cavernous hemangiomas. Acta Radiol. (Diag) 10:81-89, Mar 1970 2. Constans JP, Dilenge 0, Vedrenne C: Angiomes veineux cerebraux. Neurochirurgie 14:641-650, Jun 1968 3. Courville CB: Pathology of the Central Nervous System. Mountain View, Calif., Pacific Press, 2d ed, 1945
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4. Heinz ER: Pathology involving the supratentorial veins and dural sinuses. [In) Newton TH, Potts DG, eds: Radiology of the Skull and Brain. St. Louis, Mosby, 1974, pp 1878-1902 5. Heinz ER, Hardman DR: Current problems in neuroradiology. Curr Problems Radiol 4:1-48, Sep-Oct 1974 6. Jonutis AJ, Sondheimer FK, Klein HZ, et al: Intracerebral cavernous hemangioma with angiographically demonstrated pathologic vasculature. Neuroradiology 3:57-63, Dec 1971 7. Kamrin RB, Buchsbaum HW: Large vascular malformations of the brain not visualized by serial angiography. Arch Neurol (Chicago) 13:413-420, Oct 1965 8. Liliequist B: Angiography in intracerebral cavernous hemangioma. Neuroradiology 9:69-72, Jun 1975 9. McCormick WF: The pathology of vascular ("arteriovenous") malformations. J Neurosurg 24:807-816, Apr 1966 10. Newton TH, Troost BT: Arteriovenous malformations and fistulae. [In) Newton TH, Potts DG, eds: Radiology of the Skull and Brain. St. Louis, Mosby, 1974, pp 2490-2565 11. Roberson GH, Kase CS, Wolpow ER: Telangiectases and cavernous angiomas of the brainstem: "cryptic" vascular malformations. Report of a case. Neuroradiology 8:83-89, Oct 1974 12. Russell OS, Rubinstein LJ: Pathology of Tumours of the Nervous System. Baltimore, Williams & Wilkins, 3d ed, 1971, pp 85-108 13. Segall HD, Segal HL, Teal JS, et al: Calcifying cerebral cavernous hemangioma with brain scan and angiographic findings. Neuroradiology 7:133-138, May 1974 14. Wolf PA, Rossman NP, New PFJ: Multiple small cryptic venous angiomas of the brain mimicking cerebral metastases. A clinical, pathological and angiographic study. Neurology (Minneap) 17: 491-501, May 1967
Neuroradiology
Intracerebral Venous Angioma
1
Lyle R. Wendling, M.D.,2 James S. Moore, Jr., M.D., Stephen A. Kieffer, M.D.,3 Herbert I. Goldberg, M.D., and Richard E. Latchaw, M.D.4 Intracerebral venous angioma is a rare congenital vascular malformation of the brain. Three cases are reported, all of which had strikingly similar angiographic findings in the venous phase, viz., a local network of small medullary veins which converge centrally into a single large venous channel which courses transcerebrally to reach the superficial venous system. No gross abnormalities are seen in the arterial phase with the usual techniques. However, magnification delineated enlarged arterial branches supplying the periphery of the malformation in 2 of the 3 cases. A poorly marginated homogeneous blush and early filling of the draining veins were also seen in these 2 patients. The findings in the venous phase agree with those described in previous isolated case reports and appear to be highly suggestive of this rare malformation. INDEX TERMS: Angioma. Brain, abnormalities. Cerebral Angiography. Magnification • Malformations, arteriovenous Radiology 119:141-147, April 1976
is an unusual vascular malformation seldom found in the spinal cord and even more rarely in the brain. On both gross and microscopic anatomic examination, this lesion quite closely resembles the more common arteriovenous malformation, except that arteries are not to be found in increased number or size in the region of the malformation (9, 12). Angiographic demonstration of an intracerebral venous angioma was first reported by Wolf et a/. in 1967 (14), and only 3 other cases with angiographic evaluation have been described in the intervening years (2, 4, 5). We have recently encountered 3 patients in whom cerebral angiography demonstrated a unique appearance which may be highly suggestive of this rare malformation.
