J Neurosurg 75:709-714, 1991

Natural history of the cavernous angioma JOHN R. ROBINSON, M.D., ISSAM A. AWAD, M.D., M.Sc., AND JOHN R. L1TI'LE, M.D.

Department of Neurological Surgery, The Cleveland Clinic" Foundation, Cleveland, Ohio v" The incidence and natural history of the cavernous angioma have remained unclear in part because of the difficulty of diagnosing and following this lesion prior to surgical excision. The introduction of magnetic resonance (MR) imaging has improved the sensitivity and specificity of diagnosing and following this vascular malformation. Seventy-six lesions with an MR appearance typical of a presumed cavernous angioma were discovered in 66 patients among 14,035 consecutive MR images performed at the Cleveland Clinic between 1984 and 1989. Follow-up studies in 86% of the cases over a mean period of 26 months provided 143 lesionyears of clinical survey of this condition. "l-he most frequent presenting features were seizure, focal neurological deficit, and headache. While most lesions exhibited evidence of occult bleeding on MR imaging, there was overt hemorrhage in seven of the 57 symptomatic patients and only one overt hemorrhage occurred during the follow-up interval. The annualized bleeding rate was 0.7%. Analysis of the hemorrhage group revealed a significantly greater risk of overt hemorrhage in females. Pathological confirmation of cavernous angioma was obtained in all 14 surgical cases. This information assists in rational therapeutic planning and prognosis in patients with MR images showing lesions suggestive of cavernous angioma. KEY WORDS cavernous angioma occult arteriovenous malformation magnetic resonance imaging 9 hemorrhage 9 seizure

HE cavernous angioma is a hamartomatous berrylike collection of vascular spaces lined by thin walls devoid of smooth muscle, s'9'19"21Typically, no brain tissue intervenes between these vascular channels, although the periphery of the lesion may contain cavernous lobules invading adjacent brain. 9'~9 Surrounding brain parenchyma is often gliotic and hemosiderin-stained, and may contain small low-flow feeding arteries and draining veins. 9"~2"~9Approximately 200 cases of cavernous angiomas have been reported since the initial pathological description of this vascular anomaly. 6'8"17"22'23"25'27'3~ Until recently, very little was known about the clinical importance of this lesion. This lack of information was largely the result of the relative insensitivity of either cerebral angiography or computerized tomography (CT) scanning for establishing clinical diagnosis. :,~ L~9,23,32 With the advent of magnetic resonance (MR) imaging there has been a substantial increase in the number of patients diagnosed as having this lesion. 7,s.~8,~9,24Prior to MR imaging, the diagnosis of cavernous angioma was usually made either at surgery or at autopsy, and little information was available regarding its natural history. 4"~'35This lack of knowledge has made treatment decisions difficult. The objective of this investigation was to describe the clinical findings and natural history

T

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of unselected consecutive lesions with a typical MR appearance of cavernous angioma, identified during a 5-year period at a single institution. Clinical Material and Methods

The reports of 14,035 MR images performed between 1984 and 1989 at the Cleveland Clinic Foundation were reviewed for findings suspicious of cavernous angioma, specifically a round or lobulated lesion with a mixed signal core surrounded by a low signal rim (Fig. 1). 7, ~o,~8.~9,24We selected 720 images for direct viewing in order to verify the presence of a lesion compatible with a presumed diagnosis of cavernous angioma. This process involved two independent reviewers who identified 107 images with such lesions. These images were then catalogued according to lesion location, size, and shape. In addition, the presence or absence of MR signals characteristic of edema, hemosiderin, or hematoma was recorded. Thirty-five patients had undergone serial imaging allowing the examination of changes in the above characteristics over time. In addition, the medical record of each patient with a presumed cavernous angioma identified on MR imaging was reviewed for age, sex, symptomatic presentation, surgical details, and other clinical data. Further data were obtained by follow-up visits or telephone 709

