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Neuroradiology |
1 From the Departments of Radiology (A.C.G., J.M.P.) and Pathology (T.J.C., R.C.D.), Duke University Medical Center, Box 3808, Durham, NC 27710. From the 2000 RSNA scientific assembly. Received March 19, 2001; revision requested April 19; final revision received December 27; accepted January 15, 2002. Address correspondence to J.M.P.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Echo-planar diffusion-weighted magnetic resonance (MR) images obtained in 11 patients with brain lymphomas (19 lesions) and in 17 patients with astrocytomas (19 lesions) were retrospectively reviewed. Regions of interest were drawn on apparent diffusion coefficient (ADC) maps in enhancing tumor. ADC values were normalized by dividing ADC values of tumors by those of normal-appearing regions and expressing the quotient as a ratio. Histologic samples from 11 patients with astrocytomas (11 lesions) and seven patients with lymphoma (seven lesions) were reviewed. Cellularity was measured by calculating the percentage of nuclear area and the percentage of cytoplasmic area and expressing the results as the nuclear-to-cytoplasmic (N/C) ratio. The ADC and N/C ratios of both tumor types were compared by using a two-tailed t test.
RESULTS: Mean ADC ratio of lymphomas was 1.15 (SD, 0.33; standard error of the mean [SEM], 0.10), and that of high-grade astrocytomas was 1.68 (SD, 0.48; SEM, 0.11) (P < .01). Mean N/C ratio of lymphoma was 1.45 (SD, 0.94; SEM, 0.36), and that of high-grade astrocytomas was 0.24 (SD, 0.18; SEM, 0.05) (P < .01).
CONCLUSION: Measurements of water diffusivity and cellularity suggest that higher cellularity contributes to more restricted diffusion.
© RSNA, 2002
Index terms: Astrocytoma, 10.363 • Brain neoplasms, 10.363 • Lymphoma, 10.34 • Magnetic resonance (MR), diffusion study, 10.12144
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Primary CNS lymphoma is an entity that was rarely encountered previously, and it accounted for only 1%–3% of CNS neoplasms prior to 1978 (15). However, incidence has increased drastically since the onset of the acquired immunodeficiency syndrome, or AIDS, epidemic, and CNS lymphomas now represent up to 15% of all brain tumors at some institutions (15). Histologically, primary CNS lymphomas are typically angiocentric tumors that form perivascular cuffs of tumor cells, which infiltrate brain parenchyma either as individual diffusely infiltrating cells or as compact aggregates of tightly packed cells (16). It has been postulated that, because of their high degree of cellularity, lymphomas are hyperattenuating to gray matter on computed tomographic scans and hypointense to gray and white matter on T2-weighted MR images (15).
Increased signal intensity on diffusion-weighted images has also been noted in lymphoma (17–19). To our knowledge, however, quantitative data regarding diffusion-weighted imaging characteristics in these tumors have not been reported, and the findings at imaging have not been correlated with measurements of cellularity. In a recent case report (11) of medulloblastoma, another tumor with high cellularity, the appearance of abnormally high signal intensity on diffusion-weighted images was also noted within the tumor. The hyperintense signal intensity was thought by the authors to reflect relatively restricted water diffusion caused by a combination of densely packed cells and a high nuclear-to-cytoplasmic (N/C) ratio (11). However, measurement of the apparent diffusion coefficient (ADC) was not performed. Furthermore, the authors of that report did not correlate imaging features with cellular density or N/C ratio, and the idea that cellularity was responsible for the observed diffusion-weighted imaging characteristics remained an unproved hypothesis.
The purpose of this study was to determine if water diffusivity of lymphomas and high-grade astrocytomas correlates with cellularity.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Two patients in the lymphoma group and eight patients in the high-grade astrocytoma group had two lesions. Therefore, a total of 19 lymphomas (in 11 patients) and 19 high-grade astrocytomas (in 17 patients) were analyzed. Inclusion criteria for entry into the study were as follows: (a) Patients underwent diffusion-weighted imaging. (b) Patients had lesions that showed a focal solid-enhancing area greater than 2.0 cm2 on contrast material–enhanced T1-weighted MR images. (c) Patients underwent biopsy within 1 month of imaging.
Patient identifiers were removed from image data at the earliest opportunity prior to analysis. A waiver for informed consent was granted by our institutional review board because of the retrospective and anonymous nature of this study.
