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Perfusion MR Imaging of Brain Neoplasms

¹ All authors: Department of Radiology, Duke University Medical Center, Box 3808, Durham, NC 27710

Received June 10, 1999; accepted after revision August 25, 1999.

 
Address correspondence to J. M. Provenzale.

Introduction

Top Introduction Principles and Methods Applications References

 
MR imaging is now a well-established tool for the evaluation of brain tumors, but conventional MR techniques continue to have important limitations. These limitations include inability to reliably distinguish high-grade from low-grade tumors, determine exact limits of tumor extension, and discriminate between recurrent tumor and radiation necrosis. Dynamic susceptibility contrast imaging is an emerging technique that allows evaluation of cerebral vasculature. Because angiogenesis is a prominent feature of neoplastic proliferation, this technique offers the possibility of providing important information about tumors that is not available on conventional MR images. We review the principles of dynamic susceptibility contrast imaging and specific applications of this technique for the imaging of brain tumors.

Principles and Methods

Top Introduction Principles and Methods Applications References

 
Dynamic susceptibility contrast imaging is based on the fact that paramagnetic contrast agents (such as gadopentetate dimeglumine) cause a substantial decrease in brain signal intensity on T2^*-weighted images. This finding results from the fact that passage of contrast material through the intravascular compartment causes local field inhomogeneities that result in magnetic susceptibility effects and reduction in the T2^* transverse relaxation time. With long TEs of from 80 to 100 msec, the susceptibility effects of a bolus of contrast agent can produce a signal decrease of as much as 50% [1]. The advent of high-speed MR imaging techniques has provided the temporal resolution necessary to exploit this T2^* effect for the study of cerebral hemodynamics. Dynamic susceptibility contrast imaging makes use of a series of rapidly acquired T2^*-weighted images to monitor changes in magnetic susceptibility in the vascular bed during first-pass transit of a bolus of contrast material (Fig. 1A,1B,1C).

View larger version (96K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —63-year-old healthy woman in whom MR imaging shows decreased signal intensity in gray and white matter on T2*-weighted images during first-pass circulation of gadopentetate dimeglumine. Axial T2*-weighted echoplanar MR image (TR/TE, 1500/90) obtained before arrival of bolus of contrast material shows baseline signal intensity of gray matter and white matter.

View larger version (29K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —63-year-old healthy woman in whom MR imaging shows decreased signal intensity in gray and white matter on T2*-weighted images during first-pass circulation of gadopentetate dimeglumine. Time-signal intensity curves show decreased signal intensity with passage of bolus of contrast material. Using T2*-weighted echoplanar pulse sequence, set of eight slices is obtained every 1500 msec over 60 sec, for total of 40 image sets (320 images). Upper and lower curves are derived from regions of interest drawn in white matter and gray matter, respectively. Gray matter shows greater decrease in signal intensity than does white matter.

View larger version (104K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —63-year-old healthy woman in whom MR imaging shows decreased signal intensity in gray and white matter on T2*-weighted images during first-pass circulation of gadopentetate dimeglumine. Same slice as that shown in A but this image at maximal-signal-intensity decrease shows substantial darkening of gray matter structures.

Typically, an ultrafast multislice acquisition technique is used to obtain images before, during, and after bolus injection of contrast material. We currently use a technique that acquires a set of eight slices every 1500 msec over 60 sec, for a total of 40 image sets (320 images). A spin-echo echoplanar pulse sequence is used, with parameters as follows: TR, 1500 msec; TE, 90 msec; slice thickness, 7 mm; matrix size, 128 x 128; and field of view, 24 x 24 cm. After the first 10 image sets are obtained, a 0.2-mmol/kg bolus of gadopentetate dimeglumine is power-injected via an 18- or 20-gauge IV catheter at a rate of 6 ml/sec.

To construct relative cerebral blood volume maps, changes in signal intensity (S) are converted to changes in T2^* relaxation rate by the formula (-ln[S / S₀] / TE), where S₀ is the baseline signal intensity. Because changes in T2^* relaxation rate are linearly proportional to the concentration of contrast material in tissue, this calculation allows conversion of a time-signal intensity curve into a time-concentration curve (Fig. 2A,2B,2C). Relative cerebral blood volume maps are then generated by integration on a voxel-by-voxel basis to yield the area under the time-concentration curve [1]. Resultant relative cerebral blood volume maps show that gray matter structures have higher blood volumes than white matter structures (Fig. 2A,2B,2C), and tumors such as high-grade gliomas can have relative cerebral blood volume equal to (or even greater than) that of gray matter (Fig. 3A,3B,3C).