J. R. Robinson, I. A. Awad, and J. R. Little

FIG. 1. Axial T2-weighted magnetic resonance image (TR 2010 msec; TE 120 msec) depicting a typical cavernous angioma of the temporal lobe. Note the reticulated core signal and surrounding hemosiderin ring with decreased signal. The latter is often irregular in shape, indicating dissection into adjacent brain parenchyma, and tends to darken and become more distinct over time.

interviews. This included information regarding the patient's current condition, history of any recent clinical events, continued symptoms, and relevant surgery. Follow-up clinical information was obtained in 86% of the cases over a mean interval of 26 months and a total of 143 lesion-years of clinical survey. Pathological confirmation of a cavernous angioma was obtained in all 14 surgical cases based on histological criteria outlined above (Fig. 2). The presence of intervening gliotic brain at the periphery of the lesion and occasional feeding arteries and draining veins did

FIG. 2. Low-power photomicrograph of a typical cavernous angioma. Note the cavernous vascular spaces with thrombosis of varying duration and occasional calcification. The spaces are lined by thin walls consisting of endothelium and collagen (devoid of smooth muscle). There is no intervening brain substance within the bulk of the lesion. At the periphery of the angioma, gliotic hemosiderin-stained brain parenchyma separating some vascular lobules or definite small feeding and draining vessels may be present. H & E, x 49. 710

FIG. 3. Block graph showing the age and sex of 63 patients at the time that the magnetic resonance image revealed a cavernous angioma. Three patients without complete data sets were excluded.

not exclude this diagnosis. Special stains were used frequently to exclude the presence of smooth muscle in the walls lining the caverns within the bulk of the lesion.8.9,19.21.27 Statistical analysis was performed using Fisher's exact two-tailed test for comparison of proportions, with significance assumed at the p = 0.05 level. Comparison of possibly nonparametric variables, such as bleeding rates, was performed using the Wilcoxon rank-sum test.

Results

Patient Age and Sex Review of the MR images identified 76 lesions in 66 patients, including 36 males and 30 females. They ranged in age from 4 months to 84 years, with a mean age of 34.6 years. Figure 3 summarizes the sex and age at presentation of these patients.

FIG. 4. Lobar distribution of 76 cavernous angiomas in this series. The "deep" lesions affected the diencephalon and septai region. Other lesions are classified as occurring in a lobar or brain-stem location.

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Natural history of the cavernous angioma TABLE 1 Symptomatic presentation by lesion location of 66 patients* Symptom

Supratentorial lnfratentorial Lesion Lesion seizure 32 2 headache 18 2 focal deficit 20 I0 none 7 2 * Some lesions were associated with more than one symptomatic presentation.

TABLE 2 Criteria for diagnosis of overt hemorrhage in 66 patients 1. Magneticresonance imagingsignal of acute or subacute blood outside the "hemosiderinring" of the lesion 2. Evidenceof previous hemorrhageon lumbar puncture 3. Evidenceof fresh clot outside the confinesof the lesion at the time of surgery

