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Primary Angiitis of the Central Nervous System at Conventional Angiography¹

¹ From the Neuroimaging Laboratory (Y.K., W.J.P., C.P.D.) and the Interventional Neuroradiology Service (C.J.M., D.T.C., C.P.D.) of the Mallinckrodt Institute of Radiology and Departments of Neurology (A.A., W.J.P., C.P.D.) and Neurological Surgery (C.J.M., D.T.C., W.J.P., C.P.D.), Washington University School of Medicine, 510 S Kingshighway Blvd, St Louis, MO 63110. Received October 6, 2003; revision requested December 23; revision received February 19, 2004; accepted March 30. Supported in part by the Amy Dennis Pierron Cerebral Vasculitis Research Fund of Barnes-Jewish Hospital. Y.K. supported in part by an American Academy of Neurology Medical Student Summer Research Scholarship. Address correspondence to C.P.D. (e-mail: derdeync@mir.wustl.edu).

	ABSTRACT

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PURPOSE: To retrospectively determine the sensitivity and specificity of cerebral angiography for the diagnosis of primary angiitis of the central nervous system (CNS).

MATERIALS AND METHODS: Institutional review board approval was obtained, and informed consent was not required. Thirty-eight patients (13 men, 25 women; mean age, 55 years) had undergone cerebral angiography followed by cortical and leptomeningeal biopsy for possible primary angiitis of the CNS during an 8-year period. Angiography reports were reviewed by investigators blinded to the results of biopsy. Angiographic findings were categorized as typical for vasculitis, normal, or other. Sensitivity and specificity of cerebral angiography for the diagnosis of primary angiitis of the CNS were calculated.

RESULTS: Fourteen patients had typical angiographic findings of vasculitis. None had primary angiitis of the CNS at brain biopsy (60% specificity). Specific pathologic diagnoses other than primary angiitis of the CNS were made in six patients. Findings of brain biopsy in the remaining eight patients were nondiagnostic. Repeat angiograms were obtained in three of the eight patients. One patient demonstrated interval improvement in multiple focal intracranial arterial stenoses and two demonstrated worsening. Primary angiitis of the CNS was found at biopsy in two of the remaining 24 patients (0% sensitivity). One of the two patients had slow filling of a single distal cortical artery, and the other patient had multiple regions of abnormally prolonged capillary blush.

CONCLUSION: In this series, patients suspected of having primary angiitis of the CNS on the basis of clinical and angiographic findings did not have primary angiitis of the CNS at biopsy. Typical angiographic findings of primary angiitis of the CNS are often associated with other specific pathologic diagnoses, which emphasizes the importance of brain biopsy.

© RSNA, 2004

Index terms: Cerebral angiography, technology, 17.124 • Vasculitis, 17.62

	INTRODUCTION

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Primary angiitis of the central nervous system (CNS) is a rare and idiopathic disorder that results in multifocal inflammation of the small arteries and veins of the cortex and leptomeninges (1–5). Results of small case series have suggested a favorable response to corticosteroids and immunosuppressive therapy when compared to natural history (6,7). Untreated, primary angiitis of the CNS is generally fatal (4,8).

The antemortem diagnosis of primary angiitis of the CNS remains challenging. Brain biopsy provides a definitive diagnosis, but it is invasive and findings may be negative in some patients with primary angiitis of the CNS because of sampling error (5,9). Given these limitations of brain biopsy, some authors have recommended presumptive treatment of primary angiitis of the CNS on the basis of clinical history and typical arteriographic findings (7,10). The purpose of the present study was to retrospectively determine the sensitivity and specificity of cerebral angiography for the diagnosis of primary angiitis of the CNS.

	MATERIALS AND METHODS

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Patients
This retrospective study was performed with approval from our institutional review board. Informed consent was not required by our institutional review board. The computerized database of the Division of Neuropathology of the Department of Pathology and Immunology at our institution was searched for names of patients who had undergone brain biopsy between January 1, 1992, and January 1, 2000, at Barnes-Jewish Hospital and for whom the term vasculitis appeared in the neuropathology report either in the clinical summary, indications, or description. A total of 73 adult patients were identified.

The medical records of all 73 patients were retrospectively reviewed (Y.K., A.A., C.P.D.) for clinical, imaging, and laboratory information. Patients were included in our study if a cerebral angiogram had been obtained prior to biopsy and vasculitis was listed as a possible diagnosis prior to biopsy. Thirty-eight (13 men and 25 women) of the 73 patients met these criteria. The mean age of the 38 patients was 55 years (range, 29–88 years). The mean interval from angiography to biopsy was 17 days. The median interval was 7 days.

