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Usefulness of diffusion/perfusion-weighted MRI in patients with non-enhancing supratentorial brain gliomas: a valuable tool to predict tumour grading?

Department of Radiology, Second Hospital of China Medical University, No.36 Sanhao St., Heping Dist., Shenyang, Liaoning,110004, People's Republic of China

	Abstract

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22 patients with non-enhancing supratentorial gliomas on contrast-enhanced MRI underwent both diffusion- and perfusion-weighted MRI (DWI/PWI) before surgical resection. 14 low-grade gliomas (WHO Grade I and II) and 8 anaplastic gliomas were verified histologically. Both apparent diffusion coefficient (ADC) values and relative cerebral blood volume (rCBV) ratios were calculated on the solid portion of the tumour, on peritumoural area, as well as on the contralateral normal white matter, respectively. The results showed that lower ADC values were present in the solid portions of anaplastic gliomas, but not in low grade (p<0.01). All ADC values in peritumoural regions of tumours were decreased compared with the contralateral normal white matter. However, there was no significant difference between anaplastic gliomas and low-grade gliomas. Meanwhile, higher rCBV ratios were present in both solid portions and peritumoural regions of anaplastic gliomas, but not in low grade gliomas (p<0.01). In conclusion, non-enhancing brain gliomas with lower ADC values in the solid portions and higher rCBV ratios in both solid portions and peritumoural regions of tumours are significantly correlated with anaplasia. Therefore, DWI and PWI should be integrated in the diagnostic work-up of non-enhancing gliomas in order to predict grading.

	Introduction

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Gliomas are the most common primary neoplasms of the brain, varying histologically from low grade to high grade [1]. MRI plays a crucial role in the evaluation of patients with gliomas [2]. The use of gadolinium-based contrast agents yields further improvement in the demonstration and detection of cerebral gliomas. Patterns and extent of contrast enhancement have been suggestive of a malignant potential [3]. However, this approach is limited because 14–45% of non-enhancing supratentorial gliomas are malignant (especially in older patients) and some enhancing gliomas (i.e. pilocytic astrocytoma) are benign [4, 5]. Moreover, large cerebral gliomas are often histopathologically heterogeneous and may have components of varying grades of malignancy within them. Hence, accurate pre-operative grading of gliomas and planning of adequate treatment strategies are often difficult with conventional MRI [5, 6].

Diffusion-weighted MRI (DWI), which is sensitive to the molecular diffusion of water, has been well established as a reliable non-invasive method for the early detection of cerebral ischaemic stroke, and DWI has been reported to be helpful in differentiating necrotic cavities associated with malignant gliomas from the benign ones [7]. The use of DWI to better characterize enhancing tumours and vasogenic oedema has been explored, but the results obtained have been conflicting [7, 8]. Recent developments in perfusion-weighted MRI (PWI) techniques have permitted the creation of relative cerebral blood volume (rCBV) maps, leading to the qualitative and quantitative assessment of tumour vascularity. These maps have helped in the assessment of tumour grade and in targeting the site of biopsy [8, 9].

Although DWI and PWI have been widely used in pre-operative grading of gliomas, to the best of our knowledge, few studies evaluating the usefulness of diffusion and perfusion MRI solely in non-enhancing gliomas have been reported, although the utility of perfusion MRI in gliomas without enhancement on conventional contrast-enhanced MRI was performed by Maia et al [10]. In addition, the efficiency of peritumour region in the grade assessment of cerebral gliomas is still being investigated.

Our hypothesis was that DWI/PWI could provide additional useful information in the assessment and tumour grading of supratentorial glial neoplasms, which lacked contrast enhancement on pre-operative neuroimaging.

	Materials and methods

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Patient selection and clinical data collection
22 patients (10 women and 12 men; median age 48.3 years, age range 38–68 years) with non-enhancing supratentorial gliomas on contrast-enhanced MRI underwent both diffusion/perfusion-weighted MRI (DWI/PWI) before surgical resection. Informed consent was obtained from all patients prior to the investigation, and all procedures were performed under the approval of our institutional review board for clinical studies. 14 low grade gliomas (WHO Grade I and II) and 8 high grade (WHO Grade III) were verified histologically. Low grade gliomas consisted of low grade astrocytomas (Grade I, n = 7), low grade oligodendrogliomas (Grade II, n = 4) and low grade mixed oligoastrocytomas (Grade II, n = 3); while high grade gliomas consisted of anaplastic astrocytomas (Grade III, n = 5) and anaplastic oligodendrogliomas (Grade III, n = 3).

