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Volumetric Arterial Spin-labeled Perfusion Imaging of the Kidneys with a Three-dimensional Fast Spin Echo Acquisition

Posted Jan 31, 2016 Updated Apr 10, 2023
By Philip M. Robson PhD , Ananth J. Madhuranthakam PhD , Martin P. Smith MD , Maryellen R.M. Sun MD , Weiying Dai PhD , Neil M. Rofsky MD , Ivan Pedrosa MD , David C. Alsop PhD
17 min read

Rationale and Objectives

Renal perfusion measurements using noninvasive arterial spin-labeled (ASL) magnetic resonance imaging techniques are gaining interest. Currently, focus has been on perfusion in the context of renal transplant. Our objectives were to explore the use of ASL in patients with renal cancer, and to evaluate three-dimensional (3D) fast spin echo (FSE) acquisition, a robust volumetric imaging method for abdominal applications. We evaluate 3D ASL perfusion magnetic resonance imaging in the kidneys compared to two-dimensional (2D) ASL in patients and healthy subjects.

Materials and Methods

Isotropic resolution (2.6 × 2.6 × 2.8 mm 3 ) 3D ASL using segmented FSE was compared to 2D single-shot FSE. ASL used pseudo-continuous labeling, suppression of background signal, and synchronized breathing. Quantitative perfusion values and signal-to-noise ratio (SNR) were compared between 3D and 2D ASL in four healthy volunteers and semiquantitative assessments were made by four radiologists in four patients with known renal masses (primary renal cell carcinoma).

Results

Renal cortex perfusion in healthy subjects was 284 ± 21 mL/100 g/min, with test-retest repeatability of 8.8%. No significant differences were found between the quantitative perfusion value and SNR in volunteers between 3D ASL and 2D ASL, or in 3D ASL with synchronized or free breathing. In patients, semiquantitative assessment by radiologists showed no significant difference in image quality between 2D ASL and 3D ASL. In one case, 2D ASL missed a high perfusion focus in a mass that was seen by 3D ASL.

Conclusions

3D ASL renal perfusion imaging provides isotropic-resolution images, with comparable quantitative perfusion values and image SNR in similar imaging time to single-slice 2D ASL.

Introduction

Imaging the distribution and heterogeneity of tissue perfusion is an important component of clinical identification and characterization of primary and metastatic cancer. Quantitative perfusion measurements in tumors may be important for monitoring disease progression , in particular in response to antiangiogenic therapy , and may play a role in assessing the early changes of disease or in understanding normal physiology. There is increasing interest in perfusion measurements as a biomarker for assessing renal function and for characterizing renal masses. Quantitative perfusion is reduced in renal insufficiency and in hemodynamically significant renal artery stenosis . In renal cell carcinoma (RCC), perfusion has proven value because of the relationship between angiogenesis, prognosis, and response to different targeted therapies in these tumors .

Arterial spin labeling (ASL) is a well-established method for measuring tissue perfusion that has been widely used in quantitative perfusion measurements of the brain with application to brain tumors , cerebrovascular disease and stroke, epilepsy, and dementia . A major advantage of ASL is the relative ease with which ASL images can be converted to quantitative images of tissue perfusion. ASL employs external magnetic fields to label nuclear magnetization of endogenous water in arterial blood and then observes the effect on tissue signal after the water flows into and diffuses throughout the tissue. Freely diffusible endogenous water is an excellent tracer for perfusion that compares well to intravenously administered contrast material, because of its lower risk for renal patients and because signal is linear in concentration and independent of venous bolus dynamics and vessel permeability effects that complicate quantification of perfusion with intravenous contrast agents.