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CASE REPORTS CASE I. A 28-year-old black man was admitted to the Minneapolis Veterans Administration Hospital because of grand mal seizures one to two times per week over the past four years. Previous EEG and CSF studies were normal. On the day of admission, the patient had three grand mal seizures. General physical examination was unremarkable, but neurological examination revealed a mild left-sided hyperreflexia. Skull x rays were normal. The dynamic portion of a 99mTc brain scan demonstrated an early appearing area of increased radioactivity in the right inferior frontal region which seemed to drain into the superior sagittal sinus and wash out in the venous phase (Fig. 1, A). Static views were normal. A right common carotid angiogram (simultaneous biplane study, 1.8 times magnification) demonstrated no gross arterial abnormality. However, on careful inspection, several slightly enlarged tertiary branches of the middle cerebral artery were identified in the inferomedial portion of the right frontal lobe. These branches appeared to penetrate the substance of the brain and supply the malformation on its periphery (Fig. 1, B). In the late arterial and capillary phases, a
poorly marginated homogeneous blush was evident in the inferomedial aspect of the right frontal lobe (Fig. 1, C). Almost simultaneously, a myriad of small medullary veins appeared in the area of the blush. In the venous phase, these small vessels converged centrally into a single large vein which traversed the substance of the frontal pole to its lateral surface and then drained upward to empty into the superior sagittal sinus (Fig. 1, D and E). On opening the dura at operation, a large cortical vein was identified which disappeared into the substance of the right frontal lobe. A cortical incision was made and the large vein was followed into an area of increased vascularity which grossly appeared to represent an arteriovenous malformation. Dissection was carried out around the enlarged vessels, and a right frontal lobectomy to the tip of the frontal horn was performed. Histologic examination of the excised frontal lobe showed numerous dilated thick-walled vascular structures separated by neural parenchyma. The wall thickening was due to increased collagenous tissue. Special stains for elastic tissue showed no elastic laminae in the vessel walls, confirming that these were in fact veins (Fig. 1, F). No arteries were identified within the malformation. CASE II. A 49-year-old black man presented at the Philadelphia General Hospital with a one-year history of generalized seizures with no focal component. The seizures typically occurred about 24 hours after discontinuance of heavy ethanol intake. The patient had sustained head trauma two years earlier but was not knocked unconscious from this episode. There were no positive findings on physical or neurological examination, and an EEG and CSF studies were normal. A 99mTc brain scan was also normal, but only static images were obtained. A left common carotid angiogram demonstrated no gross abnormality in the early arterial phase. In the late arterial phase, a faint, poorly marginated blush was noted in the posterior frontal parasagittal region, and an early filling vein ascended from the region of the blush to empty into the superior sagittal sinus (Fig. 2, A). In the capillary phase, numerous small medullary veins were evident in the region of the blush and appeared to drain into the ascending vein which was densely opacified ,(Fig. 2, B).