All studies were performed with 1.5-T clinical MR imaging units (Signa Horizon; GE Medical Systems, Milwaukee, Wis) and circularly polarized head coils. Diffusion imaging was performed in the transverse plane by using a spin-echo echo-planar imaging sequence with the following parameters: repetition time msec/echo time msec/inversion time msec, 12,000/100/2,200; diffusion gradient encoding in three orthogonal directions; b = 1,000 sec/mm2; field of view, 20 x 40 cm; matrix size, 128 x 64 pixels; section thickness, 5 mm; section gap, 2.5 mm; and number of signals acquired, one. T1-weighted sequences were performed in the transverse plane with the following parameters: 500/11; field of view, 22 cm2; matrix size, 256 (frequency) x 192 (phase); section thickness, 5 mm; section gap, 2.5 mm; and number of signals acquired, two. The T1-weighted sequences were performed before and after administration of 0.2 mmol per kilogram of body weight of gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ). The T2-weighted sequence was performed in the transverse plane with 2,800/100. Other parameters were the same as those for the T1-weighted sequences.
ADC values were calculated and were based on the following equation: ln S(G) = ln S(0) - 2[
2 x G2 x 
2 x (
- / 3)] x ADC, where G is the amplitude of the pulsed diffusion gradient, is the gyromagnetic ratio, is the interval between the diffusion gradients, is the duration of the diffusion gradients, S(G) is the signal strength with pulsed diffusion gradient on, and S(0) is the signal strength with the pulsed diffusion gradient off (8). ADC maps were generated with software (Functool; GE Medical Systems) and were registered with contrast-enhanced T1-weighted images. The adequacy of registration was assessed with visual inspection by a single observer (A.C.G.). Uniform regions of interest (ROIs) of 88 mm2 ± 10 (equivalent to 10 pixels ± 1) were manually drawn on ADC maps in areas corresponding to the enhancing portion of lesions to obtain ADC values for lymphomas (ADClym) and high-grade astrocytomas (ADCast).
ROIs were placed centrally within the largest solid-enhancing area of tumor to avoid volume averaging with cystic or necrotic regions that might influence ADC values. Same-size uniform ROIs were also drawn in matching structures in the contralateral hemisphere in each patient to obtain ADC values of normal-appearing white matter (ADCwm) for the purpose of normalization. The matching white matter structure represented either the same structure in the contralateral hemisphere or a comparable structure, if the contralateral hemisphere was involved with tumor. One neuroradiologist (A.C.G.), who was not blinded to the diagnosis, drew all ROIs in lymphomas. Another neuroradiologist drew all ROIs in high-grade astrocytomas. Because the two types of lesions were typically easily distinguishable from one another according to MR imaging appearance, neuroradiologists were not blinded to lesion type when placing ROIs. Methods for drawing the ROIs were the same for both sets of lesions.
Visual Inspection
Three neuroradiologists performed qualitative visual inspection of diffusion-weighted images and ADC maps of lymphomas and high-grade astrocytomas with consensus reading. Each lesion was evaluated as being predominantly hyperintense, isointense, or hypointense to gray matter, and the findings were recorded.
Histologic Data Acquisition
Two pathologists (T.J.C., R.C.D) retrospectively reviewed histologic samples from 11 of 17 patients with high-grade astrocytomas (11 lesions; two evaluated as WHO grade III and nine as WHO grade IV tumors) and samples from seven of 11 patients with CNS lymphoma (seven lesions). The histologic data in the remaining six patients with high-grade astrocytomas and four patients with lymphoma were obtained at other institutions and were not available for the analysis used in this study. One lesion was studied in each of the 11 patients with high-grade astrocytomas and of the seven patients with lymphoma. The neuropathologists were not blinded to the diagnosis and worked in consensus. Six patients who received a diagnosis of high-grade astrocytoma and four patients who received a diagnosis of lymphoma underwent biopsy at other institutions, and their histologic specimens were not available for review. Hematoxylin-eosin–stained sections of 5-µm-thick formalin-fixed paraffin-embedded tissue were examined.