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Materials and Methods

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MRI Imaging

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ASL

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Figure 1, (a) Pulse sequence diagram showing the arterial spin labeling preparation before the 3D FSE segment acquisition ( yellow block ): the 1.5-second long pseudo continuous arterial spin labeling (pCASL) module is shown as a green block, saturation pulses ( black ) at 4.1 seconds prior to imaging, tall pulses are adiabatic inversion pulses, the inversion pulse before labeling is a frequency-offset-corrected pulse, shorter pulses during the 1.5-second postlabeling delay are arterial saturation bands. A strong gradient killer pulse is played after the last inversion pulse before imaging (not shown for clarity). (b) Labeling diagram showing pCASL labeling plane below the diaphragm labeling blood in the descending aorta, the extent of the background suppression (BGS) region, defined by the selective presaturation and frequency-offset-corrected inversion (FOCI) pulses shown by the pink dashed box, and the arterial saturation bands shown as a blue cross-hatched box. (Color version of figure is available online.)

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BGS

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Postlabeling Arterial Saturation

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Perfusion Quantification

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3D FSE Acquisition

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2D Single-shot FSE (SSFSE) Acquisition

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Quantitative Perfusion Imaging in Volunteers

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Renal Masses

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Statistical Analysis

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Results

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Figure 2, Perfusion difference images for a volunteer from one 5-minute three-dimensional (3D) fast spin echo (FSE) sagittal acquisition of the left kidney (a) shown with reformatted orthogonal planes (b, c) covering the whole left kidney. Data were acquired with near-isotropic 2.6 × 2.6 × 2.8-mm resolution; images are displayed with four consecutive slices averaged giving 11.2-mm slice thickness to improve signal-to-noise ratio (SNR). Excellent depiction of the renal cortex is seen; the bright signal above the kidney (*) is perfusion in the spleen. Quantitative perfusion images are shown for one volunteer from (d) two-dimensional (2D) single-shot FSE data, and (e, f) coronal reformats of 3D FSE data of the left and the right kidneys. Agreement of quantification between acquisition methods is good.

TABLE 1

Quantitative Perfusion Measurements (mL/100 g/min)

Sequence 3D FSE 2D Single-shot FSE Test Test Retest Free Breathing Test Kidney 1 239 236 227 231 Kidney 2 222 227 201 194 Kidney 3 318 290 285 272 Kidney 4 254 206 348 280 Kidney 5 377 375 298 347 Kidney 6 319 337 345 333 Kidney 7 261 282 236 316 Mean ± SE 284 ± 21 279 ± 23 277 ± 22 282 ± 21

2D/3D, two-/three-dimensional; FSE, fast spin echo.

Quantitative renal cortex perfusion measurements are given in mL/100 g/min for each of the tests and sequences. Kidneys 1–7 are left and right from normal volunteers 1–4. One kidney in one volunteer was not imaged. Mean ± standard error over seven kidneys is also given.

TABLE 2

Quantitative Perfusion Difference Image SNR

Sequence 3D FSE 2D Single-shot FSE Slice Thickness 11.2 mm 2.8 mm 11.2 mm 10 mm Synchronized Breathing Yes Yes No Yes Kidney 1 5.85 3.0 4.9 7.8 Kidney 2 5.82 3.2 4.1 6.0 Kidney 3 8.07 4.6 5.7 8.9 Kidney 4 6.37 4.2 9.3 8.8 Kidney 5 14.2 8.3 5.2 14.1 Kidney 6 11.1 6.2 8.3 12.5 Kidney 7 5.9 3.4 4.3 6.0 Average SNR (±SD) 8.2 ± 3.3 4.7 ± 1.9 6.0 ± 2.0 9.2 ± 3.1 Average SNR norm (±SD) 6.1 ± 2.1 14.1 ± 4.7 4.4 ± 1.3 9.2 ± 3.1

2D/3D, two-/three-dimensional; FSE, fast spin echo; ROI, region of interest; SNR, signal-to-noise ratio.

