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Cerebral Microbleeds: Accelerated 3D T2*-weighted GRE MR Imaging versus Conventional 2D T2*-weighted GRE MR Imaging for Detection¹

¹ From the Departments of Epidemiology & Biostatistics (M.W.V., M.A.I., M.M.B.B.) and Radiology (M.W.V., P.A.W., G.P.K., A.v.d.L.), Erasmus MC University Medical Center, 's-Gravendijkwal 230, 3015 CE Rotterdam, the Netherlands. Received July 3, 2007; revision requested September 3; revision received September 25; final version accepted February 1, 2008. Address correspondence to A.v.d.L. (e-mail: a.vanderlugt@erasmusmc.nl).

	ABSTRACT

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The purpose of this study was to prospectively compare high-spatial-resolution accelerated three-dimensional (3D) T2*-weighted gradient-recalled-echo (GRE) magnetic resonance (MR) images with conventional two-dimensional (2D) T2*-weighted GRE MR images for the depiction of cerebral microbleeds. After obtaining institutional review board approval and informed consent, 200 elderly participants (age range, 69.7–96.7 years; 108 [54%] women) were imaged at 1.5 T by using both sequences. Presence, number, and location of microbleeds were recorded for both sequences, and differences were tested by using McNemar and signed rank tests. Cerebral microbleeds were detected in significantly more participants on 3D T2*-weighted GRE images (35.5%) than on 2D T2*-weighted GRE images (21.0%; P < .001). Furthermore, in persons with microbleeds visualized on both image sets, significantly more microbleeds (P < .001) were seen on 3D images than on 2D images. For both sequences, the proportion of participants with a microbleed in a lobar (cortical gray and subcortical white matter), deep, or infratentorial location was similar. In conclusion, accelerated 3D T2*-weighted GRE images depict more microbleeds than do conventional 2D T2*-weighted GRE images.

© RSNA, 2008

	INTRODUCTION

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Cerebral microbleeds are hemosiderin deposits in the brain that are caused by leakage of red blood cells from small blood vessels (1). These hemosiderin deposits can be visualized by using T2*-weighted gradient-recalled-echo (GRE) magnetic resonance (MR) imaging sequences, and they appear as small foci of decreased signal intensity (1). The paramagnetic properties of hemosiderin induce local magnetic field inhomogeneities that result in phase shifts. T2*-weighted GRE sequences are very sensitive to such phase shifts, as they lack a 180° refocusing pulse (2,3).

The presence of microbleeds has been found to be related to risk of hemorrhagic transformation after ischemic stroke and to recurrence of spontaneous intracerebral bleeding (4–7). There are controversial results (8–12) suggesting that the presence of cerebral microbleeds indicates an increased risk of bleeding complications from thrombolytic treatment or the use of antiplatelet drugs. For these reasons, it is important to accurately identify those patients who have cerebral microbleeds.

Traditionally, two-dimensional (2D) T2*-weighted GRE sequences have been used for imaging of microbleeds (2,4,6,13). Haacke et al (14) presented a new method, which they refer to as susceptibility-weighted imaging, to further enhance T2*-weighted effects by using the phase information of the images collected. This susceptibility-weighted imaging method was primarily designed to increase the conspicuity of deoxygenated blood for applications in venography. For the detection of microbleeds, it is not so much phase information that needs to be enhanced (as hemosiderin will cause strong phase shifts anyway), but that advances may lie more in imaging at a higher spatial resolution to minimize partial volume effects and enable the detection of smaller microbleeds. The longer acquisition time associated with imaging at small voxel sizes can be reduced through acceleration by parallel imaging. The purpose of our study, therefore, was to prospectively compare images obtained with a high-spatial-resolution accelerated three-dimensional (3D) T2*-weighted GRE sequence with those obtained with a conventional 2D T2*-weighted GRE sequence for the depiction of cerebral microbleeds.

	MATERIALS AND METHODS

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Study Participants
Our study was performed in participants from a larger population-based prospective cohort study, the Rotterdam Study, that aims to assess determinants of diseases in the elderly (15). For the larger study, institutional review board approval was obtained, as was informed consent from all participants. In previous years of the study, MR imaging had been performed in a randomly selected subset of participants. In 2006, all individuals who had undergone MR imaging in a previous round of the study and who were still alive and did not have contraindications to MR imaging were invited for repeat brain MR imaging with a new imaging protocol, which included sequences sensitive enough to allow detection of cerebral microbleeds, as described below. Our institutional review board (Erasmus MC University Medical Center, Rotterdam, the Netherlands) approved the study. In total, 254 participants from the larger study were eligible for our study; 207 (81.5%) agreed to participate and gave informed consent. In four participants, imaging could not be completed due to physical problems; while in three participants, artifacts from motion or metallic dental implants prevented proper assessment. This left a total of 200 participants for analysis.