Cerebral Angiographic Imaging and Report Review
Cerebral angiography had been performed by using one of two dedicated biplane neuroangiographic units (Neurostar; Siemens, Erlangen, Germany). Transfemoral access was used for all patients. Thirty-five of the studies included selective catheterization of both common carotid arteries and at least one vertebral or subclavian artery. There were three single-vessel carotid artery studies. These studies were directed as a result of focal abnormalities (mass or hemorrhage) at brain imaging. Anteroposterior, lateral, and oblique magnified views were obtained for all carotid injections. All studies had been performed and findings were interpreted under the supervision of one of three fellowship-trained attending staff interventional neuroradiologists (C.P.D., C.J.M., D.T.C.). At the time of the first dictated report, C.P.D. was just out of training, D.T.C. had been out of training for 5 years, and C.J.M. had been out of training for 12 years.

The angiography reports were reviewed by an investigator (Y.K. or C.P.D) blinded to the results of brain biopsy. Angiographic findings were categorized as typical for vasculitis (isolated multiple cerebral arterial segmental narrowings [5,11,12]), normal, or other abnormal findings.

Biopsy Examination
In all cases, the biopsy examination included a sample of the cortical surface and adjacent leptomeninges. Specimens were examined by a neuropathology fellow and an attending staff neuropathologist.

The histopathologic diagnosis of primary angiitis of the CNS used at our institution required the fulfillment of three criteria (2,9). First, there must be a transmural inflammation of small- or medium-sized blood vessels of the meninges and/or cortex of the brain. Inflammatory infiltrate is predominantly lymphocytic with variable number of plasma cells, histiocytes, neutrophils, and eosinophils. Granulomas, which consist of Langerhans or foreign-type multinucleated giant cells, may or may not be present. Second, there must be a fibrinoid necrosis of the vessel wall. Third, alternative diagnoses must be excluded.

Five fellowship-trained neuropathologists evaluated the specimens during the course of the study. At the time of their first dictated report for these patients, one had just completed training, two had 1 year, one had 2 years, and one had 17 years of experience after completion of training. The neuropathology reports were reviewed (A.A., C.P.D.) for the diagnosis of primary angiitis of the CNS.

Data Management
A spreadsheet was created to include the following data for each patient: age at biopsy, sex, interval between biopsy and angiography, biopsy results, biopsy location, attending neuropathologist, angiographic results, number of angiographic views obtained (including magnified views), attending neuroradiologist, results of follow-up angiography (if performed at our institution), and results of prebiopsy brain imaging (A.A., C.P.D).

Statistical Analysis
The numbers of patients with false-positive (angiogram typical for vasculitis but no primary angiitis of the CNS at biopsy), true-positive (typical angiogram and primary angiitis of the CNS at biopsy), false-negative (no typical angiographic findings but primary angiitis of the CNS at biopsy), or true-negative (no typical angiographic findings and no primary angiitis of the CNS at biopsy) cerebral angiograms were determined (C.P.D). Sensitivity was calculated as the proportion of patients with primary angiitis of the CNS at biopsy and an angiogram demonstrating typical features of vasculitis. Specificity was calculated as the proportion of patients without primary angiitis of the CNS at biopsy and an angiogram without typical findings of vasculitis. Tabulation of data and calculation of sensitivity and specificity were performed by two authors (Y.K., C.P.D.).

	RESULTS

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Cerebral Angiography
Fourteen of 38 patients were considered to have typical findings of vasculitis. Atherosclerotic changes in extracranial vessels or more proximal portions of the internal carotid artery were also observed in eight of the 14 patients. The angiographic findings were considered normal in 11 of the 38 patients. Ten of the 38 patients had angiographic findings that were consistent with extracranial atherosclerotic disease. Five of these 10 patients also had irregularity of the contour of one or both carotid siphons, one of whom also had minimal caliber changes in the intracranial arteries that were considered to be atherosclerotic in nature. The remaining three of the 38 patients had abnormal study findings that did not fit the three categories; one patient had slow filling of an isolated angular branch of the middle cerebral artery, one patient had diffuse abnormal parenchymal blush with areas of early venous drainage, and one patient had an isolated stenosis of a P1 segment of the posterior cerebral artery.

