Radiol Phys Technol (2015) 8:4–12 DOI 10.1007/s12194-014-0278-x

Bilateral breast MRI by use of dual-source parallel radiofrequency excitation and image-based shimming at 3 Tesla: improvement in homogeneity on fat-suppression imaging Kinya Ishizaka • Fumi Kato • Satoshi Terae • Suzuko Mito • Noriko Oyama-Manabe • Tamotsu Kamishima • Mitsuhiro Nakanishi Hiroyuki Sugimori • Hiroyuki Hamaguchi • Hiroki Shirato



Received: 17 January 2014 / Revised: 9 June 2014 / Accepted: 9 June 2014 / Published online: 26 June 2014 Ó Japanese Society of Radiological Technology and Japan Society of Medical Physics 2014

Abstract In this study, we aimed to compare fat-suppression homogeneity on breast MR imaging by using dual-source parallel radiofrequency excitation and imagebased shimming (DS-IBS) with single-source radiofrequency excitation with volume shim (SS-Vol) at 3 Tesla. Twenty patients were included. Axial three-dimensional T1-weighted turbo-field-echo breast images with DS-IBS and SS-Vol were obtained. Fat suppression was scored with four grade points. The contrast of the pectoral muscle and the fat in each breast area was obtained in the head medial,

head lateral, foot medial, and foot lateral areas. The axillary space was calculated and compared between DS-IBS and SS-Vol. The average DS-IBS score was significantly higher than that of SS-Vol. The mean contrasts of fat in the foot lateral areas and axillary spaces on DS-IBS images were significantly higher than on SS-Vol images. Keywords Breast MRI  Fat suppression  Dual-source parallel radiofrequency excitation  Image-based shimming  3 Tesla

1 Introduction K. Ishizaka (&)  S. Mito  H. Sugimori  H. Hamaguchi  H. Shirato Department of Radiological Technology, Hokkaido University Hospital, N14 W5, Kita-ku, Sapporo 060-8648, Japan e-mail: [email protected] F. Kato  N. Oyama-Manabe Department of Diagnostic and Interventional Radiology, Hokkaido University Hospital, N14 W5, Kita-ku, Sapporo 060-8648, Japan S. Terae Department of Diagnostic Radiology, Sapporo City General Hospital, N11 W13, Chuo-ku, Sapporo 060-8604, Japan T. Kamishima Graduate School of Health Science, Hokkaido University, N12 W5, Kita-ku, Sapporo 060-0812, Japan M. Nakanishi Division of Radiology, Sapporo Medical University Hospital, S1 W17, Chuo-ku, Sapporo 060-0061, Japan H. Shirato Department of Radiation Oncology, Hokkaido University Hospital, N14 W5, Kita-ku, Sapporo 060-8648, Japan

Three-tesla (3T) magnetic resonance imaging (MRI) can theoretically obtain twice the signal-to-noise ratio as 1.5tesla (1.5T) imaging. In breast MRI with the patient in the prone position, breath movement has little effect on image quality, and breath-holding is not needed; therefore, 3T MRI has the advantage in breast MRIs that require high spatial and temporal resolution. However, 3T MRI is more sensitive than 1.5T to radiofrequency magnetic field (B1) inhomogeneities due to the standing radiofrequency (RF) wave effects accentuated by short RF quarter-wavelengths [1–4]. B1 inhomogeneities cause signal differences between the left and the right breasts by non-uniform flip angles in bilateral axial breast imaging [1–3]. In addition, in breast MRI’s main magnetic field (B0), inhomogeneities are exacerbated by the complicated shape of the breast and the wide field of view (FOV) used for bilateral breast scans [5]. In breast MRI with contrast material, fat suppression is necessary for distinguishing enhancing lesions from adjacent mammary fatty tissue [6–8]. Various fat-suppression techniques are available, but chemical-shift-selective