Digital images were captured by using a microscope (BX40; Olympus, Melville, NY) and a digital camera (DEI 750 3 CCD; Optronics, Goleta, Calif). A high-power objective with a magnification of x40 and a camera adapter with a magnification of x0.45 were used to generate an optically magnified image with a magnification of x18, which was captured at a digital resolution of 1,024 x 768 pixels. The digital images were analyzed with image analysis software (Optimas version 6.1; Media Cybernetics, Del Mar, Calif) by keying on color-specific features (blue-staining nuclei and pink-staining cytoplasm). One 0.042-mm2 area of tissue was analyzed for each case. The field to capture was selected in areas of solid tumor growth with the least amount of nonneoplastic tissue, such as blood vessels, necrotic tissue, inflammatory cells, and tissue-sectioning artifacts. Similarly, areas of the brain with single-cell tumor infiltration or reactive gliosis were avoided. This process was performed to analyze as pure a sample of tumor as possible.
The cellularity of each tumor was represented by the N/C ratio, which was calculated by dividing the percentage of the nuclear area by the percentage of the cytoplasmic area. This method of measuring cellularity is similar to the methods used by other investigators who compared diffusion-weighted imaging features with tumor cellularity (9,12). The glial matrix surrounding the cells was also included with the cytoplasmic area. This was unavoidable, because in hematoxylin-eosin–stained sections, individual cell borders are not readily delineated, which precludes distinction of cytoplasm from glial matrix. However, inclusion of the glial matrix is desirable because the N/C ratio calculated with this method correlates closely with tumor cellularity, as defined by the number of cells per given area of histologic field. If the glial matrix were excluded, then hypothetically a specimen that has only a few tumor cells with scanty cytoplasm in a large area filled with glial matrix would have a high N/C ratio but low cellularity. The difference between cellularity and true N/C ratio will be further elaborated in the Discussion section.
Data Analysis
ADC values were normalized for interimager and interimage variability by dividing the ADC value of lymphomas (ADClym) and the ADC value of high-grade astrocytomas (ADCast) by the ADC value of normal-appearing white matter (ADCwm) in the contralateral hemisphere in the same patient. As noted previously, histologic samples were not available for N/C ratio calculation in all patients. Subsequently, ADClym/ADCwm ratios (all lymphoma lesions) were compared with ADCast/ADCwm ratios (all high-grade astrocytomas), and N/C ratios of lymphomas (all lymphomas) were compared with N/C ratios of high-grade astrocytomas (all high-grade astrocytomas) by using a two-sample two-tailed t test, assuming that variance was unequal. A P value of less than .05 was considered to represent a statistically significant difference in all cases.
ADC ratios of individual lesions were correlated with their N/C ratios (in lesions for which histologic samples were available for the calculation of the N/C ratio). The correlation coefficient, r, was obtained with the following equation: r = {covariance (RADC, N/C)/[
(RADC) x (N/C)]}, where RADC is the ADC ratio and is the SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Mean ADClym/ADCwm for all patients with lymphoma (including those in whom an N/C ratio was not available) was 1.15 (SD, 0.33; SEM, 0.10), and mean ADCast/ADCwm was 1.68 (SD, 0.48; SEM, 0.11). Mean ADClym /ADCwm was significantly lower than mean ADCast/ADCwm (P < .01), as demonstrated by means of a t test after a log transformation. Within the group of seven patients with lymphoma and the group of 11 patients with astrocytomas in whom N/C ratios were derived, mean ADClym/ADCwm was 1.15 (SD, 0.38; SEM, 0.14) and mean ADCast/ADCwm was 1.76 (SD, 0.61; SEM, 0.18). The means of the ADC ratios in patients in whom N/C ratios were available were compared after log transformation, which yielded a P value of less than .01.
Measurements of N/C Ratios
The histologic specimens used for N/C ratio calculations showed more densely packed cells in lymphomas than in high-grade astrocytomas (Fig 3). Mean N/C ratio of lymphomas was 1.45 (SD, 0.94; SEM, 0.36), and mean N/C ratio of high-grade astrocytomas was 0.24 (SD, 0.18; SEM, 0.05). The means of the N/C ratios were compared after log transformation, which yielded a P value of less than .01.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Our results revealed that the rate of water diffusion of CNS lymphomas, as represented by ADC values, was significantly lower than that of high-grade astrocytomas (P < .01), and the cellularity of lymphomas, as represented by the N/C ratio, was significantly higher than that of astrocytomas (P < .02). These findings were also consistent with our observations at visual inspection of diffusion-weighted MR images and ADC maps. Lymphomas were generally hyperintense to gray matter on diffusion-weighted images and isointense to hypointense on ADC maps, findings that were consistent with lower diffusivity. In contrast, high-grade astrocytomas were generally hyperintense to gray matter on both diffusion-weighted images and ADC maps. Therefore, the hyperintense appearance of astrocytomas on diffusion-weighted images in the presence of elevated ADC values is likely caused by T2-weighting effects of diffusion-weighted images, or so-called T2 shine-through, rather than by low diffusivity. Both the quantitative measurements and the qualitative observational data showed that the diffusivities of lymphomas and high-grade astrocytomas are inversely related to their cellularities, and these findings suggest that the appearance of tumors on diffusion-weighted images likely reflects their cellularity.