Biopsy
None of the 14 patients with angiographic findings typical of vasculitis had a biopsy finding that was positive for primary angiitis of the CNS (60% specificity). Another pathologic diagnosis was found at biopsy in six of these patients, and the remaining eight patients had nonspecific biopsy results (Table). Follow-up angiography had been performed in three of the eight patients. One patient demonstrated complete or near complete resolution of the multiple intracranial stenoses, and two patients showed an interval increase in the number and severity of the intracranial stenoses (Figure).

View larger version (105K): [in this window] [in a new window] [Download PPT slide]   Figure a. (a) Oblique lateral angiogram of middle cerebral artery branches in a 37-year-old woman after injection of contrast material into the right common carotid artery shows new focal arterial narrowings (arrows) compared with (b) angiogram obtained 23 months prior, which shows some of the sites of narrowing (*). Similar lesions were identified after the injection of contrast material into contralateral carotid artery. Brain biopsy showed abnormal leptomeningeal vessels with thick eosinophilic and collagenized walls. Congo red stain for amyloid resulted in negative findings. No evidence of inflammation or vasculitis was present. CADASIL was considered but rejected given the lack of family history and absence of a granular eosinophilic appearance of the vessel walls. The final diagnosis was vasculopathy. Patient was treated with steroids and immunosuppressive drugs, but disease progressed clinically and angiographically.

View larger version (84K): [in this window] [in a new window] [Download PPT slide]   Figure b. (a) Oblique lateral angiogram of middle cerebral artery branches in a 37-year-old woman after injection of contrast material into the right common carotid artery shows new focal arterial narrowings (arrows) compared with (b) angiogram obtained 23 months prior, which shows some of the sites of narrowing (*). Similar lesions were identified after the injection of contrast material into contralateral carotid artery. Brain biopsy showed abnormal leptomeningeal vessels with thick eosinophilic and collagenized walls. Congo red stain for amyloid resulted in negative findings. No evidence of inflammation or vasculitis was present. CADASIL was considered but rejected given the lack of family history and absence of a granular eosinophilic appearance of the vessel walls. The final diagnosis was vasculopathy. Patient was treated with steroids and immunosuppressive drugs, but disease progressed clinically and angiographically.

	DISCUSSION

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Several important conclusions may be drawn from these data. First, the typical angiographic features of vasculitis—multiple segmental narrowings of cerebral arteries—do not reliably identify patients with primary angiitis of the CNS, as was determined at leptomeningeal brain biopsy with use of neuropathologic criteria (2,9). In this group of 38 patients suspected of having vasculitis and who had undergone brain biopsy, none of the 14 patients with these angiographic findings had proved primary angiitis of the CNS (60% specificity), while the two patients with proved primary angiitis of the CNS did not have typical angiographic findings. Second, many patients with clinical and angiographic features of vasculitis are found to have other pathologic diagnoses. Third, the nature of vasculopathy in patients with multiple segmental arterial narrowings and negative brain biopsy findings is unknown, and it is unlikely to be primary angiitis of the CNS.

One problem with the published data regarding the accuracy of angiography for the diagnosis of primary angiitis of the CNS is the rigorousness with which the diagnosis is confirmed. Many series (7,13,14) have used angiography as a diagnostic criterion that could be substituted for biopsy: A tissue diagnosis was never made in some patients in these studies. Given the data from the present study, many of the patients may have had other specific diseases. In addition, the pathologic criterion for the diagnosis of primary angiitis of the CNS has been liberal in many studies. Some studies have included patients with varicella zoster infection (15), and others have not required transmural inflammation or vessel necrosis (16). The criteria used in the present study are conservative and consistent with the original reports of primary angiitis of the CNS (2,9).

Because only two patients in this series had biopsy-proved primary angiitis of the CNS, no strong conclusions may be drawn regarding the sensitivity of angiography for this disease. Neither patient had typical findings of multiple segmental arterial narrowings. The sensitivity of cerebral angiography may be low in patients with biopsy-proved primary angiitis of the CNS. In an autopsy series, findings have shown that primary angiitis of the CNS typically, but not invariably, involves small arterioles and venules less than 300 µm in diameter (1–5). These vessels are below the resolution of conventional digital subtraction angiographic equipment (17,18). Newer, higher resolution systems may provide better visualization of these vessels. Although film hard-copy systems provide better spatial resolution than does digital subtraction angiography, facilities, including ours, may no longer have film hard-copy capability. Selective internal carotid injections, rather than the common carotid injections performed in most of our patients, may have provided a better view of any subtle luminal irregularities, if present, in these two patients. Vollmer and colleagues (19) reported a patient with a biopsy-proved primary angiitis of the CNS and a normal angiogram and reviewed the literature. They identified 39 patients with histologically proved primary angiitis of the CNS who had undergone angiography or imaging before death or biopsy. A total of 27% of angiograms obtained in 31 of the 39 patients were typical for vasculitis. Typical findings at angiography were found in only one of three patients with proved primary angiitis of the CNS in a series reported by Koo and Massey (20). Histologic changes in primary angiitis of the CNS in the two patients with normal angiograms were limited to arterioles and venules less than 300 µm in diameter.