Bilateral breast MRI

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Fig. 1 Images of shimming area with use of image-based shimming and local field correction shim. a The shaded area indicates the shimming area used in the image-based shimming. B0 shimming can be performed selectively for the breast and axillary regions without

including the lungs and the surrounding air. b The shaded area indicates the shimming area used in the local field correction shim. B0 shimming is performed for the breast and axillary regions, including the lungs and the surrounding air

methods are the most commonly used [9, 10]. With the use of these methods, it is predicted that B1 and B0 inhomogeneities cause nonuniformity in fat suppression. The dual-source (DS) parallel RF excitation technique uses two RF ports to adapt the RF distribution to optimize RF deposition and reduce dielectric resonance effects at high field strengths [4, 11]. The use of independent transmission channels allows for optimization of the local and whole-body specific energy absorption rate (SAR), leading to reduced SAR deposition levels and decreased scan times. This technique has been reported to improve B1 homogeneity by RF shimming of each individual patient compared with the standard single-source RF excitation technique with use of 3T breast MRI [11]. ‘‘SmartExam Breast’’ is a software product that uses sophisticated algorithms to recognize the breast anatomy. ‘‘SmartExam Breast’’ provides consistent fat suppression with a fully automated three-dimensional breast-shimming technique (image-based shimming, IBS). IBS has been introduced to optimize the B0 field during MR image acquisition [12]. In IBS, a low-resolution-phase unwrapped B0 map is calculated from fast-field-echo images before clinical imaging [13]. With this technique, B0 shimming can be performed selectively for the bilateral breasts and axillary regions without including the arms, the lungs, or the surrounding air (Fig. 1). Therefore, the B0 homogeneity in these areas is expected to improve. Dual-source and image-based shimming can be used in combination; thereby, B1 and B0 inhomogeneities in fat suppression of chemical-shift-selective methods can be improved simultaneously. Additionally, B1 calibration scans [11] as well as B0 shimming can be performed selectively for the bilateral breasts and axillary regions by use of a combination of these techniques. Our purpose in this study was to determine whether or not fat suppression by dual-source parallel RF excitation with the image-based shimming (DS-IBS) method is

superior in homogeneity to that by single-source RF excitation (SS) with the local field correction shim (volume shim) in the breast and axillary regions.

2 Materials and methods 2.1 Subjects 2.1.1 Phantom study A custom phantom was created in the shape of the breast by use of a radiotherapy shell (Fig. 2). Agar and olive oil, which corresponded to the mammary gland and fat respectively, were put into a 100-mm-diameter cylindrical container. Fifty-mm-diameter containers were filled with olive oil as surrogates for axillary fat tissue. Moreover, olive oil and distilled water, which corresponded to the chest wall and thorax, respectively, were oriented to be recognized as breast by SmartExam Breast. 2.1.2 Clinical experiment This study included a total of 20 postmenopausal patients who were scheduled for a conventional breast MRI examination before operation between May 2010 and September 2010 at our institution. Their mean age was 59.3 years (range 53–78 years). The study protocol was approved by our Institutional Review Board, and the informed consent requirement was waived. 2.2 Scans 2.2.1 Phantom study All MR imaging was performed with a whole-body 3T magnet equipped with two RF ports (Achieva TX, Philips

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Fig. 2 Images of the breast phantom. a The exterior of the breast phantom, made with the radiotherapy shell. b T1-weighted image of the phantom. Olive oil corresponded to fat. Moreover, olive oil and distilled water, which corresponded to the chest wall and thorax,

respectively, were oriented to be recognized as breast by SmartExam Breast. Br breast, M mammary gland, Ax axillary, Wa chest wall, Th thorax

Medical Systems, Best, The Netherlands) and a sevenchannel SENSE breast coil. The phantom was scanned with axial 3D turbo-field echo (TFE) with DS-IBS, SS with IBS (SS-IBS), DS with volume shim (DS-Vol), and SS with volume shim (SS-Vol). The imaging parameters for the 3D-TFE imagings were as follows: a repetition time (TR) of 4.6 ms; echo time (TE) of 2.3 ms; flip angle of 10°; bandwidth of 540.1 Hz/pixel; slice thickness of 1.6 mm; matrix size of 400 9 400; FOV of 320 9 320 mm; inplane resolution of 0.8 9 0.8 mm; turbo-field echo factor of 41; and a total scan time of 1 min. Parallel imaging with a reduction factor of 2.4 was used for reduction of the total scan time. The 3D-TFE sequence incorporated a spectral attenuated inversion recovery (SPAIR) RF pulse to provide fat suppression. Volume shims were placed so that the breast and axilla phantom could be imaged adequately.

