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Evaluating Pediatric Brain Tumor Cellularity with Diffusion-Tensor Imaging

¹ Department of Pediatrics, St. Louis Children's Hospital, Rm. 3S34, One Children's PI., St. Louis, MO 63110.
² Department of Neuroradiology, Mallinckrodt Institute of Radiology, Washington University Medical Center, Box 8131, 510 S. Kingshighway Blvd., St. Louis, MO 63110.
³ Departments of Pathology and Neuropathology, Washington University School of Medicine, Box 8118, 660 S. Euclid Ave., St. Louis, MO 63110.
⁴ Department of Pediatric Neurology, St. Louis Children's Hospital, St. Louis, MO 63110.
⁵ Department of Pediatric Neurosurgery, Medical College of Wisconsin, 9000 W. Wisconsin Ave., P. O. Box 1997, Milwaukee, WI 53201.
⁶ Department of Pediatrics, Washington University School of Medicine, Box 8116, St. Louis, MO 63110.

Received December 1, 2000; accepted after revision February 16, 2001.

 
Supported by the American Academy of Pediatrics Resident Research Grant.

Address correspondence to K. M. Gauvain.

Abstract

Top Abstract Introduction Materials and Methods Results Discussion References

 
OBJECTIVE. MR imaging of central nervous system (CNS) malignancies falls short of a definitive evaluation. Tissue diagnosis remains the gold standard. Diffusion-tensor MR imaging measures the apparent diffusion coefficient and diffusion anisotropy of water in tissue. The purpose of this study was to test the hypothesis that the apparent diffusion coefficient may improve the MR imaging evaluation of newly diagnosed CNS neoplasms. We examined the relationship between the apparent diffusion coefficient, anisotropy, and tumor cellularity in 12 pediatric patients.

MATERIALS AND METHODS. On the basis of histopathologic evaluation, tumors in this case series were segregated into three types: low-grade gliomas, embryonal tumors, and nonembryonal high-grade tumors. Mean apparent diffusion coefficient and anisotropy values obtained from the solid components of each tumor were compared with cellularity, total cellular area, and total nuclear area derived from biopsy material.

RESULTS. The apparent diffusion coefficient ratio (tumor to normal brain) correlated well with tumor classification (p = 0.001). Anisotropy was decreased similarly in all tumor classifications. The absolute apparent diffusion coefficient correlated well with cellularity (p = 0.014) and total nuclear area (p = 0.005) per high-power field. The correlation between apparent diffusion coefficient and total cellular area per high-power field was not statistically significant.

CONCLUSION. The apparent diffusion coefficient may be predictive of tumor classification and may be a useful tool in characterizing tumor cellularity and total nuclear area. These parameters are not available in standard MR imaging. Therefore, diffusion-tensor imaging may enhance the diagnostic process in pediatric CNS malignancies.

Introduction

Top Abstract Introduction Materials and Methods Results Discussion References

 
Pediatric central nervous system (CNS) tumors encompass a heterogeneous group of cell types [1]. Clinical treatment and prognosis varies with tumor type, grade, stage, and extent of resection. Conventional MR imaging incorporating contrast-enhanced T1-weighted and T2-weighted sequences helps to characterize the location and extent of these tumors, but MR imaging provides limited information regarding tumor type and grade. Consequently, conventional MR imaging falls short as a definitive diagnostic examination; that role is reserved for histopathologic evaluation after biopsy.

Diffusion imaging produces images in which relative intensity is related to microscopic displacement of water molecules [2]. Diffusion-tensor imaging is a more sophisticated quantitative form of diffusion imaging. For diffusion-tensor imaging, water diffusion is measured in several orientations relative to the sample. When these measurements are combined, it is possible to calculate not only an absolute measure of average water diffusion for each voxel (the apparent diffusion coefficient) but also a measure of how water diffusion varies along different axes of the image (diffusion anisotropy). Water diffusion is anisotropic in white matter, for example, with diffusion coefficients measured parallel to nerve fibers being higher than those measured perpendicular to them. Overall, both apparent diffusion coefficient and diffusion anisotropy reflect the microstructure of the tissue in which they are measured.