SNR values are calculated from average ROI signal on perfusion difference images on native 2.8-mm thick slices in the 3D sequence, or from the 11.2-mm thick average of four contiguous slices. The 2D slice was 10-mm thick. Kidneys 1–7 are left and right from normal volunteers 1–4. One kidney in one volunteer was not imaged. The average SNR ± standard deviation over 7 kidneys is also given, and finally the SNR value normalized for slice thickness and square-root-imaging time (SNRnorm). Also shown in one column are results from measurements made during free breathing compared to those with synchronized breathing.

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Figure 3, Three-dimensional perfusion difference images in patient 2 initially acquired in the sagittal plane with near-isotropic resolution 2.6 × 2.6 × 2.8 mm (a) allowed for reformatted images in (b) coronal and (c) axial orientations, displayed with 11.2-mm slice thickness. Perfusion is clearly high compared to surrounding parenchyma and of a heterogeneous nature, which correlates well with the anatomical appearance of the lesion (two-dimensional [2D] multislice single-shot fast spin echo [FSE]) shown in (d) . Scan time for this three-dimensional (3D) image data was ~5 minutes.

Figure 4, Three-dimensional (3D) perfusion difference images in patient 1 initially acquired in the sagittal plane with near-isotropic resolution 2.6 × 2.6 × 2.8 mm (a) allowed for reformatted images in (b) coronal and (c) axial orientations, displayed with 11.2-mm slice thickness. Perfusion is clearly high compared to surrounding parenchyma and of a heterogeneous nature, which correlates well with the anatomical appearance of the lesion (two-dimensional [2D] multislice single-shot fast spin echo [FSE]) shown in ( d ). The lesion is very large and complex, extending beyond the borders of the kidney. Scan time for this 3D image data was ~5 min.

Figure 5, Utility of three-dimensional (3D) coverage in clinical applications is demonstrated in images of a renal mass in patient 3, shown in a two-dimensional (2D) single-shot fast spin echo (FSE) anatomical reference image (a) . Good agreement of perfusion difference images in the same slice ( solid box ) is seen between (b) 2D single-shot FSE and (c) 3D FSE coronal reconstructed images, showing a highly perfused nodule ( arrow ); low perfusion is seen in the surrounding parenchyma. In the 3D perfusion image data ( coronal (c) and sagittal (d) ), additional highly perfused foci are seen more anteriorly in the kidney ( arrowhead ), as well as perfusion of the parenchyma in posterior portions of the kidney.

Figure 6, Comparison of perfusion difference images of renal masses in all patients. Single coronal slices reformatted from three-dimensional (3D) fast spin echo (FSE) sagittal datasets ( top ) and coronal two-dimensional (2D) single-shot FSE acquisitions ( middle ) are shown. Anatomical reference images (multislice single-shot FSE) are also shown ( bottom ). Perfusion image scan time for 3D scans was ~5 minutes and perfusion image scan time for 2D single-shot FSE was 3.5 min.

TABLE 3

Semiquantitative Assessment by Radiologists: Rating of Image Sharpness by Acquisition Sequence

Reader Patient Totals 1 2 3 4 n2D n3D 1 3D 3D 2D 3D 1 3 2 2D 3D 2D 2D 3 1 3 3D 3D 2D 2D 2 2 4 3D 3D 2D 3D 1 3

2D/3D, two-/three-dimensional.

The sequence preferred for image sharpness is given for each patient and each reader. The data are summarized per reader on the right, with n2D and n3D being the number of patients for which 2D and 3D imaging was preferred.

TABLE 4

Semiquantitative Assessment by Radiologists: Scores for Similarity of Perfusion Features Between Sequences

Reader Patient Average 1 2 3 4 1 4 4 4 5 4.25 2 4 3 2 2 2.75 3 4 4 2 3 3.25 4 3 4 4 5 4 Average 3.75 3.75 3 3.75 3.56

2D/3D, two-/three-dimensional.

Scores for the similarity in perfusion features between 2D and 3D sequences for each patient given by each reader are given, as well as averages by patient and reader.

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Discussion

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Acknowledgments

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Academic Radiology, Volume 23, Issue 2
Journals General Radiology
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