Early investigators (20) in diffusion-weighted imaging have noted that densely packed tumor cells can inhibit effective motion of water molecules and can, therefore, restrict diffusion. In a study of various grades of astrocytomas, investigators (9) also noted that tumor cellularity was inversely correlated with tumor ADC values, and they determined a similar correlation between ADC values and histologic tumor grading. The latter finding is not surprising, because cellularity is one of the features used to determine histologic grading (9). Other studies (6,10) of human astrocytomas also suggested an inverse correlation between diffusivity and cellularity.
In addition, researchers (12) in an investigation of implanted astrocytomas in an animal model noted that ADC values in tumors were inversely correlated with cellularity. Treatment of these tumors produced changes in ADC values that were highly sensitive to changes in tumor cellularity. Because decreasing tumor cellularity is a reflection of cell death and treatment effect, these investigators (12) suggested that diffusion-weighted imaging could provide a surrogate marker for early therapeutic effectiveness. As previously mentioned, the authors (11) of a case report of medulloblastoma also noted increased signal intensity within the tumor on diffusion-weighted images, which was associated with densely packed cells in a histologic specimen. Our results corroborated these previous findings. However, in addition, our results demonstrated a correlation between diffusivity and cellularity across tumor types, which has not been previously shown.
Our quantitative measurements of ADC values in high-grade astrocytomas also correlated well with those in previous studies. In one report, a mean ADC value of (1.2 ± 0.4) x 10-3 mm2/sec for high-grade astrocytomas (n = 17, 16 high-grade astrocytomas and one anaplastic oligoastrocytoma) was reported, and this value is similar to our mean ADC value of (1.21 ± 0.35) x 10-3 mm2/sec (9). Other investigators (6,8,13) measured mean ADC values ranging from (1.1 ± 0.2) x 10-3 mm2/sec to (1.37 ± 0.52) x 10-3 mm2/sec in high-grade glial neoplasms, most of which were astrocytomas. In another study (7), a mean ADC value of (1.31 ± 0.25) x 10-3 mm2/sec in solid contrast-enhancing portions of astrocytomas was reported, although high-grade and low-grade tumors were not measured separately. These ADC values are also in good agreement with our measurements. However, other investigators (6–9,13) did not report measurements of tumor cellularity to allow comparison with our study.
Cellularity of tumors, defined as the number of cells in a given area of tumor tissue, is an important factor that influences microscopic water diffusion in tumors, because it determines the ratio of extracellular to intracellular space in a given area of tissue. It has been shown that water diffusion in biological tissue is highly dependent on the ratio of extracellular to intracellular space (21–23). Furthermore, water diffusivity is greater in the extracellular space compared with that in the intracellular space (23,24). Therefore, an increase in cellularity, which would decrease the fraction of extracellular space, would also likely result in more restricted water diffusion. The importance of the ratio of extracellular to intracellular space in determining water diffusivity has also been noted in other disease processes. In acute cerebral ischemia, the decrease in extracellular-to-intracellular volume ratio is thought to be an important, or even the dominant, mechanism underlying ADC reduction (5,21,23).
Single-neuron MR imaging microscopic studies of water diffusivity have shown that intranuclear water may have a higher diffusion coefficient than has cytoplasmic water (23,24). Findings in other studies (25) concerning the effects of molecular crowding and viscosity on ADC also suggest that water diffusivity is higher in the nucleus compared with that in the cytoplasm owing to decreased molecular crowding. These studies would seem to suggest that tumors with a high N/C ratio would actually have higher (rather than lower) ADC values. However, diffusion measurements in single cells may not adequately reflect diffusion in a multicellular environment. It has been shown that measurement of water diffusion in tissue is affected by diffusion outside the cell as well as that inside the cell (22,24).
