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1
Department of Radiology, Neuroradiology Division, Duke University Medical
Center, Box 3808, Durham, NC 27710-3808.
2
Duke University School of Medicine, 131 Davison Bldg., Duke University Medical
Center, Box 3005, Durham, NC 27710.
3
Department of Radiology, University of Virginia Health Sciences Center,
Charlottesville, VA 22908.
4
Department of Community and Family Medicine, Biometry Division, Duke
University Medical Center, Durham, NC 27710-3808.
5
Department of Pathology, Duke University Medical Center, Durham, NC
27710-3808.
Received January 28, 1999;
accepted after revision August 23, 1999.
Address correspondence to J. M. Provenzale.
Abstract
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MATERIALS AND METHODS. Our study population consisted of 15 female patients and 10 male patients with a mean age of 20 years. The early childhood group was composed of six children with a mean age of 5.5 years. The older group was composed of 19 patients with a mean age of 25.6 years. We assessed tumor volume, tumor location, percentage of tumor that was cystic, pattern of contrast enhancement, and degree of edema.
RESULTS. The temporal lobe was the most common tumor location in both groups. Mean tumor volume in the early childhood group was 83 cm3, which was significantly larger than the mean tumor volume (9.78 cm3) for the older group (p = 0.001). Cystic tumors were more common in the early childhood group (83%) than in the older group (63%), and the average percentage of cysts in the cystic tumors was much higher in the early childhood group (67%) than in the older group (30%). Contrast enhancement was seen in five of six early childhood tumors and 13 of 16 tumors in older patients. Four of six tumors in the early childhood group and five of 19 tumors in the older patient group had associated edema.
CONCLUSION. The mean tumor volume of gangliogliomas in the early childhood group was significantly larger than that of the older patient group. This finding may be indicative of differences in tumor growth patterns in the two groups, ability of the hemicranium to adjust to mass effect in childhood, or sampling error as a result of a relatively small sample size.
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4 cm in
diameter) and predominately cystic, unlike the small, predominately solid
lesions shown in adults in published reports. In fact, other groups of
investigators have described examples of such large gangliogliomas in children
[4,5,6].
We set out to compare MR imaging characteristics of gangliogliomas in young
children with those in the population over the age of 10 years, with
particular emphasis on tumor size and proportion of tumor that was cystic. |
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The total study population consisted of 15 female patients and 10 male
patients, ranging in age from 1 to 48 years (mean age, 20 years). We divided
patients into an early childhood group (<10 years old) and an older group
(10 years old) on the basis of a natural division in the data because we
had no patients in the 8- to 12-year age range and the tumor sizes in the
less-than-10-years age group were so dissimilar from those in the remaining
patient population. The early childhood group was composed of six children
(four boys, two girls) with a mean age of 5.5 years (range, 1-8 years). The
older group was composed of 19 patients (13 females, six males) with a mean
age of 25.6 years (range, 15-48 years).
Imaging sequences included unenhanced T1- and T2-weighted images in all
patients, with contrast material administration in 22 patients. MR imaging
studies were jointly reviewed by two observers who were aware of patient age
and tumor type. Differences between the two observers were resolved by
consensus. The following features were assessed: tumor volume, tumor location,
percentage of tumor that was cystic, pattern of contrast enhancement, and
degree of edema. Tumor volume was calculated using the equation 4 / 3
r3. The percentage of tumor that was cystic was determined by
comparing the diameter of the tumor cyst on cross-sectional images with the
overall diameter of the tumor on those images. Contrast enhancement pattern
was judged to be diffuse, partially enhancing, or nonenhancing. The degree of
edema was judged on a scale of 0 (no edema) to 4+ (marked edema), using the
following criteria: mean diameter of peritumoral edema less than or equal to 5
mm was scored as 1+; 6-10 mm (inclusive), 2+; 11-15 mm (inclusive), 3+; and
greater than 16 mm, 4+. Imaging characteristics were compared for these two
groups.