The purpose of this study was to determine if quantitative diffusion-tensor imaging improves the MR imaging of pediatric CNS malignancies in vivo by comparing the tumor apparent diffusion coefficient to light microscopic features. We hypothesized that the most cellular tumors and those with the least amount of cytoplasm (greater nuclear area) would have the lowest apparent diffusion coefficient values. This information could play an important adjunctive role in the workup and treatment of pediatric CNS neoplasms.

Materials and Methods

Top Abstract Introduction Materials and Methods Results Discussion References

 
The protocol described in our study was approved by the institutional review board at our institution. As a first step, diffusion-tensor imaging was added to the tumor MR imaging protocol. We then retrospectively reviewed our clinical experience over an 18-month period for tumors that met predefined inclusion criteria. Each pediatric patient enrolled in our study had preresection pretreatment MR imaging at our institution that included diffusion-tensor imaging. Furthermore, each patient included in the study had an intraaxial mass with solid portions suitable for region of interest (ROI) analysis. Finally, the resection should have been performed at our institution to enable histopathologic analysis of the specimen. Patients who had preoperative examinations at other institutions, patients who were treated before imaging, and patients with extraaxial or entirely cystic tumors were excluded.

We retrospectively screened 35 consecutive patients to identify those who met these criteria. Twelve patients (six boys, five girls, one infant) were included in the subsequent analysis. The diagnoses were histologically confirmed in all patients. The number of each tumor type was small; therefore, we subdivided each tumor into three basic categories: low-grade (World Health Organization, grade I-II) gliomas (n = 4), nonembryonal high-grade (World Health Organization, grade III-IV) tumors (n = 4), and embryonal tumors (n = 4) (Table 1).

All examinations were performed on a 1.5-T system (AnalyzeAVW software; Mayo Clinic Foundation, Rochester, MN) with circularly polarized head coils. The diffusion-tensor—imaging protocol (TR/TE, 3000.0/97.4) consisted of a single-shot multisection spin-echo echoplanar pulse sequence with a 24 x 24 cm field of view, 5-mm section thickness, and a 1-mm gap between sections [3, 4]. Four tetrahedrally oriented diffusion-weighted images (diffusion sensitivity, b = 1012.4 sec/mm²), three orthogonally oriented diffusion-weighted images (b = 337.5 sec/mm²), and a reference T2-weighted intensity image (b = 0.0 sec/mm²) were obtained at each transverse section. Fourteen transverse sections were acquired in 35 sec with a 96 x 128 voxel matrix (2.50 x 1.88 x 5.00 mm voxels), interpolated to a 192 x 256 pixel matrix. All images were realigned in two dimensions, with a combination of intra- and cross-modality affine realignment procedures, to correct for image displacements and linear stretch and shear due to eddy currents [4]. For technical reasons, the diffusion-tensor images must be oriented in the transverse plane relative to the magnet bore. The diffusion-tensor images were, therefore, not necessarily acquired in register with those of the conventional MR sequences in the clinical neuroimaging protocol, which were oriented along the plane parallel to the anterior commissure and posterior commissure.

For each pixel, the elements of the diffusion tensor were derived from this combination of tetrahedral and perpendicular diffusion measurements [3, 4]. The reference T2-weighted intensity image was not included in the diffusion-tensor calculations because of the presence of artifacts in some studies that arose from spurious free induction decay signal. The apparent diffusion coefficient, a measure of the directionally averaged magnitude of diffusion with units of mm²/sec, was computed as one third of the trace of the diffusion tensor.

