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Sensitivity Encoding for Diffusion-weighted MR Imaging at 3.0 T: Intraindividual Comparative Study¹

¹ From the Department of Radiology, University of Bonn, Sigmund-Freud-Strasse 25, D-53105 Bonn, Germany. Received October 7, 2003; revision requested December 30; final revision received March 18, 2004; accepted April 19. Address correspondence to C.K.K. (e-mail: kuhl@uni-bonn.de).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To prospectively evaluate whether diffusion-weighted (DW) magnetic resonance (MR) imaging with sensitivity encoding (SENSE) at 3.0 T can help to improve image quality and confidence in and accuracy of diagnosis of ischemic lesions, compared with DW MR imaging with conventional phase encoding, in patients.

MATERIALS AND METHODS: Patients provided informed consent after the study had been explained, and the institutional review board approved the study protocol. Eighty-five patients (46 male and 39 female patients; age range, 13–86 years; mean age, 52 years) underwent single-shot spin-echo echo-planar DW MR imaging at 3.0 T twice, in a randomized order: once with conventional phase encoding (repetition time msec/echo time msec, 4283/79) and once with SENSE (3141/69, with a reduction factor of three). With both, 128 x 128 matrix, 24 4-mm-thick sections, and two b values of 0 and 1000 sec/mm² were used. An eight-element SENSE-compatible receive-only surface coil was used; the built-in body coil served for radiofrequency transmission and generation of the coil sensitivity profile. SENSE and conventional phase encoding were compared for image quality, signal-to-noise ratio, relative signal intensity (SI), and lesion contrast. Two neuroradiologists read images. Diagnostic accuracy of and confidence in detection of apparent diffusion coefficient (ADC) lesions with conventional phase encoding and SENSE at MR imaging were compared; matched-pairs Wilcoxon signed rank test was used to test statistical significance.

RESULTS: No major SENSE-related artifacts were seen. At MR imaging with SENSE, consistently and significantly (P < .001) higher image quality scores were achieved because of substantial reduction of image distortions and blurring. Lesion contrast was equivalent with both techniques. Diagnostic confidence for demonstration and exclusion of lesions was significantly (P < .001) higher at MR imaging with SENSE. In three patients, small microembolic lesions were only prospectively diagnosed at MR imaging with SENSE, whereas they were masked by adjacent susceptibility effects and therefore overlooked at MR imaging with conventional phase encoding.

CONCLUSION: Parallel MR imaging with SENSE is feasible at 3.0 T. It significantly improves image quality, particularly by reducing or even preventing susceptibility-induced SI changes and image blurring. There was a significantly improved diagnostic confidence with which ADC changes were identified or excluded.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Diffusion-weighted (DW) magnetic resonance (MR) imaging has become the cornerstone for the timely diagnosis of acute stroke. There is convincing evidence to suggest that DW MR imaging is substantially more sensitive than regular T1- and T2-weighted or fluid-attenuated inversion-recovery MR imaging and far more sensitive than computed tomography (CT) for detection of acute and subacute ischemic lesions (1–7). So far, the majority of clinical DW MR imaging studies are performed with MR systems operating at a field strength of 1.5 T. Still at 1.5 T, DW MR imaging is associated with limited signal-to-noise ratio (SNR), which may impair its sensitivity for subtle apparent diffusion coefficient (ADC) changes (8).

MR systems operating at a higher field strength, such as 3.0 T, have recently become available not only for research purposes but also for clinical use in patients. As SNR increases linearly with increasing field strength, high-field-strength systems promise to improve SNR in DW MR imaging, as well as diffusion-tensor imaging. Susceptibility artifacts, however, increase not only linearly but even exponentially with field strength. This has already been shown to cause significant geometric image distortions, stretching, and blurring on DW MR images obtained at 3.0 T (9).

Parallel imaging has been shown to be an efficient tool for speeding up image acquisition through a reduction of the number of phase-encoding steps that are necessary for image generation (10–15). The resulting gain can be used not only to cut down on MR image acquisition time but also to prevent susceptibility artifacts (16): In particular, in single-shot echo-planar MR imaging, a reduction of phase-encoding steps translates directly into a reduced echo train length that, in turn, prevents or reduces phase errors.

Thus, the purpose of our study was to prospectively evaluate (a) whether DW MR imaging with sensitivity encoding (SENSE) (11) is feasible at 3.0 T, (b) whether SENSE can help to improve image quality compared with DW MR imaging with conventional phase encoding, and (c) whether SENSE helps to improve confidence in and accuracy of the diagnosis of ischemic lesions in patients.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Study Design
At an academic tertiary care center, an intraindividual comparative study was performed in patients who underwent single-shot echo-planar DW MR imaging at 3.0 T twice, in a randomized order, within minutes of each other, once with conventional phase encoding and once with SENSE, to enable the comparison of the two pulse sequence techniques in regard to their image quality and diagnostic yield. Patients provided informed consent after the study had been explained to them. Our institutional review board approved the study protocol.

Patients
Inclusion criteria were as follows: (a) the patient had no contraindication to high-field-strength MR imaging (no known metallic implants) and no history of cardiac surgery or neurosurgical procedures, (b) the patient had a clinical indication to undergo MR imaging with or without diffusion, and (c) the patient had the ability to provide conscious informed consent. Between November 2002 and February 2003, a total of 85 consecutive patients (46 male and 39 female patients) met the inclusion criteria and were included in the study. The mean age of the entire study population was 52 years, with an age range of 13–86 years; the age range of male and female patients was 13–83 years and 17–86 years, respectively; the mean age was 53.49 and 53.13 years, respectively (not significantly different with the t test for independent samples). All patients who were recruited underwent MR imaging with both techniques. The patients were referred for MR imaging for the following: symptoms of subacute or chronic stroke (50 of 85 patients), including a current history of arrhythmia (one of 50), vasculitis (five of 50), or patent foramen ovale (one of 50); suspected brain tumors (15 of 85); psychiatric disorders (13 of 85); vascular malformation (three of 85); suspected sinus thrombosis with venous infarction (two of 85); and chronic epilepsy to rule out hippocampal sclerosis (two of 85). The patients with psychiatric disorders and those who were suspected of having hippocampal sclerosis were included to also have a subset of patients who were unlikely to have focal ischemia-like diffusion abnormalities (ie, who could serve as negative controls). This, in turn, was important owing to the well-known difficulty to validate DW MR imaging findings with other imaging techniques. For assessment of the specificities of the techniques (ie, to investigate the number of false-positive findings), it appeared necessary to include patients in whom the a priori probability of having true ischemia-like diffusion abnormalities was very low and who could serve as normal controls.