1 From the Departments of Radiology (L. W., J. M., S. K.), Minneapolis Veterans Administration Hospital and University of Minnesota Health Sciences Center, Minneapolis, Minn., Philadelphia General Hospital (H. G.), Philadelphia, Pa., and United States Air Force Hospital (R. L.), Travis Air Force Base, Calif. Accepted for publication in October 1975. Presented at the Thirteenth Annual Meeting of the American Society of Neuroradiology, Vancouver, B.C., June 4-7, 1975. 2 Formerly Fellow in Neuroradiology (NINDS Traineeship 5T01-NS-05422). Present address: Department of Radiology, Sacred Heart Medical Center, Spokane, Wash. 3 Present address: Department of Radiology, State University of New York, Upstate Medical Center, Syracuse, N.Y. 4 Present address: Department of Radiology, University of Minnesota Health Sciences Center, Minneapolis, Minn. shan
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Fig. 1. CASE I. A. 99mTc brain scan. The dynamic portion of the study (upper row) demonstrates increased radioactivity in the right inferior frontal region (single arrow) which drains early into the superior sagittal sinus (double arrows). The static images (lower row) are normal. B. Right common carotid arteriogram, midarterial phase, lateral view, 1.8 times magnification. There are several slightly enlarged peripheral branches of the middle cerebral artery in the inferior frontal region (arrows). These branch arteries cross several other larger middle cerebral branches, indicating that they lie within the substance of the frontal lobe. With the exception of the lenticulostriate arteries, such penetrating branches are normally not visualized, even with magnification. C. Same study, late arterial phase, anteroposterior view. There is a poorly marginated heterogeneous blush in the inferomedial aspect of the right frontal lobe (arrows). D. Same study, midvenous phase, anteroposterior view. A spoke-like network of smaller veins (arrows) converges centrally into a single large vein (crossed arrows) which courses inferiorly and laterally to reach the floor of the anterior cranial fossa and then ascends medially to drain into the superior sagittal sinus. On careful inspection, the converging smaller veins can be identified on Figure 1, C in the midst of the blush. E. Same study, midvenous phase, lateral view. The centripetally draining venous network outlines the extent of the malformation. F. Low power photomicrograph of the excised specimen from the inferomedial right frontal lobe; Verhoeff's elastic tissue stain. Smaller thin-walled vascular channels (2) are separated by normal neural tissue. These channels drain into a much larger caliber vessel which is also thin-walled ( 1). No elastic tissue is demonstrated in the walls of the visualized vessels.
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Fig. 2. CASE II. A. Left common carotid angiogram, late arterial phase, lateral view. There is a faint, poorly defined blush in the posterior frontal parasagittal region. An early filling vein (arrow) ascends from the area of the blush toward the superior sagittal sinus. B. Same study, capillary phase, lateral view. Numerous smaller veins are evident in the region of the blush and appear to drain into the larger ascending vein which is now more densely opacified. C. Repeat injection, early arterial phase, coned-down lateral view, 5 times magnification. Several small branches arise from the callosomarginal artery in this region. These smaller arteries circumscribe the area of blush seen in Fig. 2, A. D. Same study, late arterial phase, lateral view, 5 times magnification. A myriad of small venous channels converges into the large ascending vein. (From Goldberg HI: Clinical cerebral magnification angiography and angiotomography: lesions of the perforating arteries. [In j Small Vessel Angiography, Hilal S, ed. St. Louis, Moseby, 1973. By permission of the authors and publisher.)
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Fig. 3. CASE III. A. 99mTc image, dynamic portion. The arterial phase (upper left) is normal. In the early phase (upper right), there is an area of increased radioactivity in the left frontal region (arrows) which persists into the late venous phase (lower row of images). The static images (not displayed) were normal. B. Left internal carotid angiogram, midarteriaJ phase, lateral view. No abnormality is evident. C. Same study (capillary phase, lateral view) is normal. D. Same study, midvenous phase, lateral view. Numerous small venous channels drain inferiorly and centrally into a larger venous channel which ascends to empty into the superior sagittal sinus.
A repeat injection was made, and serial films were obtained at 5 times magnification. In the early arterial phase, prior to the appearance of any blush, a callosomarginal branch of the anterior cerebral artery in the posterior frontal parasagittal region gave rise to several small tributaries which appeared to supply the vascular lesion at its periphery (Fig. 2, C). In the late arterial phase, a network of medullary veins is more clearly identified on the magnification study;
these veins are dilated, irreqular, tortuous, and drain centrally into the large ascending cortical vein (Fig. 2, D). The patient was placed on seizure control medications and discharged without operation. His subsequent clinical course over a three-year period has been stable. CASE
III.
A 24-year-old white man was hospitalized for a minor
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surgical procedure on an extremity. Thirty minutes before the procedure was to begin, he was given 0.2 ml intradermal test injection of lidocaine in the operating room. This was followed immediately by a generalized seizure. Follow-up evaluation revealed a patient who had been in excellent health until the recent incident. There was no history of previous seizures or drug allergies. His general physical and neurological examinations were normal. Skull x rays and EEG were normal. He was transferred to the United States Air Force Hospital at Travis Air Force Base, California, for furtherevaluation. On the dynamic study, a 99mTc brain scan demonstrated an area of increased uptake in the left frontal region in the early portion of the venous phase, with a lesser degree of uptake on subsequent routine anddelayed static views (Fig. 3, A). A selective left internal carotid angiogram demonstrated no gross abnormality in the arterial or capillary phases (Fig. 3, B and C). In the venous phase, numerous small but dilated medullary veins drained centrally into a single large channel which courses transcerebrally to reach the cortical surface and then posteriorly to drain into the superior sagittal sinus (Fig. 3, D). No surgical intervention was undertaken. Results of the follow-up examination six months later, including EEG and brain scan, were unchanged from the previous admission.