The MR images were analyzed as follows: we used T2-weighted images and enhanced T1-weighted images to define the slice to be analyzed, to exclude regions of hemorrhage, and to distinguish cystic from enhancing solid portions of the mass (Figs. 1A,1B,1C,2A,2B,2C,3A,3B,3C). We drew ROIs on the apparent diffusion coefficient and anisotropy maps, using AnalyzeAVW software (Mayo Clinic Foundation, Rochester, MN) in areas of solid tumor (Figs. 1A,1B,1C,2A,2B,2C,3A,3B,3C). As many as three ROIs were drawn on one or two transverse slices. Areas of edema, cystic change, and central necrosis were excluded from the analysis.

View larger version (133K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —8-year-old girl with juvenile pilocytic astrocytoma. Gadolinium-enhanced T1-weighted image reveals mass in mid cerebellum with large enhancing nodule.

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —8-year-old girl with juvenile pilocytic astrocytoma. Turbo spin-echo T2-weighted image obtained at same level as A shows cystic component of mass and surrounding edema in cerebellum.

View larger version (102K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —8-year-old girl with juvenile pilocytic astrocytoma. Apparent diffusion coefficient image obtained at the same level as A with regions of interest (ROIs) shows that one ROI represents solid portion of mass. Other two ROIs are averaged to represent normal cerebellum.

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —10-year-old girl with glioblastoma multiforme. Gadolinium-enhanced T1-weighted image shows mass in right thalamus with heterogeneous enhancement.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —10-year-old girl with glioblastoma multiforme. Turbo spin-echo T2-weighted image obtained at same level as A shows hyperintense mass and surrounding edema.

View larger version (88K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —10-year-old girl with glioblastoma multiforme. Apparent diffusion coefficient image obtained at same level as A with regions of interest (ROIs) shows that one ROI represents solid enhancing portion of mass, whereas other ROI represents normal brain in contralateral hemisphere.

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —2-year-old boy with atypical teratoid-rhabdoid tumor. Gadolinium-enhanced T1-weighted image reveals lobulated mass in basal ganglia region of left lateral ventricle with heterogeneous enhancement.

View larger version (120K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —2-year-old boy with atypical teratoid-rhabdoid tumor. Turbo spin-echo T2-weighted image obtained at same level as A shows that mass is isointense to gray matter.

View larger version (99K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —2-year-old boy with atypical teratoid-rhabdoid tumor. Apparent diffusion coefficient image obtained at same level as A with three regions of interest (ROIs) shows that ROIs in left hemisphere are averaged to represent solid enhancing portion of mass. Single ROI in right hemisphere serves as control region in normal brain.

ROIs were obtained from contralateral homologous brain regions to serve as control regions. The apparent diffusion coefficient and anisotropy values were computed from the mean of the pixel values obtained for the ROIs placed on these images. When more than one region was drawn, the mean apparent diffusion coefficient and anisotropy values were calculated from all regions and averaged by the number of pixels. The ratio of the apparent diffusion coefficient to contralateral control brain region was then computed (apparent diffusion coefficient ratio) (Table 1). This computation was performed because apparent diffusion coefficient values of normal brain vary with age [5], and the contrast achieved between tumor and surrounding tissue depends on this ratio. One author drew all ROIs, and proper placement was confirmed by a consensus of a board-certified radiologist and an attending neuroradiologist with a certificate of added qualification in neuroradiology.

A board-certified attending neuropathologist performed the histopathologic analysis. Tumor cellularity was defined as the number of cells across a single representative high-power field (Fig. 4A,4B,4C,4D). We measured average cellular and nuclear diameters for each tumor, using an ocular micrometer. Total cellular area was computed from the measured cell area of each tumor cell type multiplied by the number of cells per high-power field. Total nuclear area was computed from the measured nuclear area of each tumor cell type multiplied by the number of cells per high-power field. The neuropathologist was blinded to the MR imaging findings and the apparent diffusion coefficient values for each tumor. We made statistical comparisons of apparent diffusion coefficient ratio to normal brain with tumor type, using one-way analysis of variance. Statistical comparisons of the absolute apparent diffusion coefficient values with tumor cellularity and with total nuclear area were made with linear regression analysis and Pearson's correlation coefficient. Absolute apparent diffusion coefficient values were used for this comparison to evaluate the possibility that apparent diffusion coefficient values change with these parameters. Ratios to normal brain tissue were not used in this case because it is unlikely that apparent diffusion coefficient values change with the age of the subject (i.e., with the apparent diffusion coefficient values of normal brain).