MR Imaging
Imaging was performed on a 1.5-T imager (GE Healthcare, Milwaukee, Wis) with an eight-channel head coil. Two technologists (both with 2 years experience performing brain MR imaging) performed all MR imaging examinations according to a standardized protocol. In all participants, conventional 2D T2*-weighted GRE MR imaging and accelerated 3D T2*-weighted GRE MR imaging (both spoiled GRE sequences) were performed (Table 1). Two-dimensional T2*-weighted GRE was performed with flow compensation with an echo time of 20 msec and a section thickness of 5 mm, in line with conventional settings (4,5,13,16–18). The 3D T2*-weighted GRE sequence was fully velocity compensated (with gradient moment nulling in all three orthogonal directions) and was performed with a smaller voxel size (Table 1) than the 2D T2*-weighted GRE sequence. To compensate for the decrease in dephasing associated with acquisition at a smaller voxel size, the echo time used for the 3D T2*-weighted GRE sequence was increased to 31 msec. Increasing the echo time also enabled us to lower bandwidth and thus to increase the signal-to-noise ratio on the 3D T2*-weighted GRE images. The flip angle for the 3D T2*-weighted GRE sequence was empirically set at 13° to obtain a rather homogeneous signal intensity for gray and white matter. By using this flip angle, the signal intensity of cerebrospinal fluid appeared just slightly darker than that of gray and white matter, enabling the distinction of sulci. Because acquisition in a 3D format considerably increases acquisition time, parallel imaging with an acceleration factor of two was applied to reduce acquisition time for the 3D T2*-weighted GRE sequence to acceptable and practical limits (5 minutes 55 seconds).

The use of parallel imaging in the 3D T2*-weighted GRE sequence led to a postacquisition reconstruction time of about 5 minutes. To avoid a lag in data output and subsequent stop in imaging, the accelerated 3D T2*-weighted GRE was always performed at the end of the MR imaging protocol.

Rating of Cerebral Microbleeds
Acquisition date and participant identification were removed from all images. The 2D T2*-weighted GRE and 3D T2*-weighted GRE images were randomly allocated to one of two reviewers (M.W.V., M.A.I., both with 2.5 years experience reading neurologic MR images). Reviewers were blinded to the other sequence and to all clinical information. Two-dimensional T2*-weighted GRE images were read first, in random order; after a 3-week gap, the 3D T2*-weighted GRE images were read, again in random order. Fifty randomly selected 2D T2*-weighted GRE and 3D T2*-weighted GRE images were rated by both reviewers.

Reviewers independently rated the presence, location, and number of all cerebral microbleeds. Microbleeds were defined as focal areas of very low signal intensity that were smaller than 10 mm in size (13,16). In accordance with previous studies (13,16), they were categorized into one of three locations: lobar (cortical gray matter and subcortical white matter), deep (deep gray matter [basal ganglia and thalamus] and deep white matter [corpus callosum]), or infratentorial (brainstem and cerebellum). Signal voids caused by sulcal vessels, symmetric calcifications in the deep gray matter, choroid plexus calcifications, pineal calcification, and signal averaging from bone were excluded.

All studies with a potential microbleed were reviewed for confirmation by an experienced neuroradiologist (A.v.d.L., with 7 years experience reading neurologic MR images), again with a 3-week gap between the review of both sequences. At this time, the T1-weighted images additionally were used to confirm the location of microbleeds, as the inherent properties of microbleeds will cause them to appear as a focus of low signal intensity (without marked blooming) on the T1-weighted image as well. Thus, the T1-weighted image further facilitated differentiation of microbleeds from calcification in the ventricle or from sulcal vessels. Afterwards, dissimilarities between conventional 2D T2*-weighted GRE and accelerated 3D T2*-weighted GRE images were assessed in a side-by-side comparison.