MRI examination
MRI examinations were performed on 1.5 T superconduction whole-body MR system (Intera Gyroscan; Philips Medical Systems, Best, The Netherlands) and an eight-channel Sensitivity Encoding (SENSE) head coil. After scout view MRI, the examination protocol consists of pre-contrast conventional MRI followed by DWI, PWI, and finally post-contrast T₁ weighted images.

Conventional MR images were obtained with T₁ (spin echo (SE), 442/15) and turbo T₂ (turbo spin echo (TSE), 3235/100) weighted spin echo sequences (both with a 256x192 matrix, 6 mm slice thickness and 2 averages). DWIs were acquired using single-shot echo-planar imaging (EPI) sequence at multiple levels. 18 slices of 6 mm thickness were obtained (repetition time (TR) 5000 ms, echo time (TE) 104 ms, field of view 40x20, matrix size 256x128, b values of 0 and 1000 mm² s^–1) in 3 orthogonal directions.

For susceptibility-based PWI, the transitory signal loss during the bolus passage was detected with a T₂* weighted fast field echo (FFE) EPI sequence (TR 232 ms, TE 25 ms, 6 slices with 6 mm slice thickness; matrix, 89x128; and 1 average). 40 dynamic scans with a time resolution of 1.6 s per image were performed after intravenous bolus injection of 20 ml Gd-DTPA (Magnevist; Schering AG) at a flow rate of 4 ml s^–1 and a 20 ml saline flush.

MR data analysis and statistics
The apparent diffusion coefficient (ADC) maps and values were calculated on a separate workstation (Easy Vision Intera workstation, release 8.1.3; Philips Medical Systems). We recorded the ADC values from both the solid portion of the tumour (seen as the highest signal intensity lesion at b value 0 and 1000) and peritumoural area. The ADC values in our study represented averaged ADCs of three to five regions of interest (ROIs). A ROI, varying from 40 mm³ to 60 mm³, was positioned carefully to avoid contamination from adjacent different tissues. The ROI was drawn as large as possible using a circular ROI on the workstation. As a control, the ADC was obtained from contralateral normal white matter.

Raw PWIs were transferred to a PC workstation (Easy Vision Intera workstation, release 8.1.3; Philips Medical Systems) for post-processing. With the aid of the implemented software, the rCBV could be calculated on the basis of the indicator dilution method and were displayed as spectral colour images. ROI analyses were performed on the solid portion of the tumour, on peritumoural area, as well as on the contralateral normal white matter, respectively. ROI was placed carefully to cover the region of expected maximum rCBV on maps of rCBV. Additionally, we measured the ratio of maximum rCBV in either the tumour or peritumoural area of that in the contralateral normal white matter in order to standardize variations in each examination.

All data obtained were summarized as the mean ± standard deviation (SD). The Student t-test was used to determine if there were statistically significant differences in both averaged ADC value and maximum rCBV ratio between anaplastic gliomas (Grade III) and low grade (Grade I and Grade II) gliomas. A p-value of less than 0.05 was considered to indicate statistical significance.

	Results

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Conventional MRI revealed heterogeneous signal intensity of tumours with clear evidence of central necrosis in all 22 patients. Of all these patients, the solid tumour tissue exhibited typical hyperintense on T₂ weighted images (T2WI) and hypointense on T₁ weighted images (T1WI) (Figure 1). Six of the seven patients with Grade II tumours and all eight patients with Grade III tumours (Figure 2) were found to have peritumoural oedema and mass effect. Infiltration of the tumour producing nodular thickening of the grey matter was seen in three patients with Grade II tumours and five patients with Grade III tumours (Figures 3 and 4). All tumours, however, did not produce significant contrast enhancement on visual assessment, suggesting lack of blood–brain barrier breakdown.

View larger version (167K): [in this window] [in a new window]   Figure 1. MRI and diffusion weighted imaging(DWI) from a patient with anaplastic astrocytoma. (a) T2 weighted image. (b) T1 weighted MR image with contrast material. (c) DWI (b = 1000). (d) Apparent diffusion coefficient (ADC). The tumour exhibited typical hyperintense on T2 weighted images; peritumoural oedema and mass effect was present; no contrast enhancement. On DWIs (b = 1000), the signal intensity in the solid portion of the tumour was hyperintense with respect to the white matter; lower ADC values were present in the solid portions of high grade gliomas.

View larger version (67K): [in this window] [in a new window]   Figure 2. Perfusion weighted imaging(PWI) and histopathological photograph from a patient with anaplastic astrocytoma (same patient as in Figure 1). (a) Relative cerebral blood volume (rCBV) colour map. (b) Signal-intensity time-curve. (c) Histopathological photograph. rCBV maps were inhomogeneous with various increases of signal intensity in both solid portion and peritumoural region of tumour. Histopathological photograph of tumour confirmed the diagnosis of anaplastic astrocytoma.