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To test the hypothesis that differences in tumor volumes between the two groups were a result of histologic differences between tumors, the histologic specimens of 13 patients available at one of the institutions involved in this study were reviewed by one of the authors. This group included four patients less than 10 years old and nine patients at least 10 years old. Tumors were assessed for mitotic activity as determined by the Mib-1 index (an index of <1% is considered evidence of a low-grade neoplasm [7]. All tumors were found to have a mitotic index of less than 1%, indicating that all tumors assessed in this manner were low grade.
To determine whether an increased ability of the brain and calvaria to remodel and accommodate for the tumor mass in the early childhood group might have allowed tumors to grow to large sizes (with a possible delay in transmission of mass effect), we measured the area of the hemicranium on the side of tumor involvement and compared it with the area of the contralateral hemicranium in all six patients in the younger age group and in a sample of five patients in the older age group. The areas of the two hemicrania were compared using the signed rank test. We found that the hemicranium containing the tumor was larger than the opposite hemicranium in all six patients less than 10 years old (Fig. 4), with a mean difference of 12% (p = 0.03). In the older age group, no difference in size of the two hemicrania was noted.
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Tumor Location
Tumor locations in the early childhood group included the temporal lobe
(three patients, including one in whom the lesion extended into the parietal
lobe), frontal lobe (one patient), occipital lobe (one patient), and basal
ganglia (one patient). In the older patient group, 15 temporal lobe lesions,
one parietal lobe lesion, one frontal lobe lesion, one occipital lesion, and
one cerebellar lesion were seen. To test the hypothesis that differences in
the mean size of tumors between the two groups might have been related to
tumor location (i.e., patients with tumors in eloquent cortex might have
undergone imaging earlier, when tumors were smaller, than patients with tumors
located in noneloquent cortex), we recorded whether tumors were located in
eloquent cortex (including primary motor cortex, primary sensory cortex,
internal capsule, language centers, medial temporal lobe and hippocampus, and
brainstem). Three of the six patients in the early childhood group were found
to have tumors located in eloquent brain regions (medial temporal lobe or
hippocampus in two patients, primary motor cortex in one patient), and six of
19 patients in the older group were found to have tumors in eloquent brain
regions (medial temporal lobe or hippocampus in four patients, primary sensory
cortex in one patient, midbrain involvement in one patient). Thus, the two
groups did not substantially differ from one another by frequency of
involvement of eloquent brain regions.
Cystic Components
In the early childhood group, five (83%) of six patients had cystic tumors
and the percentage of cysts in tumor ranged from 50% to 95% (average, 67%). In
the older group, 12 (63%) of 19 patients had cystic tumors and the percentage
of cysts in tumor ranged from 10% to 95% (average, 30%) (p = 0.1, not
statistically significant). At least 50% of the tumor was cystic in five (83%)
of six early childhood tumors, compared with six (32%) of 19 tumors in the
older patient group. In four (67%) of six early childhood tumors, at least 85%
of the tumor was cystic, compared with four (21%) of 19 tumors in the older
patient group.
Edema
In the early childhood group, four (66%) of six tumors had associated
edema; three lesions were graded 1+ and one lesion was graded 3+. In the older
patient group, five lesions (26%) had associated edema; two lesions were
graded 3+, two lesions were graded 2+, and one lesion was graded 1+.
Enhancement Pattern
Contrast material was administered in all six early childhood patients and
16 of 19 older patients. Contrast enhancement was seen in five six early
childhood tumors and in 13 of 16 tumors in older patients. In all five of the
early childhood patients with enhancing tumors and 12 of the 13 older patients
with enhancing tumors, diffuse homogeneous enhancement of the solid portion of
the tumor was seen. In another adult, only a small portion of the tumor was
contrast-enhanced.
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The imaging features of gangliogliomas, previously reported, include cyst formation in 35-55% of patients and calcification in approximately 35% [2,3,4,5, 9]. Contrast enhancement is reported in approximately one half of tumors [2,3,4,5, 9]. Previous published studies of patients with gangliogliomas have spanned the spectrum from being entirely composed of adults [8] to solely composed of children [10, 11]. With reference to our early childhood group, children younger than 10 years have composed between 5% [3] and 25% [12] of patients in general studies and 55-65% of patients in childhood studies [6, 11]. Although adult gangliogliomas reported in the medical literature are typically 2-3 cm in diameter [2,3,4,5], examples of pediatric gangliogliomas reported in the medical literature are often larger [4,5,6]. Specific radiologic features are not typically discussed in these reports; therefore, no conclusion can be reached solely on the basis of previous studies as to whether the appearance of these tumors differs between young children and the rest of the population.