TABLE 3 Outcome in 5 7 symptomatic cases of cavernous angioma correlated with hemorrhage and treatment* Lesion Location and Size There was a preponderance of supratentorial lesions, with the frontal and temporal lobes being the most frequent sites (Fig. 4). The lesions ranged in size from 0.3 to 4.0 cm with a mean size of 1.7 cm. There was no significant difference between the median size of the angiomas in supratentorial versus infratentorial locations (p = 0.582). Clinical Presentation The most frequent clinical presentation was seizures (34 patients), followed by focal neurological deficits (30 patients) and headaches (20 patients). The cavernous angioma was an incidental finding in nine patients. Patients with infratentorial angiomas were significantly more likely to present with focal neurological symptoms (p = 0.006), while supratentorial angiomas were significantly more likely to be associated with seizures (p = 0.005) (Table 1). Among the symptomatic group were six patients initially presenting with acute exacerbation of one or more symptoms. Findings in these patients were consistent with overt hemorrhage based on the criteria outlined in Table 2. Two of the six patients presenting with overt hemorrhage were pregnant women. Hemorrhage Rate A major objective of this study was to gain further insight into the risk of brain hemorrhage in patients with cavernous angioma. Analysis of our series revealed evidence of overt bleeding (based on the criteria outlined in Table 2) in seven of 57 symptomatic patients harboring a total of 66 lesions. While this represented 10.6% of the angiomas in our study, six of the seven patients presented initially with overt hemorrhage, and only one patient suffered a hemorrhage during the follow-up period. Thus, the bleeding rate was 0.7% per year per lesion based on the one hemorrhage that occurred during a follow-up period of 143 lesion-years. Further investigation into characteristics of the group with brain hemorrhage revealed bleeding in two ( 11.8 %) of 17 infratentorial lesions and in five (8.4%) of 59 supratentorial lesions. There was no apparent relationship between the size of the cavernous angioma and the likelihood of hemorrhage. The mean age of patients suffering overt hemorrhage was 30.4 years, but there J. Neurosurg. / Volume 75/November, 1991

Hemorrhage

Surgical Treatment

Good

Outcome Fair Poor

yes (7 cases)

yes 4 0 0 no 2 0 1 no (50 cases) yes 10 0 0 no 32 8 0 * Outcome definitions: good = minor impairment, occasional symptoms, no limitation of activities; fair = recurrent impairment, several symptomatic occurrences per week, limitation of activities; poor = frequent symptoms,an invalid.

was no significant difference in bleeding rate between patients over and under 40 years of age. Hemorrhage was significantly more prevalent in female patients (p = 0.05); five of the six overt hemorrhages occurred in females. Clinical Course and Surgical Intervention Four of the seven patients suffering a hemorrhage underwent surgical resection of the lesion; of the three patients with hemorrhage who were managed conservatively, one suffered a second episode of bleeding. All 18 patients whose seizures were managed conservatively continued to have seizures despite anticonvulsant therapy; of 14 patients with seizures who underwent surgical resection (including 10 cases with truly intractable epilepsy), seven had persistent seizures postoperatively despite continued anticonvulsant therapy. Eleven patients who presented initially with headaches were treated nonsurgically; five of these had resolution of symptoms during the follow-up period. Two of three patients undergoing surgery had no recurrence of headaches. Four of the nine asymptomatic patients developed symptoms related to their cavernous angiomas during follow-up periods of 6 months to 2 years (mean 18 months). The indication for surgery was the presence of intractable seizures in 10 patients and overt hemorrhage in four. All patients in the surgically treated group had experienced seizures at some time preoperatively. This group, including eight males and six females, had an average age of 21.3 years. The outcome of patients in this group is summarized in Table 3 and compared to 711

J. R. R o b i n s o n , I. A. A w a d , a n d J. R. Little the outcome for patients without surgery. There was no mortality or morbidity resulting from surgery.

Patient Outcome The overall mortality rate was 5.3% based on three deaths among the 57 symptomatic patients. However, none of the deaths was directly attributable to the cavernous angioma. Analysis of the cause of death revealed metastatic tumor in two patients and pneumonia in the third. The outcome of all patients in this study is summarized in Table 3. Outcome definitions are modified from the categories of Fults and Kelly5 as follows: good = minor impairment, occasional symptoms, no limitation of activities; fair = recurrent impairment, several symptomatic occurrences per week, limitation of activities; and poor = frequent symptoms, an invalid. Gross hemorrhage did not have a significant effect on outcome, as six of the seven patients presenting initially with hemorrhage had a good outcome; the seventh had a poor outcome as the result of a second hemorrhage. Table 3 also demonstrates a significant correlation between a good outcome and surgery. The outcome for all lesions was good in 48 patients, fair in eight, and poor in one.