View larger version (143K): [in this window] [in a new window]   Figure 3. MRI and diffusion weighted imaging(DWI) from a patient of anaplastic astrocytoma. (a) T2 weighted image. (b) T1 weighted MR image with contrast material. (c) DWI (b = 1000). (d) Apparent diffusion coefficient (ADC). The tumour exhibited typical hyperintensity on T2 weighted images; infiltration of the tumour producing nodular thickening of the grey matter was observed. The tumour did not produce significant contrast enhancement on visual assessment, On DWIs (b = 1000), the signal intensity in the solid portion of the tumour was hyperintense with respect to the white matter; lower ADC values were present in the solid portions of high grade gliomas.

View larger version (70K): [in this window] [in a new window]   Figure 4. Perfusion weighted imaging(PWI) and histopathological photograph from a patient with anaplastic astrocytoma (same patient as in Figure 3). (a) Relative cerebral blood volume (rCBV) colour map. (b) Signal-intensity time-curve. (c) Histopathological photograph. rCBV maps were inhomogeneous with various increases of signal intensity in solid portion of tumour. Histopathological photograph of tumour confirmed the diagnosis of anaplastic astrocytoma.

View larger version (138K): [in this window] [in a new window]   Figure 5. MRI and diffusion weighted imaging(DWI) from a patient with low-grade oligodendrogliomas. (a) T1 weighted image. (b) T2 weighted image. (c) DWI (b = 1000). (d) Apparent diffusion coefficient (ADC). The tumour exhibited inhomogeneous with various increase of signal intensity on both T2 weighted image and DWI.

The signal intensity in the peritumoural region was homogeneous on rCBV map in all 14 cases of low-grade (Grade I and Grade II) tumours (Figure 6). However, a slight increase of signal intensity of the tumour was observed in three cases of Grade II tumours and in one case of Grade I tumour. In contrast, all rCBV maps for Grade III tumours were inhomogeneous with various increases of signal intensity in solid portions of tumour (Figures 2 and 4).

View larger version (79K): [in this window] [in a new window]   Figure 6. Perfusion weighted imaging(PWI) and histopathological photograph from a patient with low-grade oligodendrogliomas (same patient as in Figure 5). (a) Relative cerebral blood volume (rCBV) colour map. (b) Signal-intensity time-curve. (c) Histopathological photograph. The signal intensity in both peritumoural region and solid portion of tumour was homogeneous on rCBV map. Histopathological photograph of tumour confirmed the diagnosis of oligodendrogliomas (Grade II).

	Discussion

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DWI has been used by some to evaluate intra-axial tumours [7, 8, 13]. DWI and calculation of ADC values have been used to distinguish the normal white matter areas from necrosis, cyst formation, oedema, and solid tumour by measuring differences in ADC values caused by water proton mobility alterations [13, 14]. These differences are thought to result from both changes in the balance between intracellular and extracellular water and changes in the structure of the two compartments [14]. Our result showed that calculated ADC values from tumoural core added more information to MRI in the differentiation and grading of non-enhancing gliomas; these results suggested different ADC values due to different tumour grades [15]. Although ADC values of biological tissue are determined by many factors, results of previous studies have already confirmed that the lower ADC values in tumour core were mainly affected by tumour cellularity. With higher diffusivity found in the extracellular volume, the increase of intracellular space due to highly cellular tissue is coupled with a decrease of the ADC [8, 15, 16]. Therefore, higher cellularity in anaplastic neoplasm would contribute to the lower ADC values.

Contrary to most previous studies, averaged ADC values in peritumoural area were also analysed in our study. The results showed that ADC values in peritumoural regions were decreased compared with the contralateral normal white matter. It is assumed that malignant gliomas are not strictly focal lesions, but rather are characterized by intracerebral dissemination of malignant glial cells along the myelinized axons and blood vessels, or through the subarachnoid space [8]. We therefore speculated that there might be a difference in the ADC values of the peritumoural region between low grade and high grade gliomas. However, no significant difference was found. We postulate that the ADC value in the peritumoural region is unreliable as a means of differentiating between high grade and low grade gliomas, because a partial volume effect contaminated by surrounding oedema may affect the accurate outcome [8, 17]. Recently, usefulness of diffusion tensor imaging (DTI) in the study of peritumoural region of gliomas has been investigated and the result seems promising [18]. DTI, which is capable of visualizing the anisotropy of proton motion, may make it possible to eliminate the partial volume effect of peritumoural oedema, and the difference between high-grade and low-grade gliomas in this respect seems worthy of evaluation.