MR Imaging Protocol
All MR imaging studies were conducted with a 3.0-T whole-body MR system (Intera; Philips Medical Systems, Best, the Netherlands) equipped with gradients with a maximum slew rate of 150 mT · m^–1 · msec^–1 and a maximum strength of 30 mT/m. A standard receive-only multielement (eight-element) surface head coil (MRI Devices, Pewaukee, Wis) was used; the built-in standard quadrature body coil served for radiofrequency transmission and, in conjunction with the surface coil, for generation of a sensitivity map of the surface coil.

After the initial scout view was obtained, the reference acquisition (ie, a sensitivity map of the surface coil) was obtained. The reference acquisition was obtained with a three-dimensional gradient-echo (fast field-echo) sequence and repetition time msec/echo time msec of 4.0/0.79, flip angle of 2°, and matrix of 64 x 64. The sensitivity map was needed for both the image homogeneity correction (constant level appearance, CLEAR; Philips Medical Systems, Best, the Netherlands) and the SENSE reconstruction. The time for this pulse sequence was 30 seconds, during which the actual diffusion and structural MR imaging pulse sequences were prescribed according to the scout images.

DW MR imaging was performed by using a single-shot spin-echo echo-planar pulse sequence, once with and once without SENSE, in a randomized order.

The two DW MR imaging pulse sequences were identical in regard to their geometric parameters: To facilitate the subsequent region of interest (ROI) analysis, both DW imaging sets were acquired with exactly matching anatomic position and transverse orientation, with 24 4-mm-thick sections, 1-mm gap, 128 x 128 matrix, two signals acquired, fat suppression with spectral-selective saturation of the fat resonance frequency (or SPIR), and two b values (0 and 1000 sec/mm²). At both b values, the diffusion sensitization was repeated in each orthogonal gradient direction (phase encoding, readout, section selection), and the final isotropic diffusion maps were automatically calculated by the system by averaging of the three measurements. For image reconstruction, a homogeneity correction algorithm (constant level appearance) was used on the DW MR images acquired with and without parallel acquisition (SENSE together with conventional phase encoding). With this algorithm, the coil sensitivity profile obtained with the reference acquisition is used to adjust local signal intensity (SI) variations secondary to the spatial properties of the surface coils. This adjustment is performed in real time during image reconstruction; it does not require extra acquisition or reconstruction time.

Owing to the reduced number of phase-encoding steps with parallel acquisition, the two DW MR imaging pulse sequences differed in regard to the following parameters: In the sequence with conventional DW MR imaging without SENSE, the shortest possible repetition time and echo time with the previously mentioned geometric parameter setting were 4283 msec and 79 msec, respectively. The sequence with DW MR imaging with parallel imaging was performed with a SENSE factor (R, or reduction factor) of three, where R is defined as the number of phase-encoding steps without parallel imaging, relative to the number of phase-encoding steps with parallel imaging. This resulted in a shorter echo-planar imaging echo train, which, in turn, resulted in the shortest possible repetition time and echo time of 3141 msec and 69 msec, respectively. The differing echo times were the reason why the image acquisition time varied between the two pulse sequences: At DW MR imaging with conventional phase encoding, acquisition time was 1 minute 34 seconds; at DW MR imaging with SENSE, it was reduced to 1 minute 9 seconds.

Maps of the ADC were calculated for each diffusion study by the standard console software of the system.

The diffusion studies were integrated into the regular clinical imaging protocol, which varied with the clinical situation. All patients, however, underwent imaging with at least a T2-weighted turbo spin-echo pulse sequence (3540/80, 31 sections, and 512 x 400 matrix), a fluid-attenuated inversion-recovery pulse sequence (12 000/140/2800 [inversion time msec] and 350 x 256 matrix) in two orientations (coronal and transverse), and a T1-weighted spin-echo sequence (500/15, 25 sections, and 256 x 256 matrix).

Quantitative Data Analysis
In the first 17 patients with lesions visible at DW MR imaging, the two sets of DW MR images were transferred to a workstation for further quantitative analysis of SNR, relative SI, and lesion contrast (ie, contrast between the lesions and the adjacent normal brain tissue on DW MR images, which we called SI), as described in the following sections.

ROI placement.—With the close supervision of two experienced neuroradiologists (J.T., C.K.K., with 7 and 10 years of experience in neurologic MR imaging, respectively), oval ROIs were placed into the white matter of the right and the left hemispheres, into the posterior horn (trigonum) of the lateral ventricles, and into the ghosting-free part of the image background. In addition, an ROI was placed directly onto the ischemic lesion and onto the adjacent normal-appearing brain tissue. As the two DW MR imaging studies were conducted with exactly the same geometric parameters, the ROIs could be copied from the diffusion images acquired without SENSE to those acquired with SENSE. The size of the ROIs varied, depending on the location; the mean area of ROIs in the trigonum was 105 mm², that in the centrum semiovale was 813 mm², and that in the background noise was 4300 mm². By using the ROI data, overall SNR, relative SI, and lesion-to–normal tissue contrast were calculated by one author (C.K.K.).

Calculation of overall SNR.—Overall SNR was calculated in all studies according to the following equation: SNR = SI_tissue/SD SI_noise, where SI_tissue is the mean of the two ROIs placed in the cerebral hemispheres and SD SI_noise is the standard deviation of the SI of the background noise.

Calculation of Relative SI.—We calculated the relative SI for white matter, signified as rSI_wmatter, versus cerebrospinal fluid according to the following equation: rSI_wmatter = SI_wmatter/SI_CSF, where SI_wmatter and SI_CSF are the SI of the white matter and of the cerebrospinal fluid, respectively. The rationale of using relative SI instead of the usual SNR was to provide a rough estimate of the overall SI of the image without the possibly misleading contribution of image noise: Noise in MR images obtained with SENSE may be artificially high because of the unfolding algorithm (11).