PATHOLOGY AND CLASSIFICATION
With the exception of arteriovenous malformations, vascular malformations of the brain are rare. Courville found only 5 venous angiomas and 18 capillary telangiectases in a series of 30,000 autopsies (3). Russell and Rubinstein (12) classify vascular malformations of the central nervous system as follows: 1.
2.
3.
Capillary telangiectasis: a collection of abnormally dilated capillaries which lack any smooth muscle or elastic tissues in their walls. The individual capillaries are separated by normal interstitial neural tissues. This lesion is typically small, solitary, and asymptomatic. Cavernous angioma: a well-circumscribed, compact honeycomb-like mass of large sinusoidal vascular spaces. These lesions vary considerably in size from one millimeter up to several centimeters (9) and are occasionally symptomatic due to associated hemorrhage or seizures. The individual vessels resemble capillaries, without muscle or elastic tissue, and there is no intervening brain parenchyma. Thromboses and punctate calcifications are common (13). Arteriovenous malformation: by far, the most common type of vascular malformation. These lesions consist of a tortuous mass of dilated, elongated, and thickened arteries and veins which may vary in size from a few millimeters ("cryptic") to a mass many centimeters in diameter. The arteries show altered lamination of elastic fibers with areas of segmental dilatation. The intervening brain parenchyma between the vessels usually degenerates with time due to hemorrhage and/or vascular insufficiency from thrombosis or arteriosclerosis (9, 10).
4.
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Venous angioma: the rarest of the types of vascular malformation, this lesion is characterized by large numbers of irregularly dilated venous channels. The walls of these vessels show irregular smooth muscle or connective tissue thickening but no elastic tissue. Both grossly and microscopically, a venous malformation resembles an arteriovenous malformation except that arteries are absent. In contrast to the cavernous angioma, the dilated vessels are separated by neural tissue (Fig. 1, F). ANGIOGRAPHIC FINDINGS
Cerebral angiograms have demonstrated a venous angioma (presumed or proved) in 7 patients, including the present series. In 6, the angiographic appearance was nearly identical. Most characteristic is the venous drainage pattern which has a caput medusae appearance: a myriad of small veins arise at the periphery of the deeply located lesion and converge centrally into a much larger vein. This large central vein follows a transcerebral course to reach a cortical surface, where it ascends to empty into larger cortical veins or a dural sinus (Figs. 1, C and D, 2, Band 0, and 3, C). Alternatively, the large transcerebral vein may drain into a subependymal vein in the wall of a lateral ventricle (2). Opacification of the venous network of the lesion may occur early, as in 2 of the 3 cases herein reported (Figs. 1, C; 2, B and D). Typically, the large central draining vein remains opacified through the late venous phase. A poorly marginated vascular blush was identified in the area of the lesion in the late arterial and capillary phases in 2 patients in this report (Figs. 1, C and 2, A) but has not been described in previous reports. In the arterial phase, no abnormalities are identified on films made using the usual techniques, even with subtraction. However, magnification studies in 2 cases did demonstrate small perforating arteries in the area of the malformation. In CASE I, at 1.8 times magnification, small middle cerebral artery branches are seen to cross larger branches, suggesting that the small branches are perforating into the substance of the brain (Fig. 1, B). In CASE II, at five times magnification, small cortical arteries at the periphery of the malformation are slightly enlarged and appear to be supplying the malformation (Fig. 2, C). Unless the malformation bleeds into the substance of the brain, it produces no vascular displacement. There was no angiographic evidence of mass effect in the 6 "typical" cases. A somewhat atypical angiographic pattern in a histologically proved venous angioma was reported by Wolf et al. (14). The patient had two intracerebral venous angiomas, only one of which was opacified at angiography. Two slightly enlarged branches of the middle cerebral artery supplied a collection of large irregular vessels. These vessels formed a disorganized collection
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which did not exhibit the centripetal drainage pattern described above. However, they did drain early into a large venous channel which coursed transcerebrally to reach the cortex and then ascended to empty into the superior sagittal sinus. The unopacified second malformation had bled, causing a large intracerebral hematoma which may have compressed and distorted the appearance of the opacified angioma.
