International
Journal
of Nuclear
Medicine
and Biology,
1977, Vol. 4. pp
1 -I?.
Pergamon
Press
Printed
in Northern
Ireland
Scintigraphy of Meningiomas: Radiologic-Pathologic Correlations in 32 Cases* R. FARKAS,
E. BINET,
J. G. McAFEE
and B. MARKARIAN
Divisions of Nuclear Medicine and Diagnostic Radiology, Department of Radiology, and Department of Pathology, Upstate Medical Center, State University of New York, Syracuse, New York (Received 28 May 1976; and in final form 21 August 1976)
Ninety per cent of meningiomas were detectible by radioisotopic imaging in both the authors’ series of 32 patients and in a review of the literature, a slightly lower accuracy than by cerebral angiography. These tumors were best demonstrated in images taken 1-2 The tumor concentration min after the intravenous injection of 99mTc pertechnetate. tended to fade after one to several hours, unlike the majority of intracerebral tumors which often show an increasing concentration with time. Eighty-one per cent of these meningiomas showed increased perfusion in “lirst transit” rapid sequential images, usually appearing about 15 set after injection. This abnormal perfusion tends to be more marked, appears later and persists longer than in most intracerebral neoplasms. The perfusion study does not improve the tumor detection rate but helps to identify them as meningiomas. A reasonable correlation was found between the degree of increased tumor perfusion and the intensity of the angiographic tumor stain. Both, however, failed to correlate to the degree of tumor vascularity evaluated histologically. No distinguishing features were found in the radioisotopic studies or angiographically between the four major histological types of meningioma, except that the angioblastic type invariably showed marked vascularity. IN THIS report, the scintigraphic, angiographic and pathologic findings in 32 patients with meningiomas were reviewed, in order to assess the relative value of rapid sequential gamma camera images versus early and delayed gamma camera images. These scintigraphic findings were compared also with those of other intracranial tumors.
tories were reviewed independently. The cerebral imaging studies were performed 30 min or more following the oral administration of 0.25-0.5 g of potassium perchlorate. Fifteen mCi of 99mTc sodium pertechnetate were administered by rapid intravenous injection and images were obtained with Nuclear-Chicago HP scintillation cameras with high sensitivity 15,000-hole collimators. These rapid sequential images (sometimes called “flow”,? “perfusion,” or “dynamic” studies) were obtained
METHODS The study includes all patients with histologically proven meningiomas seen at the Upstate Medical Center between 1968 and 1972, on whom cerebral scintigraphy and cerebral angiography were performed prior to surgery. The radioisotopic rams, histological sections
t In this presentation, “perfusion” will be used to qualitatively refer to the relative concentration of intravascular radioactive pertechnetate in one area compared to another during its first transit through the brain dependent on both intravascular volume and blood flow. In contrast, the term “flow” is used widely as a quantitative term to refer to blood flow (nutritional and non-nutritional) in cm3 per min, or cm3 per min per unit of organ mass.
images, angiogand clinical his-
* This work was supported in part by USPHS Training Grant No. GM-01583. I
I
2
R. Farkas, E. &net, J. G. McAfee and B.Markarian
in either the anterior or posterior projection such that the suspected lesion was closer to the detector. Polaroid images were exposed every 3 set, beginning 6 set after injection. During the last year of this project, additional 70 mm images were exposed automatically every 1.5 set for about 30 sec. After this sequential series, detailed static images were obtained with a pre-set count of 300,000 in anterior, posterior and both lateral projections beginning 1-2 min after injection (hereafter called “early images”). A set of delayed images was obtained in these same projections, usually 3 or 4 hr after injection (hereafter called “delayed” images). Frequently an additional vertex view was taken. RESULTS There were 32 patients with proven meningiomas in this series; 20 females and 12 males. The ages ranged from 25 to 79 yr, with a median age of 55 yr. Two-thirds of the patients were in the age range from 40 to 70 Yr* The initial rapid sequential images revealed increased perfusion at the tumor site in 26 of the 32 patients, striking in intensity in twelve (Figs. 2 and 4), but barely perceptible in six (Fig. 3). No abnormalities in perfusion were detected in the remaining six patients (19%). The intensity of the lesions was invariably less on the rapid sequential images than on the early