Calculation of lesion contrast.—We calculated the SI, according to the following equation: SI = SI_lesion – SI_adjtiss, where SI_lesion is the SI obtained in the lesion visible on the DW MR image and SI_adjtiss is the SI in the normal brain tissue adjacent to the lesion.

The means and standard deviations (calculated for the pooled data for DW MR images obtained with SENSE and with conventional phase encoding in all 85 patients) for SNR, relative SI, and lesion contrast were calculated and compared.

Image Quality Evaluation
The DW MR images of all 85 patients were transferred to hard copy with standardized window settings. Two neuroradiologists (J.T., C.K.K.) interpreted the images. They had 7 and 10 years of experience, respectively, in reading neurologic MR images and 14 months of expertise in the interpretation of high-field-strength 3.0-T DW MR images (particularly in regard to the distinction of susceptibility-induced high SI at tissue interfaces at 3.0 T). These neuroradiologists were blinded to the imaging technique and the identity and clinical symptoms of the patients.

Readers were asked to rate, in consensus, the image quality with a five-point scale in regard to presence of artifacts (susceptibility-induced image distortions or SI changes), delineation of anatomic details (presence of blurring), SENSE-related artifacts (incomplete unfolding and periodic artifacts), and overall apparent SNR. A score of 1 was assigned in cases in which the image quality was considered nondiagnostic. A score of 2 (poor) was assigned in cases in which substantial artifacts (image distortions or SENSE-related artifacts) were observed that interfered with the diagnosis in some but not all anatomic parts of the images (usually the posterior fossa and/or base of the skull and the frontopolar region). A score of 3 (satisfactory) was assigned in cases in which major image distortions or major blurring were observed or in which major SENSE-reconstruction artifacts were observed but a diagnosis was still believed to be possible in all anatomic regions. A score of 4 (good) was assigned in cases in which only minor artifacts (discrete image distortions or periodic artifacts and no blurring) were present. A score of 5 (excellent) was assigned in cases in which there were no artifacts.

Image Interpretation
At two separate reading sessions, the same two neuroradiologists, who were blinded to the respective imaging technique, to the findings in structural cerebral MR imaging, and to the clinical findings in the 85 patients, were asked to interpret the diffusion images in consensus. For this purpose, the two sets of imaging studies (respective DW MR images obtained with SENSE and with conventional phase encoding in the same patient, together with the corresponding ADC maps) were separated. On the first day, the DW MR images obtained with SENSE plus ADC maps in 45 patients were intermixed with those obtained with conventional phase encoding in the remaining 40 patients. At the second reading session, the DW MR images obtained with conventional phase encoding in the first 45 patients were mixed with those obtained with SENSE in the other 40 patients. By using this setup, we attempted to reduce a possible diagnostic bias, which would have occurred if the images had been shown within one session.

Readers were asked to interpret the images and code the confidence in their diagnoses according to the following categories: A category of 1 or 2 was assigned if the image was considered definitively or probably negative in regard to the presence of ADC abnormalities. A category of 3 was assigned if the image was considered equivocal. A category of 4 or 5 was assigned if the image was considered probably or definitively positive. For the purpose of assessing diagnostic accuracy, a diagnosis category of 4 or 5 was considered positive, and categories of 1–3 were considered negative. If the final diagnosis was ischemia or other cause of focal ADC changes (eg, secondary to a tumor), diagnosis categories of 4 and 5 were considered true-positive, and a diagnosis category of 1–3 was considered false-negative; if the patient’s final diagnosis was "no DW MR imaging abnormality," categories of 1–3 were considered true-negative, and categories of 4 and 5 were considered false-positive.

Reference Standard
A study was considered positive for lesions on DW MR images if a circumscribed area of high SI was identified on the isotropic DW images ("diffusion trace images") that revealed a low SI correlate on the ADC maps (in cases of subacute stroke) and/or that proved to have a distinct correlate on the corresponding structural images (fluid-attenuated inversion-recovery or T2-weighted turbo spin-echo MR images). Confluent microembolic lesions that occurred in the territory of the same brain-supplying artery were considered as a single lesion. Follow-up MR imaging was available to confirm the presence of completed stroke at the site of the presumed lesion on DW MR images in 61 of 85 patients; however, owing to the well-established volatile nature and reversibility of ADC changes, follow-up would not seem an adequate means for validation anyway.

Statistical Analysis
The statistical software package (SPSS, version 12.0 for Windows; SPSS, Chicago, Ill) was used for analysis. The matched-pairs Wilcoxon signed rank test was used to compare DW MR imaging with conventional phase encoding and that with SENSE for the following: (a) image quality, (b) overall SNR, (c) overall relative SI, (d) lesion contrast ( SI), (e) number of lesions detected, (f) diagnostic confidence with which a diagnosis of a lesion was determined on a DW MR image, and (g) confidence with which exclusion of a lesion was possible. The Wilcoxon signed rank test for matched pairs was chosen rather than the Student t test for matched pairs, because the latter requires proof of normal distribution of values, which is impossible to obtain and is probably inadequate to assume in view of the small size of the respective data samples. A difference with P < .05 indicated statistical significance. The SNR, contrast-to-noise ratio, relative SI, and lesion contrast were determined in the first 17 of 85 patients. Image quality, number of lesions detected, and diagnostic confidence were assessed in all 85 patients. To account for clustering of data in patients with more than one lesion, we calculated lesion contrast and diagnostic confidence; a mean value was calculated per patient and used for further analysis.