Changes in Lesions Over Time A review of MR imaging in the 35 patients who underwent serial MR imaging allowed assessment of changes in the appearance of the angioma during periods of 3 months to 4 years. There was no consistent change over time in lesion shape or in the extent of edema in adjacent brain. Three lesions became larger over an average 11.7 months between MR images. A change noted consistently on serial images was the tendency of the hemosiderin ring to widen and to become more distinct with time. This was observed in 31 of the 35 cases.

Accuracy of Radiological Diagnosis The patients in our series were selected based on an MR appearance presumptive of a cavernous angioma. We reviewed the results of other diagnostic studies of these patients with respect to their efficacy in diagnosing this lesion. The results confirm that MR imaging is more sensitive than CT or angiography in characterizing the angioma. The CT scan was diagnostic but not specific in 38% of cases while angiography was diagnostic but not specific in only 9%. This fact was reinforced by pathological confirmation in the 14 surgically treated cases. The MR images in this series were reviewed for evidence of other lesions. The most common associated lesion was a second presumed cavernous angioma. Multiple cavernous angiomas were seen in seven of the 66 patients. A cavernous angioma was seen in conjunction with a venous angioma in three patients, and with a brain tumor in five patients.

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Discussion The natural history of cavernous angiomas has remained largely unexplored. The literature is replete with anecdotal reports of small collections of cases. T M 10,22,23,25.27-29,30-34,36 We have reviewed 76 lesions in 66 patients diagnosed by MR imaging with a mean followup period of 26 months for a total of 143 lesion-years of clinical survey. This series includes both surgically and conservatively treated lesions as well as symptomatic and asymptomatic cases, thereby allowing inferences to be made as to the natural history of this vascular malformation.

Sensitivity of Diagnosis by MR Imaging In order to assess the thoroughness of our review, we cross-checked the list of patients with presumed cavernous angiomas by MR imaging against a list of 17 patients who had been diagnosed as a result of surgical excision or biopsy. This revealed that the initial report survey had not missed any patient with cavernous angioma who had undergone MR imaging. The introduction of MR imaging has greatly enhanced the diagnosis of cavernous angiomas, and we and others have found this to be the most sensitive neuroradiological procedure available to diagnose this lesion. 7'Sasag,24,26Despite the fact that MR imaging was typically performed for a variety of indications, it is remarkable that the case incidence of 0.47% in this series is similar to that of several large autopsy series including those of Otten, el at., 16 (24,535 autopsies, 0.53% incidence) and Sarwar and McCormick :2 (4000 autopsies, 0.4% incidence).

Pathological Specificity Although no accurate analysis of specificity can be performed, thus far we have 100% pathological confirmation of 14 surgically treated cavernous angiomas originally diagnosed by MR imaging. More importantly, no lesion identified by MR imaging as a probable cavernous angioma has been found at surgery to be any other form of cryptic vascular malformation. Undoubtedly, other lesions may theoretically mimic the MR image appearance of a cavernous angioma. Our experience indicates that this is quite unlikely in clinical practice. There has been considerable debate in the recent literature about the pathological specificity of an appearance of occult vascular malformation on MR imaging, t'3,7'~3-~5,~Sa9,24'26 Some authors indicate that the appearance of cavernous angioma is quite specific.V,8.18,19.26Others propose that many such lesions are actually partially thrombosed arteriovenous malformations or "hybrid lesions" with pathological features of mixed cavernous and arteriovenous angiomas. 3'13-15 The controversy is partially related to semantics, with few authors defining a priori the pathological criteria of each diagnosis. Furthermore, we agree with Ogilvy and coworkers 14'" that the pathologist is often at a

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Natural history of the cavernous angioma disadvantage, receiving a coagulated fragmented specimen. Clearly, pathological features distinguishing these lesions can be subtle, and may be misleading at the periphery of the angioma (where there may be intervening gliotic brain and definite feeding and draining vessels). Lastly, several authors have emphasized that such a compulsive subdivision of lesions on pathological grounds may not be justified as there is no evidence that various angiographically occult vascular malformations imply different natural histories. 1.3.14.15