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —Photomicrographs of histopathologic specimen from each of tumor categories. Tumor in 8-year-old girl with juvenile pilocytic astrocytoma is characterized by low cellularity, small nuclear size, and microcystic stroma. (H and E, x 400)

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —Photomicrographs of histopathologic specimen from each of tumor categories. Glioblastoma multiforme in 10-year-old girl has moderate cellularity and moderate nuclear size. (H and E, x200)

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —Photomicrographs of histopathologic specimen from each of tumor categories. Tumor in 14-year-old boy with medulloblastoma has high cellularity with small cells containing minimal cytoplasm. (H and E, x200)

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —Photomicrographs of histopathologic specimen from each of tumor categories. Tumor in 13-year-old girl with large cell medulloblastoma is highly cellular with large cells containing moderate cytoplasm. (H and E, x400)

Results

Top Abstract Introduction Materials and Methods Results Discussion References

 
The apparent diffusion coefficient values for low-grade gliomas are 1.33 ± 0.21 x 10^-3 mm²/ sec (range, 1.132-1.60 x 10^-3 mm²/sec) with a ratio to normal brain of 2.10 ± 0.35 (range, 1.75-2.54) (Fig. 5). The nonembryonal high-grade tumor apparent diffusion coefficients are 1.22 ± 0.09 x 10^-3 mm²/sec (range, 1.128-1.303 x 10^-3 mm²/sec) and ratio to normal brain, 1.6 ± 0.15 (range, 1.45-1.8) (Fig. 5). The group of embryonal tumors (primitive neuroectodermal tumor, medulloblastoma, malignant teratoid-rhabdoid tumor) have apparent diffusion coefficient values of 0.72 ± 0.20 x 10^-3 mm²/sec (range, 0.538-0.974 x 10^-3 mm²/sec) and a ratio to normal brain of 1.03 ± 0.26 (range, 0.7-1.26) (Fig. 5). There is a clear distinction between the low-grade gliomas and the embryonal tumors, with the high-grade nonembryonal tumor group (glioma, germ cell, and ependymoma) having some overlap (p = 0.001). Apparent diffusion coefficient values are inversely correlated with tumor cellularity (Fig. 6); the apparent diffusion of water is slower in tumors with higher cellularity. This relationship is statistically significant (p < 0.05). In addition, apparent diffusion coefficient is inversely correlated with the estimated total nuclear area (p < 0.01) (Fig. 7). The anisotropy values were decreased to near zero in all tumors and, thus, were not analyzed further. Total cellular area was computed and compared with the apparent diffusion coefficient values, but this correlation did not reach statistical significance in this study.

View larger version (8K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —Graph shows comparison of apparent diffusion coefficient ratio and tumor classification. Analysis of variance data is the following: n = 12, mean = 1.577 ± 0.5196, and p = 0.001. ADC = apparent diffusion coefficient.

View larger version (10K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —Graph shows comparison of apparent diffusion coefficient value and tumor cellularity. Pearson's correlation coefficient is -0.684, with a significance of 0.014. ADC = apparent diffusion coefficient.

View larger version (10K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7. —Graph shows comparison between apparent diffusion coefficient value and total nuclear area. Pearson's correlation coefficient is -0.752, with a significance of 0.005. ADC = apparent diffusion coefficient.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Diffusion imaging has been widely used in the evaluation of acute cerebral ischemia [6, 7]. The mechanism of the decrease in apparent diffusion coefficient observed with recent stroke is controversial [8, 9], but imaging findings are quite reliable. Diffusion imaging is also useful in distinguishing tumor from abscess [10,11,12,13]. These studies have shown that the apparent diffusion coefficient values of abscess fluid are markedly lower than those of cystic or necrotic portions of tumor. This difference is thought to be due to the impeded water mobility of purulent fluid related to its high cellularity and viscosity [13]. Diffusion imaging has also been shown to distinguish epidermoid from arachnoid cysts [14, 15]. Arachnoid cysts are characterized by free diffusion similar to that of cerebrospinal fluid. Epidermoids, conversely, show slower diffusion, presumably as a result of the more complex nature at the microscopic level, which impedes water diffusion. These observations prompted this investigation of the relationship of the apparent diffusion coefficient of water to the complexity of the tissue sample at the microscopic level.