Diagnostic sensitivity was calculated by dividing the number of true-positive diagnoses by the number of true-positive plus false-negative diagnoses. Specificity was calculated by dividing the number of true-negative diagnoses by the number of true-negative plus false-positive diagnoses. Diagnostic accuracy was calculated by dividing the sum of true-positive and true-negative diagnoses by the total number of all diagnoses. The exact 95% confidence interval was calculated on the basis of the binomial distribution.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A total of 48 areas with restricted diffusion, high SI on DW MR images and low SI on corresponding ADC maps (in short, ADC lesions), were present in 24 (28%) of 85 patients, with one to six lesions per patient: 13 patients had one lesion each, seven patients had three each, two patients had two each, and two patients had four and six lesions each. In 24 patients, 17 had subacute embolic or microembolic ischemic stroke, five had a primary brain tumor, and two had inflammatory lesions with restricted diffusion. Of 85 patients, 61 (72%) received the final diagnosis of no ADC abnormality.

Image Quality Assessment
An example of the image quality obtained with DW MR imaging without and with SENSE is presented in Figure 1. The distribution of image quality scores is presented in Figure 2.

View larger version (48K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (89K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (55K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (67K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (98K): [in this window] [in a new window] [Download PPT slide]   Figure 1e. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (60K): [in this window] [in a new window] [Download PPT slide]   Figure 1f. Transverse DW single-shot MR images obtained in a 56-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) due to ischemia in left internal capsule. The patient had a history of left-sided hemorrhagic cerebellar infarction. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) acquired with conventional phase encoding show comparison of image quality in different anatomic areas (posterior fossa, temporal lobes, hemispheres close to vertex). (d-f) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition) in the same anatomic location as in a-c. On the DW MR images acquired with conventional phase encoding in a-c, significant image distortions were observed in all three anatomic regions. Diffuse SI increase in cerebellum is seen in a, which is due to susceptibility effects, compared with the same section on DW MR image acquired with SENSE in d. Old hemorrhagic infarction (arrow) is hardly visible in a but clearly visible in corresponding d. Image distortions and focal SI increase secondary to susceptibility are seen in b; effects are reduced, although not completely absent, in corresponding e. Substantial image blurring of cortical gyri and sulci are observed in c; blurring is substantially reduced in corresponding f. Absence of artifacts related to the SENSE algorithm is observed.

View larger version (18K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Histogram of image quality scores assigned in 85 patients with DW MR imaging with conventional phase encoding (c-DWI) and with SENSE (S-DWI). Image quality was rated with a five-point scale.

View larger version (92K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Transverse DW single-shot MR images obtained in 48-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) caused by ischemia in territory of left middle cerebral artery secondary to high-grade stenosis of internal carotid artery. Note equivalent apparent SNR on DW MR images acquired with conventional encoding and with SENSE. (a, b) MR images (4283/79) of consecutive sections acquired with conventional phase encoding. Diffuse susceptibility-induced SI changes and their effect on lesion conspicuity. (c, d) MR images (3141/69, reduction factor of three) of consecutive sections acquired with SENSE (parallel data acquisition). Note the confluent SI changes in the right hemisphere in a and b, which were classified as susceptibility induced on the basis of ADC maps, follow-up MR imaging findings, and clinical data. Compare these findings with the normal appearance of the same cerebral areas in c and d. Conspicuity of the embolic ADC lesions in the left hemisphere is maintained in c and d compared with a and b.

View larger version (75K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Transverse DW single-shot MR images obtained in 48-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) caused by ischemia in territory of left middle cerebral artery secondary to high-grade stenosis of internal carotid artery. Note equivalent apparent SNR on DW MR images acquired with conventional encoding and with SENSE. (a, b) MR images (4283/79) of consecutive sections acquired with conventional phase encoding. Diffuse susceptibility-induced SI changes and their effect on lesion conspicuity. (c, d) MR images (3141/69, reduction factor of three) of consecutive sections acquired with SENSE (parallel data acquisition). Note the confluent SI changes in the right hemisphere in a and b, which were classified as susceptibility induced on the basis of ADC maps, follow-up MR imaging findings, and clinical data. Compare these findings with the normal appearance of the same cerebral areas in c and d. Conspicuity of the embolic ADC lesions in the left hemisphere is maintained in c and d compared with a and b.

View larger version (91K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. Transverse DW single-shot MR images obtained in 48-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) caused by ischemia in territory of left middle cerebral artery secondary to high-grade stenosis of internal carotid artery. Note equivalent apparent SNR on DW MR images acquired with conventional encoding and with SENSE. (a, b) MR images (4283/79) of consecutive sections acquired with conventional phase encoding. Diffuse susceptibility-induced SI changes and their effect on lesion conspicuity. (c, d) MR images (3141/69, reduction factor of three) of consecutive sections acquired with SENSE (parallel data acquisition). Note the confluent SI changes in the right hemisphere in a and b, which were classified as susceptibility induced on the basis of ADC maps, follow-up MR imaging findings, and clinical data. Compare these findings with the normal appearance of the same cerebral areas in c and d. Conspicuity of the embolic ADC lesions in the left hemisphere is maintained in c and d compared with a and b.

View larger version (64K): [in this window] [in a new window] [Download PPT slide]   Figure 3d. Transverse DW single-shot MR images obtained in 48-year-old man with clinical symptoms of acute ischemia (right-sided hemiparesis) caused by ischemia in territory of left middle cerebral artery secondary to high-grade stenosis of internal carotid artery. Note equivalent apparent SNR on DW MR images acquired with conventional encoding and with SENSE. (a, b) MR images (4283/79) of consecutive sections acquired with conventional phase encoding. Diffuse susceptibility-induced SI changes and their effect on lesion conspicuity. (c, d) MR images (3141/69, reduction factor of three) of consecutive sections acquired with SENSE (parallel data acquisition). Note the confluent SI changes in the right hemisphere in a and b, which were classified as susceptibility induced on the basis of ADC maps, follow-up MR imaging findings, and clinical data. Compare these findings with the normal appearance of the same cerebral areas in c and d. Conspicuity of the embolic ADC lesions in the left hemisphere is maintained in c and d compared with a and b.

View larger version (119K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Transverse DW single-shot MR images acquired in 70-year-old man with clinical symptoms of acute ischemia (left-sided brachiofacial hemiparesis) show focal susceptibility-induced SI changes on MR images obtained with conventional phase encoding that led to false-positive diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a, b) MR images (4283/79) acquired with conventional phase encoding. (c, d) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition). Circumscribed ischemic lesion (arrow in a and c) in right central region is visible on images acquired with both pulse sequences. Circumscribed focal SI increase, which was observed in contralateral cortex in b (arrow), was rated as false-positive (susceptibility induced) on the basis of ADC map and clinical data. Lesion is absent on corresponding DW MR image acquired with SENSE in d.