In this study, we found a statistically significant difference in the size of tumors between two patient groups, with the mean volume of early childhood tumors being approximately eight times that of the remaining population. These results may be accounted for by a number of explanations. One possible explanation is that the early childhood tumors have fundamentally different growth rates from those in the rest of the population. Verification of this hypothesis would have necessitated serial imaging studies in our patients before surgery, which were not performed. Analysis of mitotic indexes of tumors in the two groups did not show a higher mitotic index for the younger patient group, which suggests that faster rate growth alone is not likely to account for the difference in mean tumor volumes. Another possible explanation is that tumors in the older population presented earlier (and at a smaller size) than those in the young childhood group. For instance, it is possible that tumors in the older group more commonly involved eloquent brain regions (such as the motor cortex), causing focal neurologic deficits, or were located in a region of the brain more likely to manifest epileptogenic activity (e.g., motor cortex or mesial temporal lobe). Tumors at such sites would be more likely to be discovered earlier, and at a smaller size, than tumors in noneloquent regions of the brain. However, the regional distribution of the tumors in the two groups was relatively similar, making this hypothesis unlikely. Furthermore, the frequency of tumor in eloquent brain regions did not substantially differ between the two groups, although this similarity could be misleading. For instance, we cannot exclude that in the childhood group, in which tumors were generally large, involvement of eloquent brain regions occurred at a later stage (i.e., after the tumor had already attained large size) than in the generally smaller tumors in the older patient population. If this were the case, frequency of involvement of eloquent brain regions might be similar but such involvement could be an early event in one group (i.e., the older patient group) and a late development in the other group (i.e., the younger patient group). Unfortunately, the available data do not allow this issue to be determined.
We found a small, but statistically significant, difference in size of the two hemicrania in the younger patient group, which may reflect the increased ability of the hemicranium to expand before the closure of cranial sutures, or increased compliance of the calvaria and brain to mold in response to a mass lesion. Such increased compliance in the younger patient group possibly allowed tumors to grow to a larger size (before development of substantial mass effect) than tumors in older patients.
Although the difference in mean tumor size between the two groups was statistically significant, the relatively small size of our population has possibly resulted in a sampling error. Previous reports have shown examples of large neoplasms in adult patients but have not systematically compared tumor size between adult and pediatric groups [4, 5]. Although our study population is larger than those of many studies reported in the medical literature, our patients represent only a small fraction of all patients with this tumor. We recognize that our findings will need to be verified by studying a larger population of patients with this tumor before our results can be generalized.
The location of tumors in both of our patient groups was usually in the temporal lobe, although the frequency of a temporal lobe location was higher in the older patient group (approximately 79%) than in the younger group (approximately 50%). These findings in both patient groups were similar to those generally reported [2,3,4,5, 10]. The frequency of cystic tumors in early childhood (approximately 85%) in our study was higher than that in older patients (approximately 60%), but not in a statistically meaningful way. In addition, the proportion of tumor that was cystic in the early childhood population (approximately 65%) was, on average, slightly more than double the cystic proportion in the older patients. Thus, not only were early childhood tumors slightly more often cystic, but also, when a cyst was present, the cyst accounted for a larger proportion of the tumor. In fact, in four of six early childhood patients, cysts composed at least 85% of the tumor volume, compared with four of 19 older patients.
In conclusion, the gangliogliomas in patients in the younger age group in this study were found to be, on average, significantly larger than those in the older patient group, although no substantial differences were found with regard to tumor location, enhancement characteristics, or edema patterns. As noted, a number of factors may be operative in producing the difference in mean tumor volume between the two groups. However, because our results may represent a sampling error as a result of the small study population, these observations deserve further study in a larger cohort of patients to determine whether our findings are truly representative of gangliogliomas as a group.
Acknowledgments
We thank James Burchette for providing expertise in the evaluation of
immunohistochemical staining material.
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