detailed images, suggesting that considerable diffusion of the radioactive tracer into the tumor bed occurred within the first one or two minutes after intravenous injection. Furthermore, nine meningiomas that showed minimal or no increased perfusion on the initial rapid sequential images exhibited a marked intensity on the early detailed images. The “early” and “delayed” radioisotopic images were positive in 29 of the 32 patients with meningioma. False negative studies occurred in two meningiomas which arose primarily from the meninges of the craniovertebral junction and extended through the foramen magnum into the posterior fossa. One of these was extremely large and exhibited marked calcification radiographically (Fig. 1). The third missed diagnosis was a small en plaque lesion near the optic foramen
and adjacent right cribriform plate. In 24 studies, the localized increase in activity due to the tumor was more intense, and appeared slightly larger in the early images than in the delayed images (Figs. 2 and 3). In no instance did the tumor activity completely disappear on the delayed images. No change in intensity from immediate to delayed images was detected in four instances (Fig. 4) and only one tumor increased in intensity on the delay images (Fig. 6). On early images, the intensity of the lesions was rated as “high” in 22 cases, compared with only 6 on the delayed images. Thus, in the majority, the intensity appeared to fade with time. As a rule, the configurations of the carotid, middle cerebral and anterior cerebral arteries are first visualized on the rapid sequential images about 9 set after the intravenous injection of 99mTc pertechnetate. The abnormal tumor perfusion usually appeared later, between 12 and 18 sec. The appearance of the increased tumor perfusion demonstrable in 26 of the meningiomas was compared with that of a series of 26 intracranial tumors other than meningiomas. No consistent differences in tumor perfusion were discovered between the two groups. Wide variations were found in the time intervals between injection and maximal tumor perfusion. Moreover, the intensity and duration of the tumor perfusion varied greatly in both meningiomas and other tumor types. However, the typical meningioma tended to have a longer total perfusion time: i.e. the maximum perfusion often persisted up to 27 set after injection. Only one meningioma demonstrated a short perfusion time less than 9 set, as compared with eight non-meningiomas. The remaining meningiomas demonstrated maximum tumor perfusion up to 27 set, compared with only one non-meningioma. For comparative purposes, the meningiomas in this series were divided into two groupssuperficial and deep lesions. The superficial tumors tended to exhibit a higher intensity than the deeper lesions on both the rapid sequential images and the detailed images. In the rapid sequential studies, 6 out of the 21 superficial lesions showed a marked intensity as compared with only 2 out of the 11 deep lesions. Likewise, in the early images, 16 of
FIG. 1. Large psammomatous meningioma right posterior fossa, not demonstrated by radioisotopic imaging. 61-yr-old male with lo-yr history of ataxia, memory loss and spasticity of lower limbs. A, B, C and D-early detailed radioisotopic images in various projections, the rapid sequential films and delayed images (not shown) failed to show any abnormality. E and F-large calcified mass right posterior fossa. G and H-lateral polytomograms show downward extension to foramen magnum.
FIG. 2. Angioblastic meningioma. 30-yr-old male with headache and blindness in left eye for two years. A and D-selected 3 set exposures 18 and 27 set after injection show marked perfusion in tumor area. B and E-early detailed anterior and left lateral images display marked tumor activity in left parasellar area which fades on the delayed images C and F at 5 hr. Carotid angiogram, G, A.P. projection capillary phase, H and I lateral projection, arterial and capillary phases, respectively, show tumor medial left sphenoid wing protruding into optic foramen. Dense tumor stain with large venous sinusoids.
5
FIG. 3. Transitional (psammomatous) meniugioma. 62-yr-old female with seixures for 8 months. A-3 set posterior image 24 set after injection shows barely detectible increase in vascularity in tumor region. D-anterior, B-posterior and E-left lateral, early detailed images show high convexity tumor. C and F--5&r posterior and left lateral images show slight fading compared with earlier views. G-lateral radiograph shows prominent middle meningeal grooves, minimal hyperostosis and punctate calcification. H and I-mid-arterial and venous subtraction films from left common carotid angiogram. Dilated middle meningeal artery, but no evidence of tumor stain. The venous angle is closed.