View larger version (32K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Construction of relative cerebral blood volume (rCBV) maps in 38-year-old healthy man. Typical time-signal intensity curve shows number of images obtained (abscissa) and signal intensity of given tissue (ordinate). Vertical lines mark beginning and end of first-pass circulation of gadopentetate dimeglumine. Horizontal line marks baseline signal intensity (S0). Shaded area represents portion of time-signal intensity curve used to calculate rCBV.

View larger version (35K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Construction of relative cerebral blood volume (rCBV) maps in 38-year-old healthy man. Time-concentration curve derived from data in A shows vertical lines, which denote limits of integration, and horizontal line, which represents baseline concentration of contrast material in tissue. rCBV is proportional to area under time-concentration curve.

View larger version (110K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —Construction of relative cerebral blood volume (rCBV) maps in 38-year-old healthy man. rCBV map derived from time-concentration curve in B. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue. Notice that cortex and subcortical gray matter structures (i.e., basal ganglia and thalamus) have higher rCBV than white matter, reflecting greater degree of darkening of these structures as shown in Figure 1C.

View larger version (118K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —67-year-old man with untreated high-grade glioma. Contrast-enhanced axial T1-weighted MR image shows large enhancing tumor (arrowhead) in left centrum semiovale.

View larger version (33K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —67-year-old man with untreated high-grade glioma. Time-signal intensity curves show signal-intensity decrease during first-pass transit of gadopentetate dimeglumine. Upper and lower curves correspond to regions of interest drawn around tumor and normal gray matter, respectively. Note decreased signal intensity in tumor at least equal to that of normal gray matter.

View larger version (79K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —67-year-old man with untreated high-grade glioma. Relative cerebral blood volume (rCBV) map generated from time-signal intensity curve in B shows tumor (arrowhead) with elevated rCBV that is at least equal to rCBV of normal gray matter. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

At this point a potential pitfall in construction of relative cerebral blood volume maps is worth noting. One of the most commonly used methods for generating relative cerebral blood volume maps is numeric integration from beginning to end of the first-pass transit of a bolus of contrast agent using a constant baseline signal intensity [2,3,4]. This method works well for normal brain tissue and many brain tumors (even enhancing ones), but substantial underestimation of relative cerebral blood volume occurs in the setting of severe blood-brain barrier disruption. This is due to the fact that gadolinium-based contrast agents have T1 effects in addition to the T2^* effects already discussed. This unwanted T1 effect is caused by extravasated contrast material and is seen as a rise in signal intensity above baseline after the initial drop. Because of the shape of the time-signal intensity curve (and therefore that of the time-concentration curve), the standard method of numeric integration underestimates relative cerebral blood volume. This occurs because the rise in signal intensity is interpreted by the algorithm as "negative" blood volume, which is subtracted from the "positive" blood volume (represented by decrease in signal intensity below baseline on the time-signal curve) (Fig. 4A,4B,4C,4D). Gamma-variate curve-fitting techniques and computational models that attempt to correct for T1 effects have been used to partially correct for this problem (Weisskoff RM et al., presented at the Society of Magnetic Resonance in Medicine meeting, August 1994). However, these methods are computationally intensive, far more time-consuming, and therefore impractical for routine clinical use. Alternatively, a small loading dose of contrast material can be infused to saturate brain tissue and lessen leakage of contrast material during the bolus.

View larger version (88K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —47-year-old woman with high-grade glioma treated with surgery and radiation therapy. This case shows how relative cerebral blood volume (rCBV) of lesions with high blood-brain barrier disruption can be under-estimated by rCBV maps created using standard numeric integration method. Contrast-enhanced axial T1-weighted MR image shows nodular enhancement around right frontoparietal resection cavity (arrowhead).