DIFFERENTIAL DIAGNOSIS
The angiographic characteristics described above are, we believe, suggestive if not specific for the diagnosis of intracerebral venous angioma. They differ quite markedly from the more common arteriovenous malformation wherein grossly enlarged arteries supply the lesion and the venous drainage typically is more rapid through multiple venous channels arising and draining peripherally. In a venous angioma, the opacified veins drain centripetally into a common channel which then drains transcerebrally into either the superficial or deep venous systems. Cavernous angioma may present some difficulty in differential diagnosis. Roberson et al. (11) have described a case of cavernous angioma of the brain stem proved at autopsy in which angiography demonstrated a centripetal type of venous network remarkably similar in appearance to the lesions herein reported; however, they attributed the venous network not to the cavernous angioma but rather to associated "telangiectases." Liliequist (8) has recently reported 3 patients (one with histologic proof, the other two unproved) with cavernous angioma of the brain, all of whom demonstrated on angiography a capillary blush, early filling of dilated veins within the deeply seated lesions, and absence of enlarged feeding arteries. The pattern of venous drainage was centripetal but the radial arrangement of the venous network was not as striking as in Roberson's case or the patients with venous angioma herein reported. Jonutis et al. (6) described another patient with histologically proved intracerebral cavernous angioma in whom angiography demonstrated slightly enlarged feeding arteries, a capillary blush, and multiple draining veins without a centripetal pattern. Bogren et al. (1) also reported 2 cases of cavernous angioma with a prominent centripetal venous network evident on angiography, but this angiographic pattern was not present in their other 2 cases nor has it been confirmed by other authors (6, 11). On the basis of the histologically proved cases, there appears to be a considerable overlap in angiographic pattern between cavernous and venous angiomas. Carcinomatous or sarcomatous metastasis might mimic the peripheral arterial and centripetal venous patterns of venous angioma but such a lesion would likely be associated with considerably larger supplying arteries, irregular tumor vessels, and local mass effect. Occasionally, on angiography, a low grade glioma
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may demonstrate capillary blush and early filling veins without grossly enlarged feeding arteries. These tumors usually have a considerable mass effect and their venous drainage is centrifugal in contradistinction to venous angioma.
DISCUSSION
Vascular malformations of the brain are congenital anomalies. The term "angioma," although widely used, is a misnomer since these lesions are not true neoplasms, i.e., they show no evidence of cellular proliferation. However, in their clinical and macroscopic features, they do somewhat resemble tumors in that they may grow (by dilatation of affected vessels) and inflict progressive destruction on the adjacent brain. In a 'broad sense, all vascular malformations of the brain must, by definition, be termed arteriovenous malformations, since the lesion must have an arterial supply. In the case of venous or cavernous angiomas, pathologists have been unable to demonstrate arteries in increased size or number in the malformation, and thus these lesions have been separated from the much larger group of arteriovenous malformations in which the arteries are indeed present in increased size and number. With magnification techniques, we have been able to demonstrate small peripheral arteries arising from major branches of the anterior and middle cerebral arteries, and coursing to the periphery of the venous malformation in 2 cases (Fig. 1, Band 2, C). These branches are not normally visualized without the aid of small focal spot magnification techniques. In the same 2 cases, a poorly defined blush