2.3 Evaluation

2.2.2 Clinical experiment In the prone position, all of the patients were scanned with axial 3D TFE with DS-IBS and SS-Vol. The scan parameters used were the same as those in the phantom study. For the scanning with SS-Vol, volume shim methods were applied from the nipple to the axillae to exclude as much of the lung and the surrounding air as possible. DS-IBS and SS-Vol were obtained continuously after the dynamic sequence at approximately 7 min following the injection of intravenous contrast. DS-IBS was obtained first in 10 cases, and SS-Vol was obtained first in the remaining 10 cases. The receiver gains of DS-IBS and SS-Vol were fixed at the maximum, and the scaling factor was also fixed. However, because the MR system does not allow the transmit gains to be fixed manually, automatic settings were used.

2.3.1 Phantom study Circular regions of interest (ROIs), each with a minimum of 200 pixels, were placed on fat in each breast and axilla phantom and each mammary gland phantom. The means of the signal intensities within the ROIs were measured. The contrast of the mammary gland and fat in each breast area and in the axillary region at DS-IBS, SS-IBS, DS-Vol, and SS-Vol was calculated. Contrast was defined as [(Sg-Sf)/ (Sg ? Sf)], where Sg was the mean signal intensity of the mammary gland and Sf was the mean signal intensity of the fat. 2.3.2 Clinical experiment 2.3.2.1 Evaluation of MR image quality The axial 3DTFE images with DS-IBS and SS-Vol were evaluated independently for the quality of the fat suppression in the breast region and the axillary region by three board-certified radiologists who were blinded to image type. For the assessment, three images in each sequence were selected by one author (K.I). Two images were for breasts (head and foot side), and the other was for axillary spaces. The poorest image in each area was selected. All images were evaluated in a completely random order. The image quality was graded on a scale of 1–4: grade 1 = poor, with distinct lingering fat signals; grade 2 = fair, with small areas with lingering fat signals; grade 3 = good, with almost no areas with lingering fat signals, but with fat signals that are not homogeneous or with a signal difference between right and left; and grade 4 = excellent, with almost no areas with lingering fat signals, and with homogeneous fat suppression (Fig. 3).

Bilateral breast MRI

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Fig. 3 Sample images for evaluation of fat suppression quality in the breast region. The image quality was graded on a scale of 1–4. a grade 1 = poor, with distinct lingering fat signals (white arrowhead); b grade 2 = fair, with small areas with lingering fat signals (white arrow); c grade 3 = good, with almost no areas with lingering fat

signals, but with fat signals that are not homogeneous or with a signal difference between right and left (black arrows); and d grade 4 = excellent, with almost no areas with lingering fat signals, and with homogeneous fat suppression

For the breast region, the lower score of the two images (head and foot side) was adopted. The average scores of the three radiologists for each region on the images with DSIBS and SS-Vol were calculated and compared. Statistical significance was tested with the Wilcoxon signed-rank test. A p value less than 0.05 was considered to indicate significance. All statistical analyses were performed with use of the statistical package R (http://www.r-project.org/). Furthermore, the axial 3D-TFE images with DS-IBS and SS-Vol were evaluated for artifacts in the breast area by one board-certified radiologist. All images with DS-IBS and SS-Vol were compared side-by-side, and the presence or absence of artifacts was assessed. When an artifact was present, the extent of the differences caused by the artifact was assessed between DS-IBS and SS-Vol.