6
FIG. 4. Recurrent vascular fibroblastic meningioma, arising from right petrous bone. 40-yrold female; anterior portion of tumor partially resected 2 yr previously. Recent ataxia, dysphagia, right facial weakness, unequal pupils. A, B and C-selected 3 set exposures 15, 21 and 27 set post injection. Note persistent area of markedly increased vascularity. D and E-early posterior and right lateral films show high concentration in the tumor posteriorly. F-right lateral film at 1 hr. Tumor activity is unchanged. G and H-AP and lateral subtraction films, right carotid angiogram, venous phase. Dense non-homogeneous tumor stain with venous sinusoids, arising from medial petrous apex.
FIG. 5. Endotheliomatous en plaque meningioma with hyperostosis. 4%yr-old female. Progressive proptosis left eye for three years, left frontal headache, narrowing left visual field. A and D-selected l-5 set 70 mm frames 18 and 24 set after pertechnetate injection. Slight, persistent increase in vascularity lower left temporal region B and E-anterior and left lateral images at 1 hr show same increase in activity in anterior temporal region as in earlier images. C and F--corresponding images 2 hr following administration of 15 mCi of 9qmTc methylene diphosphonate (skeletal agent) shows markedly increased concentrations left temporal bone and orbit. Above studies failed to differentiate meningioma with hyperostosis from fibrous dysplasia G, H and I-left internal carotid angiogram. Marked hyperostosis on left. Bowing anterior cerebral. superomedial displacement middle cerebral artery. Enlarged recurrent meningeal branch of ophthalmic artery supplies tumor (arrow).
FIG. 6. Endotheliomatous meningioma with recent large subdural hematoma. 72-yr-old female. Right-sided seizures for 6 months, severe headache for 3 days and comatose for 1 day. A and D-3 set images at 18 and 24 set after injection. The increased perfusion in the left parasagittal tumor appeared late. Any decreased perfusion lateral to the tumor on the left side was not appreciated. B and E-posterior and left lateral early images show the tumor well. C and F-corresponding images at 2 hr shows obvious change in the tumor concentration. Subdural hematoma not demonstrated. G and H-left common carotid arteriogram, arterial phase. Left parietal subdural hematoma on AP view. Faintly staining extracerebral mass causing lateral displacement and bowing of callosomarginal artery. I-venous phase. Closed venous angle. Draining veins circumscribe the mass. Note impingement on a segment of the superior sagittal sinus.
Scintigraphy of meningiomas
the 21 superficial lesions showed a marked intensity compared with 6 of the 11 deep lesions. This difference in intensity may be explained by the greater in vivo absorption of the gamma photons from the deeper lesions. As one would expect, larger lesions tended to exhibit a higher intensity than the smaller ones. Correlation
with radiographic
findings
Cerebral angiography demonstrated a mass lesion in 3 1 out of 32 patients. The single false negative occurred with a small en plaque meningioma of the optic foramen and cribriform plate without vascular displacement or tumor stain (also not detected by radioisotopic imaging). The tumor stain identified on the cerebral angiogram had a homogeneous appearance in 13 patients (Fig. 2), was non-homogeneous in 12 patients (Fig. 4), and was not visible in 7 patients (Fig. 3). The intensity of the tumor stain was considered marked in 8 patients. Neovascularity (discrete tumor vessels) was present in 20, marked in 9, and absent in 11 instances. In the majority, the intensity of the perfusion as seen in the initial sequential radioisotopic images matched the intensity of the angiographic tumor stain. In 3 instances, the angiographic stain was more marked than the radioisotopic perfusion, because the latter study was performed in the posterior projection whereas the lesions were actually located anteriorly. In 3 other instances, a localized increase in perfusion was observed in the radioisotopic study in the absence of an angiographic stain. On the other hand, there were two instances where an arteriographic stain was visible without detectible increase in perfusion radioisotopically. A poor correlation was obtained between the intensity of the early or delayed detailed images and the angiographic tumor stain. Correlation ings
with surgical and pathological
find -
The area of increased activity on the immediate detailed radioisotopic images as a rule corresponded closely with the size, configuration and site of the tumor found at surgery. For the larger lesions, it was found
9