View larger version (36K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —47-year-old woman with high-grade glioma treated with surgery and radiation therapy. This case shows how relative cerebral blood volume (rCBV) of lesions with high blood-brain barrier disruption can be under-estimated by rCBV maps created using standard numeric integration method. Comparison of standard numeric integration method and limited integration method of generating rCBV maps. Upper curve corresponds to region of interest drawn around lesion seen in A. Lower curve corresponds to region of interest drawn around whole brain as depicted on single slice. Horizontal lines denote baseline signal intensity for each curve. Vertical lines mark beginning and end of first-pass transit of gadopentetate dimeglumine using lower curve as guide. Rise in signal intensity above baseline in upper curve is caused by T1 effects of ex-travasated contrast material. In calculation of rCBV maps, change in signal intensity is converted to tissue concentration of contrast material using following relationship: concentration (-ln[S / S0] / TE), where S is signal intensity at particular time point on time-signal intensity curve and S0 is baseline signal intensity. Whenever S > S0 (i.e., when signal intensity rises above baseline), tissue concentration of contrast material is calculated to be "negative." Integration of "negative" time-concentration curve yields "negative" blood volume. In this example, rCBV derived from portion of curve shaded yellow (where S > S0) is considered "negative" and subtracted from "positive" rCBV calculated from combined blue and green portions (where S < S0), resulting in underestimation of relative cerebral blood volume. Using limited-integration method, only portion of time-signal intensity curve shaded in green is used to calculate rCBV. This simple modification eliminates part of time-signal intensity curve most subject to distortion by T1 effects of extravasated contrast material, thereby avoiding underestimation of rCBV in regions of high blood-brain barrier permeability.

View larger version (101K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —47-year-old woman with high-grade glioma treated with surgery and radiation therapy. This case shows how relative cerebral blood volume (rCBV) of lesions with high blood-brain barrier disruption can be under-estimated by rCBV maps created using standard numeric integration method. rCBV map generated using limited-integration method shows area of high rCBV (arrowhead) corresponding to contrast enhancement. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4D. —47-year-old woman with high-grade glioma treated with surgery and radiation therapy. This case shows how relative cerebral blood volume (rCBV) of lesions with high blood-brain barrier disruption can be under-estimated by rCBV maps created using standard numeric integration method. rCBV map generated using standard numeric-integration method fails to show area of high rCBV seen in C (arrowhead) because "negative" relative cerebral blood volume derived from portion of time-signal intensity curve above baseline signal intensity has been subtracted, resulting in falsely low rCBV in region of lesion. Notice that normal brain looks similar using either method. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

We currently use a method of limited integration that, rather than attempting to correct for the part of the time-signal intensity curve distorted by extravasated contrast material, simply excludes it by ending the integration at peak signal intensity decrease before T1 effects become evident (Fig. 4A,4B,4C,4D). Our experience has been that this simple modification of the standard numeric integration method (which we term the "limited integration method") creates relative cerebral blood volume maps that are almost identical to those constructed using more sophisticated (but far more time-consuming) methods. Unless otherwise indicated, the images presented in this essay were created using this limited-integration method.

Applications

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Guiding Stereotactic Biopsy
Because brain tumors are often histologically heterogeneous, samples obtained at biopsy are subject to sampling error that may adversely affect treatment decisions. This problem is especially evident in stereotactic biopsies, in which only very small specimens are taken and the chance of sampling error is correspondingly large [5]. Although in general high-grade tumors are more likely to enhance than low-grade tumors, enhancement pattern is not a highly reliable indicator of tumor grade for guiding biopsy because high-grade tumors occasionally do not enhance (Fig. 5A,5B,5C) and enhancing tumors may be low-grade. Therefore, contrast enhancement is not a dependable guide for indicating the site within a tumor that is most likely to have the highest histologic grade.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —44-year-old woman with untreated unenhancing high-grade glioma with high relative cerebral blood volume (rCBV) despite lack of contrast enhancement. Axial T2-weighted MR image shows tumor as hyperintense region in left frontal lobe (arrowhead).

View larger version (112K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —44-year-old woman with untreated unenhancing high-grade glioma with high relative cerebral blood volume (rCBV) despite lack of contrast enhancement. Contrast-enhanced axial T1-weighted MR image shows no abnormal enhancement in corresponding region (arrowhead).