(Fig. 4b). ROIs were placed so as to avoid motion artifacts and mammary gland signals as much as possible. However, in six subjects, an ROI could not be placed on one side of the axillary space because of motion artifacts from the heart. The mean of the signal intensities within the ROIs was measured. The contrast of pectoral muscle and fat in each breast area and in the axillary region at DS-IBS and SS-Vol was calculated. Contrast was defined as [(Sm-Sf)/ (Sm ? Sf)], where Sm was the mean signal intensity of the pectoral muscle and Sf was the mean signal intensity of the fat. Contrast was compared statistically between the two scans. Statistical significance was tested with the Wilcoxon signed-rank test. A p value less than 0.05 was considered to indicate significance.

3 Results 2.3.2.2 Contrast measurement Circular ROIs, each with a minimum of 50 pixels, were placed on fat tissue in each breast at the head medial (A region), head lateral (C region), foot medial (B region), and foot lateral area (D region) (Fig. 4a). In each area, ROIs were placed on the near and far sides from the chest wall; thus, a total of eight ROIs were placed on each breast. Two circular ROIs were placed on fat tissue in each bilateral axillary space, and an oval ROI was placed on the greater pectoral muscle

3.1 Phantom study Table 1 shows the mean contrasts of fat in each breast and axillary space on the images with DS-IBS, SS-IBS, DSVol, and SS-Vol. There was no difference in the fat suppression effect between DS and SS, in contrast to a significant lingering fat signal from having changed from IBS to volume shim (Fig. 5).

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Fig. 4 Measurement of signal intensities. Images in the head side of the breast region (a) and axillary region (b) are shown. a Head side of breast region: circular ROIs with a minimum of 50 pixels were placed on fat tissue on the near and far sides from the chest wall at the medial

and lateral areas in each breast. A total of four ROIs were placed on each breast in this image. ROIs were also placed on the foot side of the breast. b Circular ROIs were placed on fat tissue in the bilateral axillary spaces, and an oval ROI was placed on the pectoral muscle

Table 1 Mean contrasts of the breast and axillary phantom

With respect to artifacts in the breast area, the metal marker clip placed after mammotome breast biopsy was observed in 6 cases out of 20. These markers resulted in no relevant difference between the two images, however. In the remaining 14 cases, no obvious artifacts were observed in the breast areas of either image.

DS-IBS

SS-IBS

DS-Vol

SS-Vol

Rt breast

0.237

0.422

-0.280

-0.272

Lt breast

0.240

0.354

0.335

0.338

Rt axillary space

0.047

0.254

-0.473

-0.449

Lt axillary space

0.089

0.248

0.251

0.246

DS-IBS dual-source parallel radiofrequency excitation with imagebased shimming, SS-IBS single-source parallel radiofrequency excitation with image-based shimming, DS-Vol dual-source radiofrequency excitation with volume shimming, SS-Vol single-source radiofrequency excitation with volume shimming

3.2 Clinical experiment

3.2.2 Contrast measurement The mean contrasts of fat in the foot lateral areas and axillary spaces on the images with DS-IBS were 0.444 ± 0.074 and 0.502 ± 0.110, respectively. These values were significantly higher (p = 0.015 and 0.005) than those with SS-Vol (0.378 ± 0.134 and 0.392 ± 0.180) (Table 2).

3.2.1 Evaluation of MR image quality 4 Discussion 3.2.1.1 Breast region For the images with DS-IBS, 58 images out of 60 (96.7 %) were scored as good to excellent (Figs. 6, 7a). For the images with SS-Vol, 27 images out of 60 (45.0 %) were scored as good to excellent. The average score of the images with DS-IBS (3.58 ± 0.40) was significantly higher than that of the images with SS-Vol (2.26 ± 0.83, p \ 0.001). 3.2.1.2 Axillary region For the images with DS-IBS, 54 images out of 60 (90.0 %) were scored as good to excellent (Figs. 7b, 8). For the images with SS-Vol, 40 images out of 60 (66.7 %) were scored as good to excellent. The average score of the images with DS-IBS (3.32 ± 0.45) was significantly higher than that of the images with SS-Vol (2.74 ± 0.82, p \ 0.001).