that the anatomical site of origin of the tumor often could not be discerned on the imaging studies. In this series, the exact anatomical site of the extracerebral origin of the tumors was discerned more accurately by cerebral angiography. Histological sections from 31 of the 32 meningiomas were available for review. The lesions were classified according to the histological ty es described by RUSSELL and (“’ . Twenty-one tumors were enRUBENSTEIN dotheliomatous (meningioendotheliomatous, meningiothelial or synctial), 3 fibroblastic (fibrous), 4 transitional (psammomdtous), and 3 angioblastic. None of the tumors was malignant. The degree of vascularity of each tumor was graded histologically. All three angioblastic lesions were highly vascular histologically. They demonstrated a marked increase in perfusion and high degree of activity on the detailed radioisotopic images and marked neovascularity by angiography (Fig. 2). Otherwise, no correlation could be demonstrated between the pathological type of meningioma or estimated vascularity on histological section, and any of the characteristics noted radioisotopically. The two tumors in the posterior fossa not demonstrated on the imaging studies were transitional (psammomatous) tumors (see Fig. 1). The small lesion near to optic foramen missed both on the isotopic study and by angiography was an endotheliomatous lesion. No clear relationship could be discerned between the angiographic tumor stain and the histological type. Of 13 cases exhibiting a homogeneous stain, 11 were endotheliomatous; of 12 cases with a non-homogeneous stain, 6 were endotheliomatous, 2 fibroblastic, 2 transitional and 2 were angioblastic lesions. Out of 6 cases without visible angiographic staining, 4 were endotheliomatous and 2 were transitional. DISCUSSION In this series of 32 histologically-proven meningiomas, the overall accuracy of detec-. tion by gamma camera imaging with 99mTc as pertechnetate was 90%, similar to a larger series collected from the literature in which
10
R. Farkas, E. Binet, J. G. McAfee and B. Markarian
both pertechnetate and older radioisotopic agents were used, chiefly with rectilinear scanning (Table 1). Detailed camera images beginning about l-2 min after injection appeared most useful in demonstrating intracranial meningiomas. Two posterior fossa transitional lesions arising from the crania-vertebral junction and one small endotheiiomatous tumor of the optic foramen were missed by the imaging method in the present series. Other workers also have failed to detect lesions in the posterior fossa(2’10) and small parasellar tumors.(1’20’33)While the detection of lesions arising primarily in the posterior fossa is apparently excellent, those arising in the upper cervical spine and extending through the foramen magnum may be missed. Rapid sequential images obtained every l-3 set during the first transit of radioactivity through the head following a bolus intravenous injection demonstrated increased perfusion in the tumor area in 81% of the cases in this series. An incidence of increased perfusion of 71% was encountered in another reTABLE 1. Diagnostic
cently reported
series of 28 meningiomas.(31) demonstrated that hydrophilic tracers injected through the carotid arteries remain intravascular during the first transit through the brain. This is true even for small molecules without plasma protein binding such as 24Na. Less than 0.6% of these radioactive tracers perfuse into normal brain tissue during the first transit. Therefore, the first sequential images with “‘“Tcpertechnetate reflect only the intravascular distribution of radioactivity. Although these sequential dynamic studies evidently do not improve the ability to detect meningiomas, they do assist in differentiating these tumors from other lesions. The tumor perfusion tends to be more marked in meningiomas than in most malignant gliomas and in those cerebral metastases which are vascular. The increased tumor perfusion tends to appear slowly, typically at 15 set, well after the ilrst appearance of radioactivity in the carotid and major cerebral arteries at about 9 sec. In only 16% of the LASSEN et ~1.“” previously
accuracy of scanning in diagnosis of meningioma: the literature
Authors Brinkman, C. A. et al. (1962)‘6’ McAfee, J. G. & Fueger, G. F. (1964)‘20’ Afifi, A. K. et al. (1965)“’ Bucy, P. C. & Ciric, I. S. (1965)“’ Bull, J. W. D. & Marryat, J. (1965)“’ Goodrich, J. K. & Tutor, F. T. (1965)‘13’ Myhre, K. et al. (1965)‘22’ Overton, M. C. et al. (1965)‘24’ Spencer, R. (1965)‘33’ Allen, M. B. et al. (1967)‘2’ Witcofski et al. (1967)‘39’ Lango, E. R. er al. (1968)“8’ (posterior fossa only) van Eck, J. H. M. & Woldring, M. G. (1969)@@ Forster, D. M. C. & Bethell, A. N. (1969)‘“’ Spalding, D. G. (1969)‘32’ Wang, Y. ( 1969)‘37’ Cowan et al. (1973)“” Present authors (1973) Total