View larger version (112K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Transverse DW single-shot MR images acquired in 70-year-old man with clinical symptoms of acute ischemia (left-sided brachiofacial hemiparesis) show focal susceptibility-induced SI changes on MR images obtained with conventional phase encoding that led to false-positive diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a, b) MR images (4283/79) acquired with conventional phase encoding. (c, d) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition). Circumscribed ischemic lesion (arrow in a and c) in right central region is visible on images acquired with both pulse sequences. Circumscribed focal SI increase, which was observed in contralateral cortex in b (arrow), was rated as false-positive (susceptibility induced) on the basis of ADC map and clinical data. Lesion is absent on corresponding DW MR image acquired with SENSE in d.

View larger version (129K): [in this window] [in a new window] [Download PPT slide]   Figure 4c. Transverse DW single-shot MR images acquired in 70-year-old man with clinical symptoms of acute ischemia (left-sided brachiofacial hemiparesis) show focal susceptibility-induced SI changes on MR images obtained with conventional phase encoding that led to false-positive diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a, b) MR images (4283/79) acquired with conventional phase encoding. (c, d) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition). Circumscribed ischemic lesion (arrow in a and c) in right central region is visible on images acquired with both pulse sequences. Circumscribed focal SI increase, which was observed in contralateral cortex in b (arrow), was rated as false-positive (susceptibility induced) on the basis of ADC map and clinical data. Lesion is absent on corresponding DW MR image acquired with SENSE in d.

View larger version (119K): [in this window] [in a new window] [Download PPT slide]   Figure 4d. Transverse DW single-shot MR images acquired in 70-year-old man with clinical symptoms of acute ischemia (left-sided brachiofacial hemiparesis) show focal susceptibility-induced SI changes on MR images obtained with conventional phase encoding that led to false-positive diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a, b) MR images (4283/79) acquired with conventional phase encoding. (c, d) MR images (3141/69, reduction factor of three) acquired with SENSE (parallel data acquisition). Circumscribed ischemic lesion (arrow in a and c) in right central region is visible on images acquired with both pulse sequences. Circumscribed focal SI increase, which was observed in contralateral cortex in b (arrow), was rated as false-positive (susceptibility induced) on the basis of ADC map and clinical data. Lesion is absent on corresponding DW MR image acquired with SENSE in d.

View larger version (77K): [in this window] [in a new window] [Download PPT slide]   Figure 5a. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (69K): [in this window] [in a new window] [Download PPT slide]   Figure 5b. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (57K): [in this window] [in a new window] [Download PPT slide]   Figure 5c. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (78K): [in this window] [in a new window] [Download PPT slide]   Figure 5d. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (65K): [in this window] [in a new window] [Download PPT slide]   Figure 5e. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (59K): [in this window] [in a new window] [Download PPT slide]   Figure 5f. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (87K): [in this window] [in a new window] [Download PPT slide]   Figure 5g. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

View larger version (103K): [in this window] [in a new window] [Download PPT slide]   Figure 5h. Transverse DW single-shot MR images in 67-year-old woman with clinical symptoms of microembolic stroke show susceptibility-induced SI changes on images obtained with conventional phase encoding that led to false-negative diagnosis. Note equivalent apparent SNR on DW MR images acquired with conventional phase encoding and with SENSE. (a-c) MR images (4283/79) of three consecutive sections acquired with conventional phase encoding. (d-f) MR images (3141/69, reduction factor of three) of corresponding consecutive sections acquired with SENSE (parallel data acquisition). (g) ADC map and close-up view (upper right image) calculated from f. (h) High-spatial-resolution T2-weighted turbo spin-echo MR image and close-up view (upper right image) (4700/80, 512 x 512 matrix, 3-mm section thickness) obtained in area of DW abnormality. Note multiple cortical SI changes in left frontal cortex in a-c. Note ischemic lesion (arrow in f), which is clearly visible on image obtained with SENSE in left frontal paramedian cortex. Lesion is visible on corresponding MR image obtained with conventional phase encoding in c but is almost obscured by confluent susceptibility-induced cortical SI changes and was therefore missed at prospective image interpretation. Subtle correlate (arrow in upper right images in g and h) was observed on corresponding T2-weighted turbo spin-echo MR image in h and ADC map in g for the lesion on the MR image obtained with SENSE but not for the susceptibility-induced cortical SI changes.

At DW MR imaging with SENSE, apparent SNR was rated as high in all cases. Both the bulk susceptibility effects and the image blurring were significantly reduced or even prevented (Fig 1d). The diffusely increased SI in the areas close to the bone structures was eliminated, as were the focal susceptibility effects in the frontolateral cortex. Image quality on the images acquired with SENSE was rated consistently at least one score point higher compared with that on those acquired with conventional phase encoding. In fact, in none of the 85 patients did the DW MR images obtained with conventional phase encoding receive the same rating as that which was assigned to the respective DW MR images obtained with SENSE. The mean score of image quality on the MR images obtained with SENSE was 4.0, with a median of 4, compared with that of 2.9 and a median of 3, for the images obtained without SENSE.

A total of four DW MR images obtained with SENSE received a rating of 5 (ie, excellent image quality without any artifacts). In the majority of studies (76 [89%] of 85 patients), there were minor distortions on images to an extent that seemed about comparable to what one would expect to see with single-shot spin-echo echo-planar DW MR imaging at 1.5 T. Also, subtle ghosting artifacts were present that did not impair the overall impression of image quality. An image quality score of 3 was assigned in the remaining five (6%) of 85 patients because of stronger susceptibility effects; major SENSE-related artifacts or reconstruction errors were not noted in our cohort. An image quality score of 2 or 1 (poor or nondiagnostic) was not assigned for the DW MR images obtained with SENSE.

The median difference in the image quality scores of the DW MR images obtained with SENSE compared with those obtained with conventional phase encoding was highly significant (P < .001, Wilcoxon matched-pairs signed rank test).