The present study showed that the quality of fat suppression was improved in both the breast and axillary regions with use of DS-IBS compared to SS-Vol. The scores for image quality and the mean contrasts with DS-IBS were superior to those with SS-Vol. One of the reasons for the improvement of fat suppression is that B0 inhomogeneities were improved by use of IBS. A chemical-shift-selective fat-suppression technique such as SPAIR is sensitive to B0 inhomogeneities and tends to induce water suppression or imperfect fat suppression [14]. Therefore, it is very important to preserve B0 homogeneity by use of active shimming [15]. Generally, B0 shimming is performed by automatic first-order shimming [16] or manual adjustment of linear shim fields by changing shim values through the

Bilateral breast MRI

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Fig. 5 Images obtained from the phantom study. a DS-IBS, b SS-IBS, c DS-Vol, d SS-Vol. There was no difference in the fat suppression effect between DS and SS, in contrast to a significant lingering fat signal upon changing from IBS to volume shim (white arrows)

Fig. 6 Images of a 63-year-old woman. The overall fat suppression is more uniform on the axial 3D-TFE image with DS-IBS (a) than on that with SS-Vol (b), as noted in the lateral right breast (white arrow)

Fig. 7 Scores for image quality in the breast region (a) and axillary region (b). Of the images with DS-IBS for the breast and axillary regions, 96.4 and 89.3 %, respectively, were scored as good to excellent. Of the images with SS-Vol for the breast and axillary regions, 54.8 and 70.2 %, respectively, were scored as good to excellent

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Fig. 8 Images of a 61-year-old woman. The right axilla on the axial 3D-TFE image with DS-IBS (a) is more clearly identified than that with SS-Vol (b). Excellent fat suppression was achieved on an axial

3D-TFE image with DS-IBS (a), including the breast and axillary region, whereas fat suppression was incomplete (white arrow) at the right axillary region on the SS-Vol image (b)

Table 2 Mean contrast in 20 patients

According to Takatsu et al. [18], volume shim achieved better fat suppression than did IBS in a breast phantom when the length in the head-to-foot direction of the shimming area was reduced. Their result is in contrast to ours. This discrepancy might have been caused by the difference in the coverage for the volume shim: Takatsu et al. localized the region of the volume shim only at the breasts, whereas we localized the region including not only the breasts, but also the axillary regions as much as possible. Therefore, a portion of the lung was included in our shimming area, and greater B0 inhomogeneity could be induced. Recently, a homogeneous fat-suppression technique with use of independent shims has been reported [19]. Incorporating independent shims into dual-band spectralspatial excitation can provide homogeneous fat suppression in bilateral breast imaging. However, IBS has the advantage of being able to recognize implants such as silicon by using the signal intensities on fast-field-echo images for constructing a B0 map [13]. Therefore, it is expected that IBS has the potential to perform stable B0 shimming for any patient. The other reason would be considered the improvement of the transmission of B1 inhomogeneity achieved by the DS system. In B1-field inhomogeneity, the fat signal remains by excitation of the fat magnetization at a shallower angle than the ideal value for the chemical-shiftselective fat-suppression technique. In the DS system, measurement of the RF field distribution by use of patientadaptive RF shimming improves the B1 inhomogeneity, and spins can be excited with more homogeneous and more correct flip angles [11]. However, there was no obvious difference in the effect of fat suppression between the DS and SS in the phantom study. With the SPAIR technique used for fat suppression in our dynamic study, the fat signal was excited by the adiabatic inversion pulse, which was

DS-IBS

SS-Vol

p value

Head medial

0.412 ± 0.056

0.446 ± 0.082

0.110

Foot medial

0.475 ± 0.066

0.477 ± 0.130

0.765

Head lateral

0.403 ± 0.066

0.358 ± 0.115

0.160

Foot lateral

0.444 ± 0.074

0.378 ± 0.134

0.015

Axillary space

0.502 ± 0.110

0.392 ± 0.180

0.005

DS-IBS dual-source parallel radiofrequency excitation with imagebased shimming, SS-Vol single-source radiofrequency excitation with volume shimming