No. of cases
summary of selected series from
No. of positive diagnoses
13 23 10 15 8 16 21 24 5 11 5
10 21 9 14 8 16 14 21 4 9 5
6 30 15 10 11 8 32
6 27 15 10 10 6 29
263
234 (89%)
No. of doubtfuls 2
1 0
2 1
0
0
No. of false negatives 1 2 1 0 0 0 7 1 1 1 0 0 3 0 0 1 2 3 23
(2.36%)
11
Scintigraphy of meningiomas
current series did the tumor perfusion appear earlier at about 9 set after injection. The increased perfusion tends to persist longer than in most other types of tumors. These differences in perfusion of meningiomas have been previously noted by other workers (10*25,3*)Other vascular lesions such as large aneurysms and arteriovenous malformations tend to appear immediately on perfusion studies, if they are seen at a11.(38)A good correlation between the intensity of the radioisotopic perfusion and intensity of the angiographic tumor stain was observed both in the present series and in that of SHELDONand SMOAK.‘~~’ Neither of these findings, however, appeared to correlate with the degree of vascularity observed histologically. The early detailed images beginning approximately 1 min after injection revealed a greater concentration of radioactivity within these tumors than in the first transit images, suggesting a rapid diffusion of the radioactivity into the tumor bed. Some lesions with a high concentration of radioactivity on both early and delayed images had no demonstrable increase in perfusion on the initial sequential study. Delayed images obtained l-5 hr after injection usually showed a lesser tumor concentration, more discrete tumor margins, and a slightly diminished size, as compared with the early images. In serial images of meningiomas obtained at frequent intervals for 30 min after injection, PENNMG(*~)observed that the lesions reached maximum intensity and size from 2 to 8 min after injection. The explanation for the apparent decrease in size of the lesions with time is not known; perhaps it is due to a faster diffusion of radioactive ions from the periphery of the tumor where the venous drainage is better than in the tumor center. Angiographically, a tumor stain was observed in 81% in the current series. This figure is in reasonable agreement with an incidence of 75% in another study.(3*) The stain is homogeneous’17,34’; nonetheless, about half of the cases of the current series had nonhomogeneous stains, similar to those observed in other cerebral tumors. The tumor stain tends to persist 8 or 9 set longer than in other tumors.“” This apparently
parallels the long persistence of tumor perfusion observed in the first transit sequential radioisotopic images. In the present series, neither the findings by radioisotopic imaging nor cerebral angiography could be related to the histological types of meningioma.(2g*40*41)All three angioblastic lesions appeared highly vascular on both types of examination. Nonetheless, according to TELENIUS(~~), about 20% of angioblastic meningiomas exhibit poor vascularity, both angiographically and histologically. CONCLUSIONS (1) In the performance of gamma scintigraphy for the diagnosis of intracranial meningiomas using ““‘Tc-pertechnetate, early images in multiple projections, beginning one or two min after injection, are most valuable for demonstrating the maximum intensity and extent of the lesion. (2) Rapid sequential images obtained immediately after the intravenous injection of ““‘Tc-pertechnetate appear Valuable in characterizing meningiomas. These “dynamic studies” have not improved the ability to detect the presence of meningiomas, but the demonstration of markedly increased tumor perfusion maximal up to 27 set after injection increases the probability of diagnosis of meningioma. A majority of meningiomas (81%) do exhibit abnormal tumor perfusion radioisotopically. Usually, the degree of increased tumor perfusion correlates with the intensity of the angiographic tumor stain, but does not correlate with the degree of vascularity assessed in histological sections of the tumor. (3) Delayed camera images from one to five hr after injection usually show the lesions with lesser intensity. They are helpful in the differentiation from other intracranial tumors, since the majority of gliomas and metastases reveal a greater intensity on delayed images.‘*@ (4) A minority of meningiomas (10% in the present series) are not demonstrable by current radioisotopic imaging technics, employing ““‘Tc-perttchnetate and the scintillation camera.
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R. Farkas, E. Binet, J. G. McAfee and B. Markarian
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