Image Interpretation
On the DW MR images obtained with SENSE, readers prospectively diagnosed 48 (100%) of 48 lesions. On the DW MR images obtained with conventional phase encoding, 45 (94%) of 48 lesions were prospectively identified, whereas three (6%) of 48 lesions in three patients were not described. In two of these three patients, the lesion that was not diagnosed at DW MR imaging with conventional phase encoding represented a solitary lesion; in one patient, multiple lesions were present, one of which was not prospectively diagnosed at DW MR imaging with conventional phase encoding. In two of three lesions that escaped the diagnosis at DW MR imaging with conventional phase encoding, a diagnostic rating of 3 (ie, equivocal) had been assigned because SI changes were seen that probably (albeit not definitely) were thought to represent susceptibility-induced changes (Fig 5). In the third patient, multiple ischemic lesions and multiple focal susceptibility effects were present; therefore, a tiny microembolic lesion in the right caudate nucleus was simply overlooked at DW MR imaging with conventional phase encoding. In retrospect, all three lesions were visible when the DW MR images obtained with conventional phase encoding were reviewed and were compared with the DW MR images obtained with SENSE.

With a patient-based analysis, all 24 patients who eventually received the final diagnosis of ADC lesions were identified at DW MR imaging performed with SENSE. Accordingly, with DW MR images obtained with conventional phase encoding, diagnostic sensitivity of that technique was 92% (22 of 24) with a patient-based analysis and 94% (45 of 48) with a lesion-based analysis. The corresponding values for DW MR images obtained with SENSE were 100% (48 of 48) and 100% (24 of 24), respectively.

Because significantly fewer SI changes were present secondary to susceptibility effects on the DW MR images obtained with SENSE, the lesions stood out against the background much more clearly than they did on the images obtained with conventional phase encoding (Figs 3, 4). This translated into a significantly higher diagnostic confidence in regard to the identification of lesions: In the 24 patients with lesions, a mean diagnostic score of 4.8 was obtained in those who underwent DW MR imaging with SENSE, compared with a mean score of 4.4 in those who underwent DW MR imaging with conventional phase encoding. This difference proved to be statistically significant (P < .05, matched-pairs Wilcoxon signed rank test).

In two of 85 patients, findings at DW MR imaging with conventional phase encoding were classified as diagnostic category 4, possibly positive for ADC lesions, whereas no clear correlative findings were observed at ADC mapping, follow-up MR imaging, or clinical examination. Accordingly, these diagnoses were classified as false-positive (one example is given in Fig 4). Both cases of false-positive classification occurred in patients who had ADC lesions in other parts of the brain. Accordingly, with a patient-based analysis, diagnostic specificity was equivalent for DW MR imaging with both conventional phase encoding and SENSE (61 [100%] of 61).

In the 61 patients who received the final diagnosis of having no ADC lesions, however, the confidence with which lesions were excluded was lower at DW MR imaging with conventional phase encoding compared with that with SENSE. The mean score at DW MR imaging with conventional phase encoding was 1.9 ± 0.7 (standard deviation), with a median of 2, compared with a mean score of 1 ± 0.1, with a median of 1, at DW MR imaging with SENSE; this proved to be statistically significant (P < .001).

Diagnostic Accuracy
In five of 85 patients, false-positive or false-negative diagnoses were determined at DW MR imaging with conventional phase encoding, whereas no false diagnoses were determined at that with SENSE. This translates into a diagnostic accuracy of 80 (94%) of 85, with a 95% confidence interval of 86.8% to 98.1% for DW MR imaging with conventional phase encoding versus 85 (100%) of 85, with a 95% confidence interval of 95.8% to 100% for DW MR imaging with SENSE.

Quantitative Analysis
An overview of the results in regard to quantitative analysis is presented in Figure 6. Overall SNR was measured in the first 17 patients, as described in Materials and Methods. The mean SNR in patients in whom DW MR imaging with SENSE was performed was significantly lower compared with the SNR in patients in whom DW MR imaging was performed with conventional phase encoding: For the DW MR images acquired with SENSE, the mean SNR was 97.2 ± 26.1, and for those acquired with conventional phase encoding, the mean SNR was 142.0 ± 46.2. The respective median values were 93.6 versus 135.0. The median difference proved to be statistically significant (P < .001, Wilcoxon signed rank test with matched pairs). The difference in SNR matches the expected SNR loss by 30% predicted according to Pruessmann et al (11); however, it did not match the apparent SNR perceived during clinical MR image reading, at which identical ratings were assigned for both techniques.

View larger version (17K): [in this window] [in a new window] [Download PPT slide]   Figure 6. Graph shows mean values and standard deviation of SNR, relative SI, and lesion contrast for DW MR imaging with SENSE (gray bars) compared with that with conventional phase encoding (white bars). Error bars represent standard deviation.

Lesion contrast (SI difference between lesion and adjacent normal tissue) was measured in the same 17 patients as described in Materials and Methods. A total of 28 lesions were identified in the 17 patients and were included in the analysis; mean values of lesion contrast were calculated in patients with multiple lesions to account for clustering of data. The mean lesion-to–adjacent brain tissue contrast on the DW MR images acquired with conventional phase encoding was comparable to that on the images acquired with SENSE: The mean lesion-to–adjacent brain tissue contrast was 308.1 ± 142 for MR images obtained with SENSE and 276.6 ± 170 for those obtained with conventional phase encoding. The difference was not statistically significant.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
DW MR imaging and diffusion-tensor imaging have become indispensable tools for the detection and characterization of a variety of cerebral disease states. Most commonly, DW MR imaging is used for the early diagnosis of ischemic stroke (1–7); however, its use is well established for the distinction between a brain abscess and cystic tumors or that between subarachnoid cysts and subarachnoid epidermoid tumors (17). It has also been advocated for further investigation of inflammatory lesions (18,19) and primary and secondary brain tumors (20–22) and for use in pediatric neuroradiology (23).