View larger version (81K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5C. —44-year-old woman with untreated unenhancing high-grade glioma with high relative cerebral blood volume (rCBV) despite lack of contrast enhancement. rCBV map shows tumor (arrowhead) to have high rCBV (approximately equal to that of gray matter) consistent with patient's biopsy-proven diagnosis of high-grade glioma. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

It is well established that increased tumor vascularity is associated with higher malignant potential and poorer prognosis, as indicated by the fact that presence or absence of neovascularity is a component of most histologic tumor-grading systems [3]. Previous studies correlating histopathologic grading of astrocytomas with relative cerebral blood volume have found a significant difference in mean relative cerebral blood volume between high- and low-grade tumors, with low-grade tumors often having homogeneous low relative cerebral blood volume and high-grade tumors exhibiting varying degrees of high relative cerebral blood volume [2, 4, 6, 7] (Fig. 3A,3B,3C). Furthermore, a positive correlation between relative cerebral blood volume and mitotic activity and tumor vascularity has been reported [3]. These findings suggest that dynamic susceptibility contrast imaging may be useful as an indicator of tumor grade and aid in guiding stereotactic biopsies.

Delineating Tumor Margins
Margins of enhancement do not always reliably indicate the true extent of tumor invasion because brain tumors, especially astrocytomas, frequently have nonenhancing infiltrative extensions into normal brain tissue. T2-weighted MR images can be helpful, but distinguishing between peritumoral edema and nonenhancing tumor is often difficult, and T2-weighted images frequently fail to reveal tumor extensions visible on contrast-enhanced T1-weighted images [8]. Consequently, surgical resection alone is rarely curative even if the entire tumor visualized on conventional MR imaging can be removed [9] (Fig. 6A,6B,6C). The ability of dynamic susceptibility contrast imaging to detect nonenhancing tumors by virtue of their elevated relative cerebral blood volume suggests that it may be able to delineate tumor borders more accurately than conventional MR techniques (Fig. 7A,7B,7C), which would be valuable for surgical planning and targeting of radiation therapy.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A. —47-year-old woman with residual high-grade glioma not evident on conventional MR images. Contrast-enhanced axial T1-weighted MR image obtained shortly after surgical resection shows surgical cavity (arrow) with thin rim of enhancement.

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B. —47-year-old woman with residual high-grade glioma not evident on conventional MR images. Axial T2-weighted MR image shows region of hyperintense signal (arrowhead) anterior to resection cavity (arrow). Note that no abnormal contrast enhancement is seen at this site in A. This region of hyperintense signal can represent residual tumor or edema.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6C. —47-year-old woman with residual high-grade glioma not evident on conventional MR images. Relative cerebral blood volume (rCBV) map shows nodule of high rCBV (arrowhead) anterior to surgical cavity (arrow), which is consistent with residual high-grade tumor not seen in A. On follow-up MR imaging 4 months later (not shown), contrast enhancement markedly increased in region of elevated rCBV, again consistent with residual tumor. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

View larger version (119K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —45-year-old man with untreated high-grade glioma. Difference between tumor borders as defined by conventional contrast-enhanced T1-weighted image and relative cerebral blood volume (rCBV) map is shown in this case. Contrast-enhanced axial T1-weighted MR image shows enhancing lesion in left temporoparietal region (arrowhead).

View larger version (119K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —45-year-old man with untreated high-grade glioma. Difference between tumor borders as defined by conventional contrast-enhanced T1-weighted image and relative cerebral blood volume (rCBV) map is shown in this case. Axial T2-weighted MR image shows area of signal abnormality larger than area of contrast enhancement (arrowhead) in A that may represent tumor, edema, or combination of both.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7C. —45-year-old man with untreated high-grade glioma. Difference between tumor borders as defined by conventional contrast-enhanced T1-weighted image and relative cerebral blood volume (rCBV) map is shown in this case. rCBV map shows elevated rCBV (arrowhead) in area larger than area of contrast enhancement in A, suggesting that much of T2 signal abnormality in B represents tumor that is not evident on conventional contrast-enhanced T1-weighted MR images. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

Differentiating Between Radiation Necrosis and Recurrent Tumor
Differentiation between radiation necrosis and recurrent tumor is important because different therapies are indicated, but is often difficult because both processes enhance on MR imaging and CT and both can present with similar symptoms. Fluorodeoxyglucose-positron emission tomography is commonly used to help show this distinction, but in a recent study investigators found the specificity of combined positron emission tomography and conventional MR for detecting recurrent tumor to be relatively low [10]. Researchers have reported that relative cerebral blood volume maps allow correct differentiation between radiation necrosis and recurrent tumor (by virtue of the former's low relative blood volume compared with that of a recurrent tumor) in cases in which positron emission tomography cannot (De-LaPaz RL et al., presented at the Radiological Society of North America meeting, November 1995), suggesting the utility of dynamic susceptibility contrast imaging for this purpose (Figs. 8A,8B,8C and 9A,9B).