In this study, the N/C ratio measured included the extracellular glial matrix as a part of the cytoplasm. Tumors that have a high N/C ratio, such as lymphoma, also tend to have a relatively small amount of extracellular matrix, because there is an increased number of cells per tissue area. As discussed previously, tumors with a smaller extracellular compartment would be expected to have lower ADC values than tumors with a larger extracellular compartment. The amount of extracellular matrix is likely more important than the minor diffusivity difference between nucleus and cytoplasm. Therefore, in tumors with high cellularity (increased N/C ratio but reduced extracellular matrix), the measured ADC value is actually decreased. In other words, it is the cellularity of tumors that is inversely correlated with their diffusivity, and not, strictly speaking, the N/C ratio.
Although our results suggest that diffusivity of brain tumors may generally correlate with their cellularity, it would be premature to state that there is an exclusive cause-and-effect relationship. The assessment of water diffusion in tissue is a complicated issue, which is affected by the viscosity of the medium, barriers to diffusion between compartments, molecular crowding, presence of active transport, bulk flow in capillaries, and the length of diffusion observation (7,25,26). The cellularity of tumor likely contributes to barriers to diffusion and molecular crowding but not necessarily to the other factors.
Although our study findings show a clear inverse association between diffusivity and cellularity when the tumors are considered as groups, the relatively modest correlation (r = -0.46) between ADC values and N/C ratios of individual tumors suggests that there are factors other than cellularity that influence water diffusion. In addition, when we measured tumor diffusivity at the macroscopic level, we could not completely avoid averaging of nontumoral tissue and cellular debris, despite our best efforts to exclude as many artifacts as possible. The inclusion of nontumoral tissue would be expected to introduce a component to the measured ADC values that is not accounted for by tumor cellularity. In addition, the relatively low spatial resolution of our diffusion-weighted images also may have contributed to partial-volume-averaging errors.
One potential limitation of this study is that in approximately one-third of our patients, histologic samples were not available for analysis, which may have introduced a patient selection bias into our N/C ratio data. The statistical analysis would have been more robust if histologic samples had been available in all patients such that the N/C ratio could be calculated for all lesions. To the degree that other institutions may have differing technical procedures, different personnel, and varying patient populations, a bias may have been introduced by a systematic (ie, by institution) pattern of missing data. In addition, the sampling bias within each tumor may also play a role in contributing to variations in ADC measurement that is independent of histologic characteristics of tumor. As mentioned before, there are probably other factors that can affect diffusivity in tumors in addition to cellularity. Unfortunately, it is difficult to control or account for these factors.
Yet another limitation is the fact that two different raters were used to measure ADC values within tumors, and raters could not realistically be blinded to tumor type because of the different appearance of the lesion types on MR images. We attempted to take this limitation into account by having the neuroradiologists use essentially the same size for ROIs in all cases and place the ROI in the center of the contrast-enhancing portion of the tumor for both tumor types. In addition, the neuropathologists measuring histologic data were not blinded to tumor type. The lack of blinding could have biased the results in both cases. Readers familiar with these methods would need to judge to what extent significant bias was likely. In addition, these raters did not undergo reference standard training for obtaining measurements and were not using a formal set of consensus rules. Further studies of this type, taking these limitations into account, are indicated to obtain statistically reliable results.
In conclusion, in this study, measurements of water diffusivity and cellularity in lymphomas and high-grade astrocytomas suggest that high cellularity, not simply a high N/C ratio, leads to more restricted diffusion. To our knowledge, our study is the first in which diffusivity and cellularity of different types of tumors were compared quantitatively and in which diffusivity in lymphomas was quantified. Therefore, other researchers will need to verify our results. If the inverse relationship between diffusivity and cellularity holds true for brain tumors in general, then diffusion-weighted MR imaging of brain tumors may become useful to refine the determination of a diagnosis, to track the histologic progression of low- to high-grade tumors, and to assess the effects of therapy.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, A.C.G., J.M.P.; study concepts and design, all authors; literature research, A.C.G.; clinical studies, A.C.G., J.M.P.; data acquisition, R.C.D., A.C.G., T.J.C.; data analysis/interpretation, all authors; statistical analysis, A.C.G.; manuscript preparation and definition of intellectual content, all authors; manuscript editing, A.C.G., J.M.P.; manuscript revision/review and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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