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Volumetric Assessment of Tumor Infiltration of Adjacent White Matter Based on Anatomic MRI and Diffusion Tensor Tractography

Rationale and Objectives

To perform a retrospective, quantitative assessment of the anatomic relationship between intra-axial, supratentorial, primary brain tumors, and adjacent white matter fiber tracts based on anatomic and diffusion tensor magnetic resonance imaging (MRI). We hypothesized that white matter infiltration may be common among different types of tumor.

Material and Methods

Preoperative, anatomic (T1- and T2-weighted), and LINESCAN diffusion tensor MRI were obtained in 12 patients harboring supratentorial gliomas (World Health Organization [WHO] Grades II and III). The two imaging modalities were rigidly registered. The tumors were manually segmented from the T1- and T2-weighted MRI, and their volume calculated. A three-dimensional tractography was performed in each case. A second segmentation and volume measurement was performed on the tumor regions intersecting adjacent white matter fiber tracts. Statistical methods included summary statistics to examine the fraction of tumor volume infiltrating adjacent white matter.

Results

There were five patients with low-grade oligodendroglioma (WHO Grade II), one with low-grade mixed oligoastrocytoma (WHO Grade II), one with ganglioglioma, two with low-grade astrocytoma (WHO Grade II), and three with anaplastic astrocytoma (WHO Grade III). We identified white matter tracts infiltrated by tumor in all 12 cases. The median tumor volume (± standard deviation) in our patient population was 42.5 ± 28.9 mL. The median tumor volume (± standard deviation) infiltrating white matter fiber tracts was 5.2 ± 9.9 mL. The median percentage of tumor volume infiltrating white matter fiber tracts was 21.4% ± 9.7%.

Conclusions

The information provided by diffusion tensor imaging combined with anatomic MRI might be useful for neurosurgical planning and intraoperative guidance. Our results confirm previous reports that extensive white matter infiltration by primary brain tumors is a common occurrence. However, prospective, large population studies are required to definitively clarify this issue, and how infiltration relates to histologic tumor type, tumor size, and location.

According to the Central Brain Tumor Registry of the United States, the incidence of primary benign and malignant brain tumors in this country is 14.1 patients per 100,000 individuals per year (6.8 per 100,000 individuals per year for low-grade tumors, and 7.3 per 100,000 individuals per year for malignant tumors) ( ).

The survival of patients harboring primary brain tumors appears to be influenced by a variety of factors, such as age, histologic tumor type, gender, preoperative Karnofsky performance score, epilepsy as presenting symptom, tumor involvement of the contralateral hemisphere, and extent of tumor resection ( ).

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Materials and methods

Patient Population

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Table 1

Patient Population and Tumor Characteristics

Case No. Sex, Age (y) Tumor Location Histopathology Eloquent Cortical and White Matter Areas Affected 1 F 33 L frontal Astrocytoma WHO II SMA, motor strip, motor pathway 2 F 34 R temporal Oligodendroglioma WHO II Wernicke’s area, optic radiation 3 F 62 L frontal Oligodendroglioma WHO II SMA, motor pathway 4 M 62 R frontal medial Anaplastic Astrocytoma Motor strip, motor pathway 5 M 38 L frontal Astrocytoma WHO II Motor strip, motor pathway 6 F 45 L fronto-parietal Anaplastic Astrocytoma Motor and sensory strip, motor pathway, arcuate (superior longitudinal) fasciculus 7 F 46 R occipital Oligodendroglioma WHO II Optic radiation 8 M 23 R insular Ganglioglioma Motor pathway, uncinate fasciculus 9 F 18 R frontal Anaplastic Astrocytoma (WHO III) Motor strip, motor pathway 10 M 49 L frontal Oligodendroglioma WHO II SMA, motor pathway, corpus callosum 11 M 47 L fronto-temporal Mixed Oligoastrocytoma WHO II Broca’s area, uncinate fasciculus 12 F 56 L fronto-parietal Oligodendroglioma WHO II Motor and sensory strip, motor pathway, arcuate fasciculus

WHO: World Health Organization; SMA: Supplementary Motor Area.

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Image Acquisition

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Diffusion Tensor Imaging

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Image Analysis

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Results

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Figure 1, Left frontal oligodendroglioma World Health Organization Grade II. (a) Postcontrast, axial three-dimensional spoiled gradient echo recall; (b) axial T2-weighted fast spin echo; (c) coronal view at the level of the posterior limb of the internal capsule; two-dimensional diffusion tensor magnetic resonance imaging visualization overlaid on the corresponding T2-weighted baseline slice (the lines represent the in-plane fibers, whereas the through-plane fibers are represented as yellow dots); note the tumor infiltration of descending fibers (arrows); (d) coronal view at a level located posterior from the slice in (a) ; fiber tracts in this area are displaced by the tumor mass (arrowheads).

Figure 2, Right temporal ganglioglioma. (a) Axial three-dimensional spoiled gradient echo recall (3D-SPGR); (b) axial T2-weighted fast spin echo; the tumor exerts mass effect on the right cerebral peduncle and right optic tract (arrows); (c) 3D tractography registered with the 3D-SPGR scan; corticospinal fibers (yellow) traversing the medial aspect of the tumor; red: manual segmentation of the tumor mass; green: manual segmentation of the tumor region intersected by corticospinal fibers.

Figure 3, Left frontotemporal oligodendroglioma World Health Organization Grade II. (a) Axial T2-weighted fast spin echo; (b) color-coded two-dimensional diffusion tensor magnetic resonance imaging visualization overlaid on the corresponding T2-weighted slice; the tumor is outlined in dark green; areas of high fractional anisotropy (light blue lines) within the tumor confines, corresponding to infiltrated white matter fibers, are outlined in red; (c) three-dimensional tractography overlaid on the baseline T2-weighted acquisition (left lateral view); note the uncinate fasciculus (arrows) running through the T2-hyperintense tumor mass.

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Table 2

Volumetric Assessment of White Matter Infiltration

Case No. Tumor Volume (mL) Tumor Volume Infiltrating Fiber Tracts (mL) Fraction of Tumor Volume Infiltrating Fiber Tracts (% of Total Tumor Volume) 1 33.7 4.8 14.2 2 51.3 13.7 26.7 3 32.3 2.4 7.4 4 9.3 2.6 28.0 5 28.3 3.5 12.4 6 62.6 23.1 36.9 7 9.2 2.6 28.3 8 13.0 2.0 15.4 9 91.8 22.6 24.6 10 87.7 30.7 35.0 11 52.8 5.7 10.8 12 70 12.8 18.3

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Discussion

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Acknowledgments

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