and early filling medullary veins within that blush support the hypothesis that the supplying arteries are truly enlarged and that this lesion does represent an arteriovenous shunt. The lesion could therefore be considered a form of arteriovenous malformation with venous predominance. When treated surgically, the malformation is not usually excised en bloc, but rather the pathologist receives bits and fragments of tissue, typically without definite orientation as to exact location. The lack of arteries in the malformation on histologic examination may be related to the location of the feeding arteries on the periphery of the malformation and therefore outside the area of the pathologist's interest. The clinical aspects of this lesion usually relate to associated hemorrhage. In 1967, Wolf et al. accumulated 9 cases of venous angioma from the previous literature (14); in all 9, the diagnosis was made at autopsy following death from intracerebral and/or subarachnoid hemorrhage. Four patients have subsequently been reported in whom the diagnosis was suggested at angiography (2, 4, 5, 14). Of those 4 patients and the 3 in this report, only one has died from intracerebral hemorrhage (14). Of the remaining 6 cases, the presenting findings included generalized seizures in 3 and sub-
INTRACEREBRAL VENOUS ANGIOMA
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arachnoid hemorrhage in 2; in one patient, the diagnosis was fortuitous and unrelated to his complaints. It is noteworthy that symptoms occurred under the age of 30 in 11 of the 16 patients. ACKNOWLEDGMENTS: The authors wish to acknowledge with grateful appreciation the assistance of Emmanuel Stadlan, M.D. (neuropathology) and Charles Weigent, M.D. (pathology), Minneapolis Veterans Administration Hospital, and Angeline Mastri, M.D. (neuropathology), University of Minnesota Hospitals, in the histologic evaluation of CASE I.
Department of Radiology Sacred Heart Medical Center West 101 Eighth Avenue Spokane, Wash. 99204
REFERENCES 1. Bogren H, Svalander C, Wickbom I: Angiography in intracranial cavernous hemangiomas. Acta Radiol. (Diag) 10:81-89, Mar 1970 2. Constans JP, Dilenge 0, Vedrenne C: Angiomes veineux cerebraux. Neurochirurgie 14:641-650, Jun 1968 3. Courville CB: Pathology of the Central Nervous System. Mountain View, Calif., Pacific Press, 2d ed, 1945
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4. Heinz ER: Pathology involving the supratentorial veins and dural sinuses. [In) Newton TH, Potts DG, eds: Radiology of the Skull and Brain. St. Louis, Mosby, 1974, pp 1878-1902 5. Heinz ER, Hardman DR: Current problems in neuroradiology. Curr Problems Radiol 4:1-48, Sep-Oct 1974 6. Jonutis AJ, Sondheimer FK, Klein HZ, et al: Intracerebral cavernous hemangioma with angiographically demonstrated pathologic vasculature. Neuroradiology 3:57-63, Dec 1971 7. Kamrin RB, Buchsbaum HW: Large vascular malformations of the brain not visualized by serial angiography. Arch Neurol (Chicago) 13:413-420, Oct 1965 8. Liliequist B: Angiography in intracerebral cavernous hemangioma. Neuroradiology 9:69-72, Jun 1975 9. McCormick WF: The pathology of vascular ("arteriovenous") malformations. J Neurosurg 24:807-816, Apr 1966 10. Newton TH, Troost BT: Arteriovenous malformations and fistulae. [In) Newton TH, Potts DG, eds: Radiology of the Skull and Brain. St. Louis, Mosby, 1974, pp 2490-2565 11. Roberson GH, Kase CS, Wolpow ER: Telangiectases and cavernous angiomas of the brainstem: "cryptic" vascular malformations. Report of a case. Neuroradiology 8:83-89, Oct 1974 12. Russell OS, Rubinstein LJ: Pathology of Tumours of the Nervous System. Baltimore, Williams & Wilkins, 3d ed, 1971, pp 85-108 13. Segall HD, Segal HL, Teal JS, et al: Calcifying cerebral cavernous hemangioma with brain scan and angiographic findings. Neuroradiology 7:133-138, May 1974 14. Wolf PA, Rossman NP, New PFJ: Multiple small cryptic venous angiomas of the brain mimicking cerebral metastases. A clinical, pathological and angiographic study. Neurology (Minneap) 17: 491-501, May 1967