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8A. —Radiation necrosis in 39-year-old man with high-grade glioma treated with radiation therapy. Contrast-enhanced axial T1-weighted MR image shows peripherally enhancing mass (arrowhead) in left frontal lobe.

View larger version (112K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8B. —Radiation necrosis in 39-year-old man with high-grade glioma treated with radiation therapy. Fluorodeoxyglucose-positron emission tomographic image shows increased fluorodeoxyglucose uptake (arrowhead) corresponding to region of enhancement in A. Combination of findings in A and B could represent progressive tumor growth or radiation necrosis.

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8C. —Radiation necrosis in 39-year-old man with high-grade glioma treated with radiation therapy. Relative cerebral blood volume (rCBV) map shows no area of high rCBV in region of contrast enhancement (arrowhead). This could indicate radiation necrosis or low-grade recurrent tumor. Subsequent biopsy found radiation necrosis. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

View larger version (111K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 9A. —38-year-old man with recurrent high-grade glioma. Contrast-enhanced axial T1-weighted MR image shows enhancement of solid portion of right hemispheric lesion with adjacent cyst (arrowhead).

View larger version (77K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 9B. —38-year-old man with recurrent high-grade glioma. Relative cerebral blood volume (rCBV) map shows marked rCBV abnormality corresponding to area of contrast enhancement (arrowhead), consistent with patient's biopsy-proven recurrent high-grade glioma. Note that cystic cavity anterior to lesion lacks rCBV. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

Dynamic susceptibility contrast imaging does have some limitations. It is often difficult to differentiate between recurrent low-grade tumor and radiation necrosis, both of which have low relative cerebral blood volume (Fig. 10A,10B). Dynamic susceptibility contrast imaging also lacks the sensitivity needed to detect very small foci of recurrent high-grade tumor. Although these small clusters of malignant cells may be highly vascular, existing techniques lack the spatial resolution necessary to detect them (Fig. 11A,11B).

View larger version (118K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 10A. —40-year-old woman with biopsy-proven low-grade recurrent tumor treated with radiation therapy that is not evident on relative cerebral blood volume (rCBV) map. Contrast-enhanced axial T1-weighted MR image shows irregular enhancement surrounding surgical cavity in right frontal lobe (arrowhead).

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 10B. —40-year-old woman with biopsy-proven low-grade recurrent tumor treated with radiation therapy that is not evident on relative cerebral blood volume (rCBV) map. rCBV map shows no evidence of high rCBV in region of contrast enhancement (arrowhead) to suggest high-grade recurrent tumor. This finding could represent low-grade tumor or radiation necrosis because both entities have low rCBV. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 11A. —20-year-old man with high-grade glioma treated with radiation therapy in whom small foci of recurrent tumor are not evident on relative cerebral blood volume (rCBV) map. Contrast-enhanced axial T1-weighted MR image shows nodular enhancement in left frontal lobe (arrowhead).

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 11B. —20-year-old man with high-grade glioma treated with radiation therapy in whom small foci of recurrent tumor are not evident on relative cerebral blood volume (rCBV) map. rCBV map shows no high rCBV in region of contrast enhancement (arrowhead) to suggest recurrent tumor. Nonetheless, at biopsy small foci of recurrent high-grade tumor were seen against back-ground of radiation necrosis, suggesting that existing dynamic susceptibility contrast imaging techniques lack spatial resolution necessary to detect such small foci of tumor. Regions that are red and yellow have higher cerebral blood volume relative to those that are green and blue.

Although experience with this relatively new technique is limited, dynamic susceptibility contrast imaging appears to have great potential for improving evaluation of brain tumors because it provides useful information about cerebral hemodynamics that cannot be obtained from conventional MR images. Furthermore, this technique is practical for routine clinical use because conventional MR equipment can be used, data acquisition is quick, and relative cerebral blood volume maps can be created in a matter of seconds using commercially available software.

References

Top Introduction Principles and Methods Applications References

 

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