For planning the optimal treatment strategy, accurate determination of tumour grade is critical, and in most histological grading systems, vascular proliferation of gliomas is a diagnostic criterion for malignancy [19]. New blood vessel growth is a critical phase of solid tumour growth. The growth of a solid tumour mass at 1–2 mm³ depends upon simple diffusion of oxygen, nutrients and other essential materials. However, tumour mass growth over 1–2 mm³ can not occur and metastasise without angiogenesis [20]. Although conventional MRI with gadolinium-based contrast enhancement has been useful for grading gliomas, contrast enhancement itself reflects disruption of the blood–brain barrier, not tumour angiogenesis [3, 5, 6]. PWI techniques now have been used for the assessment of tumour vascularity in vivo. rCBV maps and measurements have been shown to correlate reliably with tumour grade and histological findings of tumoural microvascular density, the current standard for assessing the degree of angiogenesis [8–11].

The correlation between the histopathological grade of cerebral gliomas and rCBV has already been evaluated by various groups. Although these studies showed a wide range of rCBV ratios and overlapping between tumours of different grades, there were statistically significant differences between high grade and low grade gliomas [8–11], even in the study of non-enhancing gliomas, as our results confirm. In our study, non-enhancing anaplastic gliomas often demonstrated significant heterogeneity and areas of high rCBV. The presence of contrast enhancement on conventional MRI only represents a pathological alteration in the blood–brain barrier (with or without concomitant angiogenesis), whereas the degree of perfusion MR abnormality can truly reflect the degree of angiogenesis (with or without destruction of the blood–brain barrier) [6, 21]. Therefore, the advantage of perfusion MRI over contrast-enhanced MRI is in depicting tumour angiogenesis and hence in pre-operative grading. Moreover, because large cerebral gliomas are often histopathologically heterogeneous, areas with higher rCBV values, which may be regarded as greater tumour vascularity, can be selectively targeted by stereotactic biopsies to reduce tumour under-grading [6, 22]. This is especially true for non-enhancing gliomas with relative intact blood–brain barrier [10]. On the contrary, for high grade enhancing gliomas with concomitant breakdown of the blood–brain barrier, the first pass of contrast material may leak into extravascular space, and thus the produced susceptibility effects may be decreased between intravascular and extravascular space near the disrupted blood–brain barrier, which is considered to cause the underestimation of the true tumour vascularity [8].

In contrast to measuring average rCBV within tumoural core alone, the measurement of maximum rCBV in peritumoural regions was also performed in our study. The results showed that elevated rCBV ratios were also present in peritumoural brain regions in high grade gliomas, suggests increased peritumoural perfusion due to tumour infiltration. In anaplastic tumours, peritumoural areas demonstrate not only altered capillary morphologic findings but also scattered tumour cells infiltrating along newly formed or pre-existing but dilated vascular channels [8, 22, 23]. In low grade gliomas, on the other hand, the peritumoural region contains less infiltrating tumour cells. This interpretation is consistent with elevated blood volume preceding the appearance of enhancement, which reflects blood–brain barrier breakdown [22]. The fact that we found comparable elevated rCBV in the peritumoural area of grade III gliomas is both novel and significant: Information regarding heterogeneity of peritumoural region in terms of vascularity as depicted by PWI can be effectively used to best estimate of the true brain tumour size pre-operatively [24].

In PWI study, we chose spin-echo echo-planar images because of their presumed higher sensitivity in detecting tumour vascularity at capillary level than at large vessel level [10]. Two different sequences, including spin echo and gradient-echo echo-planar sequences are generally used in first-pass perfusion MR study [21]. Because the gradient-echo echo-planar technique is sensitive to susceptibility effects from the total volume of blood contained in both capillaries and large vessels, we prefer spin echo echo-planar sequences in PWI study of non-enhancing gliomas in order to eliminate the interference of susceptibility artefact [25].

In conclusion, usefulness of DWI and PWI in non-enhancing cerebral gliomas is not only feasible, but also offers clinically relevant physiological data not obtainable by conventional MRI. Non-enhancing brain gliomas with lower ADC values in the solid portions and higher rCBV ratios in both solid portions and peritumoural regions of tumours are significantly correlated with anaplasia. Therefore, DWI and PWI should be integrated in the diagnostic work-up of non-enhancing gliomas in order to predict grading. However, with the advent of advanced MR techniques, a more sophisticated study using a larger sample is needed in the near future.

	Acknowledgments

 
We wish to thank Dr Bing Yu and Dr Songmin Quan for their expert neuroradiological opinion and assistance, and Prof. Liying Chen for helpful advice and discussion.

The authors also thank Department of Neurosurgery of China Medical University for their fellowship.

Received for publication January 9, 2006. Revision received January 27, 2006. Accepted for publication February 2, 2006.

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