In general, DW MR imaging (and even more so diffusion-tensor imaging) is associated with borderline SNR, particularly in regard to DW MR imaging with high b values (8,24). In addition, the minute measurement of the ADC is a time-consuming process—yet time is critical not only in the setting of acute stroke but also in restless patients who are unable to cooperate. This is why DW MR imaging has become clinically available only with the advent of rapid single-shot echo-planar imaging pulse sequences. To ensure acceptable acquisition times, the spatial resolution used for DW MR imaging is low; typically, a 128 x 128 imaging matrix and 6-mm-thick sections are used to keep SNR and acquisition time within clinically acceptable limits.

High-field-strength (3.0-T) MR systems seem, in principle, ideally suited to improve clinical DW MR imaging because they can be expected to offer doubled SNR compared with that offered with the 1.5-T reference standard. The high magnetic field strength, however, will degrade DW MR images because of the stronger susceptibility effects that not only increase linearly but scale exponentially with increasing field strength.

An efficient approach to reduce unwanted susceptibility effects and image blurring associated with long echo-planar readouts in single-shot DW MR imaging is to use parallel imaging. Several different techniques for parallel imaging have been proposed by different MR system vendors; they currently allow a reduction of phase-encoding steps by a factor of two to six (and recently even higher). In single-shot echo-planar imaging pulse sequences with parallel acquisition, the reduced number of phase-encoding steps translates directly into a shorter echo-planar imaging readout. This, in turn, has been shown to reduce image blurring, as well as image distortions, at DW MR imaging already at 1.5 T (16,25). As a favorable side effect, the shorter echo train also is associated with a reduction of the shortest possible echo time and repetition time. The shorter echo time and repetition time that are brought about by SENSE contribute further to the reduction of susceptibility effects and offset some of the SNR loss that is usually associated with parallel imaging: The reduced k-space coverage in parallel imaging is associated with an SNR penalty of about 30%; therefore, most clinical applications at 1.5 T are limited to a reduction factor of two to maintain acceptable SNR levels.

At 3.0 T, the inherently higher SNR should compensate for the SENSE-induced SNR loss; at the same time, having an effective means at hand that helps avoid susceptibility-induced image distortions and blurring seems to be a bare necessity.

We investigated (a) whether DW MR imaging with SENSE is feasible at 3.0 T, (b) whether DW MR imaging with SENSE can improve image quality compared with that with conventional phase encoding, and (c) whether SENSE helps to improve confidence in and accuracy of the diagnosis of ischemic lesions in patients.

In regard to the first issue, our results suggest that DW MR imaging with SENSE is feasible with 3.0-T systems. The surface coil sensitivity profile generated with the built-in quadrature body coil and the array of eight surface coils was accurate enough to allow an exact and error-free unfolding of the reduced source images affected by aliasing. The reference acquisition obtained at the beginning of the imaging session was sufficient to provide the necessary surface coil sensitivity profiles for all further parallel imaging pulse sequences; in addition, also in the pulse sequence with conventional phase encoding, the information from the reference acquisition was exploited to correct SI inhomogeneity by removing all coil-related SI variations across the field of view (constant level appearance). Errors of the reconstruction algorithm or significant SENSE-related artifacts were not seen in our patient cohort. Very subtle periodic artifacts did occur in the majority of patients; however, they were not considered to be clinically relevant.

In regard to the second issue, our results suggest that parallel imaging, such as that in our study with SENSE, was highly effective in reducing susceptibility-induced image distortions and image blurring. Without parallel imaging, there were substantial geometric distortions in the areas close to the base and the vertex of the skull (ie, in the posterior fossa, the brainstem, the basal temporal lobe, the frontopolar region, and the uppermost part of the frontoparietal cortex). The geometric image distortions were associated with a diffuse SI increase of the cerebellar and cerebral parenchyma located close to bone structures and air-filled sinuses. In addition, there were focal areas of high SI in the paramedian frontolateral cortex. Last, significant blurring impaired the assessment of cortical anatomic details, particularly in the uppermost sections of the DW MR images obtained with conventional phase encoding. These artifacts led to a poor image quality of DW MR images obtained with conventional phase encoding at 3.0 T in a substantial number of patients.

With parallel imaging, these artifacts were prevented or at least significantly reduced: The geometric distortions were reduced to a level one would expect to see with DW MR imaging at 1.5 T; the diffuse and focal SI changes were almost eliminated. This led to a consistent and significant upgrading of the image quality of the DW MR images obtained with SENSE compared with the DW MR images obtained with conventional phase encoding in the same patients. With SENSE, none of the DW MR images obtained at 3.0 T was rated as nondiagnostic or of poor image quality; in 80 (94%) of 85 patients, images were rated to offer good or excellent image quality. The nominal loss of SNR that occurred as a result of use of SENSE did not translate into reduced image quality. In fact, the images appeared to offer a higher SNR compared with the SNR of the DW MR images obtained with conventional phase encoding; we speculate that this finding was, at least in part, attributable to the shorter echo time that was achieved with the reduction of phase-encoding steps at DW MR imaging with SENSE.

In regard to the third issue, the following statements can be made: Only on DW MR images obtained with SENSE were all 48 lesions prospectively identified in the 24 patients with the final diagnosis of ADC abnormalities. Given the considerably and significantly inferior image quality of DW MR images obtained with conventional phase encoding, compared with MR images obtained with SENSE, the diagnostic sensitivity of DW MR images obtained with conventional phase encoding was still surprisingly high. With that technique, 45 (94%) of 48 lesions were correctly diagnosed, 22 (92%) of 24 patients were correctly classified as having ADC abnormalities, and diagnostic accuracy was 94% (80 of 85) compared with 100% (85 of 85) for DW MR imaging performed with conventional phase encoding versus that performed with SENSE. In regard to the mere numbers of lesion detection, the clinical advantage of SENSE seemed small compared with the substantial advantage in terms of image quality.

Yet, there was still a substantial difference in using DW MR imaging with SENSE versus that with conventional phase encoding for the diagnosis of ADC changes (P < .001). As an immediate consequence of the improved image quality, the confidence with which ADC changes could be diagnosed or excluded was significantly higher on the DW MR images obtained with SENSE compared with those obtained with conventional phase encoding. Because of the reduced susceptibility artifacts with DW MR imaging with SENSE, true ADC lesions stood out clearly, with high SI, against an otherwise calm background—as opposed to the situation at DW MR imaging with conventional phase encoding, where multiple SI changes were present at tissue interfaces, which may cause both false-positive and false-negative diagnoses, as will be discussed next.