The poor specificity of cerebral angiography for the diagnosis of primary angiitis of the CNS is also not surprising, since the angiographic appearance of multiple segmental arterial narrowings is nonspecific. The list of possible causes is long and includes intracranial atherosclerotic disease, vasospasm, and many other entities, some vasculitic in nature (11,12,21–23). One such entity may be CADASIL. One patient in our series with an angiogram typical of vasculitis was found to have CADASIL at biopsy. Two patients with CADASIL and angiographic findings suggestive of vasculitis have been reported in the literature (24,25).

It is possible that some of the patients in our study had false-negative biopsy findings owing to the patchy distribution of histologic involvement. In addition, the site of biopsy may not have been in the territory of the arterial abnormality. The frequency of false-negative biopsy findings is low, however, particularly when both brain and leptomeninges are sampled. One of 15 patients in an autopsy series reported by Lie (5) had negative antemortem biopsy findings. Younger et al (9) reviewed the literature for histologically proved primary angiitis of the CNS (using strict pathologic criteria similar to those of the current study) and reported nondiagnostic pathologic findings in only two of 35 biopsies of brain and leptomeninges.

The nature of the vasculopathic process in patients with negative biopsy findings is unknown. Brain biopsy is limited to small leptomeningeal vessels. Large-diameter arteries such as those typically identified at angiography are not generally sampled. The angiographic findings were dynamic in nature in all three patients who underwent follow-up studies, indicating an active vasculopathic process. Call and co-workers (23) described four patients with severe headache and reversible large-vessel stenoses. Three of the four patients were treated with steroids or cyclophosphamide, however. Calabrese et al (26) have described a benign angiopathy of the CNS that had a different clinical profile than that in most patients with primary angiitis of the CNS. It is important to note that biopsies had not been performed in these patients. The diagnosis was made on the basis of angiographic and clinical findings. On the basis of the results of the present series, it is likely that these patients have had a variety of different conditions.

Alreshaid et al (27) reported the clinical outcomes at 1 year of 25 patients suspected of having primary angiitis of the CNS and who had nondiagnostic brain biopsy findings. Good outcome was observed in six of 10 treated patients and in eight of 15 untreated patients. Eighteen of the 25 patients underwent cerebral angiography and are included in the present study. Eight of the 18 patients had typical findings of vasculitis at angiography; three of them underwent repeat angiographic studies and had nondiagnostic biopsy findings.

This was a retrospective review and therefore subject to limitations. The analysis was limited to patients who had undergone angiography and biopsy at our institution. Many additional patients may have been treated empirically on the basis of clinical history and angiographic findings. The reasons for pursuing biopsy rather than empiric treatment are multifactorial, subjective, and difficult to define. It is possible that some of these patients had primary angiitis of the CNS and that our study findings therefore underestimate the sensitivity of angiography in the diagnosis of this disease.

In conclusion, most patients suspected of having primary angiitis of the CNS and with angiographic findings of multiple segmental arterial narrowings do not have primary angiitis of the CNS. These angiographic findings are frequently associated with other specific pathologic diagnoses, which emphasizes the importance of brain biopsy in the care of these patients. The etiology of vasculopathy in patients with negative biopsy findings is unknown. The dynamic nature of the angiographic findings in some patients, as well as the high frequency of nondiagnostic biopsy findings, suggest the possible common presence of a large artery cerebral vasculopathy (or vasculopathies) that is not primary angiitis of the CNS.

	FOOTNOTES

 
Abbreviations: CADASIL = cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy, CNS = central nervous system

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, C.P.D.; study concepts and design, all authors; literature research, C.P.D., W.J.P., Y.K.; clinical studies, C.P.D., C.J.M., D.T.C., A.A.; data acquisition, C.P.D., Y.K., A.A.; data analysis/interpretation, all authors; statistical analysis, C.P.D.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, all authors

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2333031621v1 233/3/878    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kadkhodayan, Y. Articles by Derdeyn, C. P. Search for Related Content PubMed PubMed Citation Articles by Kadkhodayan, Y. Articles by Derdeyn, C. P.