Natural Course The natural history of the cavernous angioma begins with symptoms exhibited usually prior to 30 years of age, with the majority of patients diagnosed prior to their sixth decade of life. The most frequently presenting symptom is seizure. The angiomas were located supratentorially in 78% of the cases in this series and infratentorially in the other 22%. The average lesion was approximately 1.7 cm in diameter and was noted to undergo progressive darkening of the hemosiderin ring over time. The lesion was asymptomatic in 16% of cases; however, 40% of these patients later developed symptoms related to the angioma. The majority of conservatively managed patients in each symptom group remained symptomatic during the follow-up period. This is in contrast to the surgically treated patients who experienced elimination of seizures in 50% of the cases, and a reduction in seizure frequency in the remainder of the patients. Sixty percent of patients suffering focal neurological deficits experienced relief of seizures following excision of the cavernous angioma. Ten percent of the lesions in our study showed evidence of overt hemorrhage. However, hemorrhage led to the initial clinical presentation and diagnosis in six of seven patients, while only one patient bled during the follow-up period. Thus, we estimate an annualized bleeding rate of 0.7% based on a single hemorrhage during 143 lesion-years of follow-up study. It is our belief that previous reports implying a higher risk of hemorrhage may have been biased by the selection of cases coming to medical attention only because of the bleeding. Such a selection bias tends to include lesions that are more likely to bleed while missing cavernous angiomas that have not bled and are asymptomatic, and thus never imaged. The risk of a second hemorrhage is difficult to assess since many patients undergo surgical resection of the cavernous angioma after a diagnosed gross hemorrhage. In this study, one of four patients with gross hemorrhage who were managed conservatively rebled. We found a significant difference in the rate of hemorrhage between male and female patients; females constituted 86% of the hemorrhage group. Two of the six women presenting with overt hemorrhage were in their first trimester of pregnancy on admission. It is our belief that this may be an important clue as to the role of endocrine factors in influencing hemorrhagic tendencies. We note that the first trimester of pregnancy witJ. Neurosurg. / Volume 75/November, 1991

nesses persistent vascular proliferation of the endometrium associated with continued secretion of human chorionic gonadotropin, progesterone, and estrogen. 2~ Analysis of results in this study using criteria introduced in literature on arteriovenous malformations revealed that the initial hemorrhage did not substantially affect the eventual outcome. 5 Surgically treated patients had more favorable outcomes than those managed conservatively. Only three of the 76 cavernous angiomas in our series changed appreciably in size. Most lesions, however, underwent some darkening of the surrounding ring. This is likely the result of a slow continuous oozing of hemoglobin into surrounding brain parenchyma, a process likely to be inherent in these thin-walled lowflow vascular lesions. ~2

Indications for Surgical Excision Based on these results, we recommend surgical excision of cavernous angiomas in patients with intractable seizures and in those with previous gross hemorrhage. Other less firm surgical indications include lesions in or near eloquent areas with progressive focal neurological deficits and accessible lesions in women contemplating pregnancy. Conclusions Our study has confirmed the role of MR imaging in the diagnosis and follow-up monitoring of cavernous angiomas, and has provided a profile of the natural history of these lesions including preliminary information about the risk of overt hemorrhage. These have provided general guidelines for rational clinical decision making. Other studies are in progress to further elucidate the natural risk of these lesions, including features predisposing to aggressive neurological course.

Acknowledgments We thank Lata Paranandi, M.S.P.H., for help with statistical analysis, Nancy Heim for the artwork, and Shirley MeDaniel for expert preparation of the manuscript. Pathological examinations were performed by Drs. Samuel Chou and Melinda Estes.

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J. Neurosurg. / Volume 75 /November, 1991

Natural history of the cavernous angioma.

The incidence and natural history of the cavernous angioma have remained unclear in part because of the difficulty of diagnosing and following this le...
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