On DW MR images obtained with conventional phase encoding, the susceptibility effects could mimic true cortical (eg, microembolic ischemic) lesions because the artifacts had similar location, size, configuration, and SI that would also be seen in actual small cortical lesions (Figs 3, 4). If these artifacts are mistaken as cortical lesions, they can cause false-positive diagnoses. False-positive diagnoses occurred in only two (2%) of 85 patients in our study, but it should be kept in mind that the readers in this study were two experienced neuroradiologists who had extensive experience with reading DW MR images in general and substantial experience with reading DW MR images obtained with high magnetic field strengths in particular. In our experience, the only way to help decide whether an SI change on a DW MR image obtained with conventional phase encoding represents a lesion or an artifact was by comparing several consecutive DW MR image sections and identifying the relatively characteristic location and course of the alleged lesion along tissue boundaries or, however time-consuming, by referring to the corresponding ADC maps.

On the other hand, the same susceptibility artifacts can give rise to false-negative diagnoses, as well. First, the diffuse or focal susceptibility-induced high-SI areas can obscure actual lesions in case they happen to have the same location and size. Again, this did not occur in our cohort; it would probably be a rare coincidence, but it is of course a conceivable scenario. Second, it is possible that small particularly peripheral cortical lesions, especially those located in the frontolateral and rostral cortex, are mistaken as susceptibility artifacts and not identified appropriately. This effect did in fact cause the three false-negative diagnoses in our study cohort (Fig 5). With SENSE, these susceptibility effects were eliminated. The absence of these possible sources of diagnostic errors explains why readers were significantly more confident in excluding the presence of a lesion by using DW MR imaging with SENSE and were more readily able to identify a lesion. We did not record the time the readers needed for interpretation of the respective DW MR images obtained with SENSE and conventional phase encoding. On the basis of the available data, however, one may speculate that the higher diagnostic confidence should not only improve the radiologic decision making but also translate into a much faster clinical MR image reading.

In addition to parallel imaging, there are other approaches that can help reduce susceptibility effects in DW imaging in general, and specifically at higher field strengths. Segmented echo-planar imaging pulse sequences (ie, multishot as opposed to single-shot techniques) reduce the echo train length and should, therefore, reduce or prevent susceptibility effects and blurring (26). Multishot techniques, however, cause a significant prolongation of the image acquisition time, usually beyond the limits that are acceptable in clinical settings, particularly in regard to the work-up of acutely ill patients. Also, and as a direct consequence of segmentation, these pulse sequences are highly sensitive to patient motion, which limits their suitability for patients with an emergency or acute stroke. Virtually the same limitations hold true for another candidate for susceptibility reduction, which is single- or multishot turbo spin-echo DW imaging. With parallel imaging, SENSE, the acquisition time is not prolonged but is even shorter, notably without any sacrifice of spatial resolution (in our setting, acquisition time was reduced from 97 seconds to 69 seconds). The calculated loss of SNR at DW MR imaging with SENSE did not translate into a clinically perceivable loss of visual SNR or image quality. This was also confirmed with the relative SI, which was even significantly higher at DW MR imaging with SENSE, compared with that with conventional phase encoding. This was probably caused by the shorter echo time and repetition time, which were achievable with SENSE and which may compensate for the SI loss attributable to use of SENSE.

There are several limitations that need to be discussed. First, although every attempt was made to blind the readers, image quality was so substantially and evidently better on DW MR images obtained with SENSE compared with those obtained with conventional phase encoding that a true blinded analysis was virtually impossible. The specific crossover setup of the two reading sessions—where at each of the two sessions images obtained with SENSE in one half of the patients were intermixed with images obtained with conventional phase encoding in the other half—was meant to help compensate for this problem with blinding. Another, even more important limitation of our study was the difficulty of obtaining an adequate standard of reference. It is well established that DW MR imaging may reveal, for example, ischemic lesions that may be undetected at structural brain imaging. Also, MR imaging follow-up is not always helpful, because actual ADC changes may be completely reversible without any trace of the changes observed on structural brain MR or CT images. This difficulty is common to all scientific studies with DW MR images; it is usually dealt with by accepting the diagnosis of a true lesion observed at DW MR imaging, provided the lesion has a clear correlate on ADC maps and is not caused by typical susceptibility effects. Still, it is possible that true lesions were rated as false-positive; that is, they were susceptibility-induced artifacts, particularly if they were observed on DW MR images obtained with conventional phase encoding.

We conclude that parallel imaging techniques such as SENSE are feasible with high-field-strength systems and offer significantly improved image quality compared with DW MR imaging with conventional phase encoding, particularly in regard to susceptibility-induced geometric image distortions and blurring. The observed gain in image quality with diffusion-weighted MR imaging at 3.0 T with SENSE significantly improved the diagnostic confidence with which ADC changes could be demonstrated or excluded. Overall diagnostic accuracy was improved from 94% (80 of 85 patients) at DW MR imaging with conventional phase encoding to 100% (85 of 85 patients) at DW MR imaging with SENSE.

	FOOTNOTES

 
Abbreviations: ADC = apparent diffusion coefficient, DW = diffusion weighted, ROI = region of interest, SENSE = sensitivity encoding, SI = signal intensity, SNR = signal-to-noise ratio

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, C.K.K.; study concepts, C.K.K., J.G., J.T.; study design, C.K.K., J.G., H.H.S.; literature research, C.K.K.; clinical studies, C.K.K., J.G., M.v.F., C.S.; data acquisition, C.K.K., J.G., M.v.F., S.G., C.S.; data analysis/interpretation, C.K.K., J.G., H.H.S.; statistical analysis, C.K.K.; manuscript preparation and definition of intellectual content, C.K.K., H.H.S., J.G.; manuscript editing and final version approval, C.K.K.; manuscript revision/review, C.K.K., H.H.S.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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