Statistical Analysis
For the 50 images of each sequence that were read by both reviewers, we tested the interobserver reliability for microbleed rating by using Cohen test. The following interpretation of the statistic was used: 0–0.20 = poor agreement, 0.21–0.40 = fair agreement, 0.41–0.60 = moderate agreement, 0.61–0.80 = good agreement, and 0.81–1 = very good agreement (19). The prevalence and multiplicity of cerebral microbleeds were calculated for both sequences, and statistical significance of the difference was tested by using the nonparametric McNemar test for paired proportions. Furthermore, for both sequences we calculated the proportion of participants who had microbleeds in lobar, deep, or infratentorial brain locations. For those participants whose studies showed microbleeds on images obtained with both sequences, we tested whether significantly more microbleeds were visible on one image set compared with the other by using the nonparametric Wilcoxon signed rank test, as the number of microbleeds was not normally distributed. A two-tailed P value less than .05 was considered to indicate a statistically significant difference. All analyses were performed by using a statistical software package (SPSS, version 11.0.1 for Windows; SPSS, Chicago, Ill).

	RESULTS

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Microbleeds
The mean age of the 200 participants was 79.2 years (range, 69.7–96.7 years). One hundred eight (54.0%) were women. Cerebral microbleeds (Figure) were detected on the 2D T2*-weighted GRE images of 42 (21.0%) participants and on the accelerated 3D T2*-weighted GRE images of 71 (35.5%) participants (Table 2). The difference in the prevalence of cerebral microbleeds between the sequences was highly significant (P < .001).

View larger version (81K): [in this window] [in a new window] [Download PPT slide]   Axial MR images obtained with conventional 2D T2*-weighted GRE (left) (repetition time msec/echo time msec, 775/20; flip angle, 25°; section thickness, 5 mm) and accelerated 3D T2*-weighted GRE (right) (45/31; flip angle, 13°; section thickness, 1.6 mm zero-padded to 0.8 mm) sequences in the same participant. More cerebral microbleeds (arrows), seen bilaterally in the thalamus region, are visible on the 3D T2*-weighted GRE image than the 2D T2*-weighted GRE image.

Side-by-Side Comparison
At side-by-side comparison, there were no microbleeds visualized on the 2D T2*-weighted GRE images that were not detected on the accelerated 3D T2*-weighted GRE images. Among those persons in whom cerebral microbleeds were visible on both image sets (n = 42), significantly more microbleeds were visualized with the accelerated 3D T2*-weighted GRE sequence than with the conventional 2D T2*-weighted GRE sequence (median number of microbleeds, 2.5 vs 1.0; Wilcoxon signed rank test, P < .001).

Interobserver Reliability
Interobserver reliabilities for the studies that were evaluated by both reviewers were very good when analyzed both at individual level (2D T2*-weighted GRE, = 0.80; 3D T2*-weighted GRE, = 0.85) and at microbleed level (2D T2*-weighted GRE, = 0.90; 3D T2*-weighted GRE, = 0.82).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCE IN KNOWLEDGE IMPLICATION FOR PATIENT CARE References

 
Cerebral microbleeds were detected in more persons by using accelerated 3D T2*-weighted GRE images than by using conventional 2D T2*-weighted GRE images. Furthermore, in participants who had microbleeds detected on images from both sequences, we identified significantly more microbleeds on the 3D T2*-weighted GRE images than on the 2D T2*-weighted GRE images.

Before interpreting our data, some considerations of method and potential study limitations need to be addressed. We performed MR imaging with both sequences in a large sample of elderly persons to increase our study power. Interobserver reliability for the detection of microbleeds was very good for both sequences. We could not blind the reviewers to the sequence type, as differences between the two are readily visible. However, we tried to minimize bias by randomizing the order in which individual images were assessed and by blinding the independent reviewers to images obtained with the other sequence and to participant identification. Furthermore, the reviewers rated the two image sets with a 3-week gap between readings to eliminate recall bias.

We should also consider potential misclassification of cerebral microbleeds. Other structures in the brain (eg, deoxygenated blood in small veins, calcifications in basal ganglia or pineal gland) may resemble microbleeds on MR images. However, on the high-spatial-resolution accelerated 3D T2*-weighted GRE images, the cerebral vessels can be clearly identified as linear structures. Moreover, calcifications in the brain have a typical location and shape and, when located in the basal ganglia, are usually symmetric in distribution. We therefore believe that we did not misclassify other structures as cerebral microbleeds and thus did not overestimate the prevalence of microbleeds in either image set.