In our study, the apparent diffusion coefficient correlated significantly with both the tumor cellularity and the calculated total nuclear area. The apparent diffusion coefficient of the 13-year-old girl with medulloblastoma was seen as an outlier in the tumor cellularity graph. This feature can likely be explained by the large cell pathology of this medulloblastoma. This patient had a high calculated total nuclear area but had lower cellularity (Fig. 4D). This tumor displayed restricted diffusion presumably because of the densely packed nature of the tumor cells and the high nuclear-to-cytoplasm ratio.

To our knowledge, published data characterizing diffusion in pediatric brain tumors are limited. Several studies have shown that different components of tumor, surrounding edema, and normal surrounding white matter have different apparent diffusion coefficient values [16,17,18,19,20,21]. Cystic and necrotic portions of tumor have higher apparent diffusion coefficient values, reflecting the increased water movement characterizing these components. Tien et al. [17] used diffusion-weighted imaging along a single axis to show that enhancing components of highgrade gliomas have a lower apparent diffusion coefficient than nonenhancing tumor and peritumoral edema. Brunberg et al. [19] found a distinction between apparent diffusion coefficient and diffusion anisotropy from normal white matter and solid enhancing tumor, cystic and necrotic areas, and regions of edema. They did not find a difference in apparent diffusion coefficient values between various glioma subtypes. Sugahara et al. [2] showed a trend similar to our study by comparing high- and low-grade gliomas to cellularity defined as the total area of nuclei of tumor cells divided by the area of histologic section. They concluded that apparent diffusion coefficient correlated with tumor cellularity.

A previous case report postulated that the densely cellular nature and high nuclear-to-cytoplasmic ratio of medulloblastoma restricts extracellular diffusion of water [22]. However, no quantitative data were presented to support this hypothesis. Our data support this hypothesis by showing that these tumors have apparent diffusion coefficient values of less than 1.0 x 10^-3 mm²/sec, consistent with reduced diffusion.

Chenevert et al. [23] used a rat—brain tumor model to show that diffusion measurements are sensitive to chemotherapy induced changes. Apparent diffusion coefficient values were obtained pretreatment, after treatment, and during tumor regrowth. Results indicated that the apparent diffusion coefficient values increase with therapy and return to the pretreatment levels during tumor regrowth. The increase in apparent diffusion coefficient during therapy suggests an increase in interstitial volume and cellular permeability from tumor-cell necrosis. Further investigation along these lines could lead to new ways of evaluating tumor response to therapy.

Our study is limited by the small number of patients and by the heterogeneous sample of tumors. ROIs analyzed on MR images may not precisely correspond to the biopsy specimens used in the pathologic evaluations. Finally, our values for the total nuclear area are calculated estimates and are not actual measurements. Despite these limitations, we believe that the observations are potentially clinically significant. All studies were performed preoperatively, and thus, there were no influences of surgery or prior therapy. Further studies in this pediatric population are needed to determine the role of this modality in clinical decision-making.

In conclusion, we found that apparent diffusion coefficients of pediatric brain tumors are significantly correlated with tumor cellularity and total nuclear area. Quantitative diffusion imaging may enhance the diagnostic process and may be predictive of patient clinical outcome before tissue sampling of pediatric CNS malignancies.

Acknowledgments
 
We thank Thomas K. Pilgram for expert advice on the statistical analyses used in this investigation.

References

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