On both the 2D T2*-weighted GRE and 3D T2*-weighted GRE images, we may have missed some microbleeds in the base of the brain owing to susceptibility artifacts in T2*-weighted GRE imaging caused by air and bone interfaces.

Not only on the accelerated 3D T2*-weighted GRE images, but also on the conventional 2D T2*-weighted GRE images, the prevalence of cerebral microbleeds in our study was much higher than that previously reported in population-based studies (13,16,20) that used comparable 2D T2*-weighted GRE sequences. Possible explanations for this higher prevalence are the higher mean age of our participants (79.2 years vs 60 years [13,16,20]) and the higher field strength (1.5 T vs 1.0 T in the Framingham Heart Study [13]), which causes susceptibility artifacts from hemosiderin deposits to be more pronounced.

Two-dimensional T2*-weighted GRE sequences have previously been shown to better depict cerebral microbleeds than conventional spin-echo and fast spin-echo T2-weighted sequences (2,16). By using a 3D T2*-weighted GRE sequence, we found cerebral microbleeds in even more participants than by using a 2D T2*-weighted GRE sequence. The imaging parameters chosen for our accelerated 3D T2*-weighted GRE sequence resulted in images that had a much higher spatial resolution in comparison to those obtained with a conventional 2D T2*-weighted GRE sequence (13,16) and that could be obtained within a reasonable imaging time through use of parallel imaging. Fazekas et al (1) showed with a histopathologic analysis that conventional 2D T2*-weighted GRE images do not depict small hemosiderin deposits that consist of only a few perivascular hemosiderin-laden macrophages. The much smaller voxel size in 3D T2*-weighted GRE MR imaging enables the detection of smaller microbleeds, while the combination of increased echo time and decreased bandwidth and flip angle ensures a high signal-to-noise ratio and adequate contrast between microbleeds and other brain tissue (14,21).

This contrast could potentially be further intensified by using the proposed susceptibility-weighted imaging technique of Haacke et al (14), in which phase information is used to create a special phase mask that, when multiplied with the magnitude images, improves the apparent susceptibility weighting. This technique has been shown to be highly effective for venography in the brain (22). However, imaging of cerebral microbleeds is less likely to greatly benefit from this susceptibility-weighted imaging postprocessing method because hemosiderin deposits, in contrast to deoxygenated blood in veins, cause a consistent dephasing of spins.

Alternatively, imaging at a higher field strength (3 T or higher) might prove beneficial for microbleed detection, as susceptibility effects caused by hemosiderin would be more pronounced (23).

The presence of cerebral microbleeds has previously been found to be associated with an increased risk of adverse neurologic events (eg, recurrence of spontaneous bleeding, hemorrhagic transformation after ischemic stroke) (4,5,7). Furthermore, although a study (9) suggested that patients with stroke who have a small number of microbleeds can be safely treated by thrombolysis, the presence of more microbleeds may indicate a diffuse hemorrhage-prone vasculopathic condition (eg, cerebral amyloid angiopathy) that warrants a more prudent approach (8,11,24–26). In clinical practice, accurate identification of those patients who have cerebral microbleeds will thus become increasingly important for clinical decision making.

In conclusion, accelerated 3D T2*-weighted GRE images depict more microbleeds than do conventional 2D T2*-weighted GRE images.

	ADVANCE IN KNOWLEDGE

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• Accelerated three-dimensional T2*-weighted gradient-recalled-echo (GRE) MR images depict more cerebral microbleeds than do conventional two-dimensional T2*-weighted GRE MR images.
  

	IMPLICATION FOR PATIENT CARE

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• Identification of patients who have cerebral microbleeds may be important for clinical decision making.
  

	FOOTNOTES

 

Abbreviations: GRE = gradient-recalled echo • 3D = three-dimensional • 2D = two-dimensional

Author contributions: Guarantors of integrity of entire study, M.W.V., M.A.I., A.v.d.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, M.W.V., M.A.I., A.v.d.L.; clinical studies, M.W.V., M.A.I., M.M.B.B., A.v.d.L.; statistical analysis, M.W.V., M.A.I., A.v.d.L.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.

	References

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2481071158v1 248/1/272    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Vernooij, M. W. Articles by van der Lugt, A. Search for Related Content PubMed PubMed Citation Articles by Vernooij, M. W. Articles by van der Lugt, A.