user interface. The shimming area can be optimized by use of a local field correction shim technique for each patient [17]. However, the breast has a complicated shape and is surrounded by air, making it hard to achieve B0 homogeneity for the whole scanning area, including part of the lung. Because the lateral breast area and axillary spaces are located off-center, it becomes difficult to achieve B0 homogeneity. In contrast, IBS can avoid air regions for shimming by auto-segmentation of the breast and axillae in each individual patient. Therefore, IBS contributes greatly to the improvement of B0 homogeneity in breast MRI. In our study, all subjects had MR examinations performed before operation, so that we could not show the usefulness in postoperative cases. In the case where there are differences in the size and shape of postoperative breasts, it is predicted that there is an increase in B0 inhomogeneity due to there being an increase in volume of air within the shimming area. IBS would be able to realize the shape of the breasts in each patient (each examination) by scanning of fast-field-echo images before clinical images are obtained. Therefore, B0 shimming could be performed selectively for the bilateral breasts and axillary regions regardless of a difference in the breast size. IBS is expected to have utility in postoperative cases as well.

Bilateral breast MRI

found to be relatively insensitive to B1 variations [20, 21]. A recent study has shown that breast MRI at 7T with adiabatic-based fat suppression produces an image quality that is as good as or better than that at 3T [9]. Therefore, we considered that IBS had a more profound effect than DS in improving fat suppression in this clinical experiment. In the phantom study, the contrast of DS-IBS was reduced slightly compared to SS-IBS. The details are unclear here; however, this is considered not to be relevant clinically as the image contrast of both looked almost the same. In this study, there were no differences in artifacts between DS-IBS and SS-Vol. There were no obvious artifacts in the breasts except for metal marker clips placed after biopsy. DS is a technique for improving B1 inhomogeneity by adapting the RF distribution by using two RF ports. IBS is a technique for improving B0 inhomogeneity by using localization improvement of the shimming area with software. Therefore, the combination of these techniques has no effect on the spatial resolution. Recently, the multipoint DIXON technique, which comprises fat–water separation methods by use of multiple echo images, has been applied to dynamic contrastenhanced MRI at 1.5T and has been shown to provide better fat suppression than that obtained with conventional fat-suppression techniques [8, 22]. However, not all MRI scanners can accommodate the DIXON technique. In contrast, because IBS is a shimming technique that improves B0 inhomogeneity, it is possible to achieve better fat suppression with IBS in conjunction with commonly used chemical-shift-selective methods of fat suppression. This study has some limitations. First, in the clinical experiment, DS-IBS and SS-Vol were scanned at different time points after the contrast injection. However, it is considered that the influence of difference in time point was small for the following reasons: (1) the scanning order of the two sequences was divided equally among subjects, (2) both images were acquired more than 7 min after the contrast injection, and (3) fat and the greater pectoral muscle, for which signal intensities were measured, are the tissues with the mildest contrast enhancement effects. Second, signal-to-noise ratios (SNRs) were not measured. It would be expected that the SNR is varied by adapting of the RF distribution to optimize the RF deposition with the DS technique. However, in this study, it was difficult to compare the SNR between DS-IBS and SS-Vol because the signal intensities of fat in the breast are greatly influenced by fat-suppression effects. Third, the contrasts of lesions were not measured. There are some limitations for using this technique in clinical practice. Because DS and IBS required a B1 calibration scan and a fast-field-echo image for the B0 map [13], respectively, the total examination time was extended by scanning these images. Further, as

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we have mentioned above, a volume shim enables better fat suppression than does IBS in some situations [18]. The shimming technique that is suitable for achievement of homogeneous fat suppression should be determined case by case, depending on the breast shape or the coverage of the shimming area. We think that IBS is a first choice as a B0 shimming method when axillary spaces are included in the shimming area; however, it may be necessary to consider using another shimming technique such as volume shim in cases of robust fat-suppression inhomogeneity.

5 Conclusion In the clinical experiment, fat suppression in the breast and axillary regions by DS combined with IBS was superior to that by SS-Vol in both qualitative and quantitative estimation. IBS is helpful for fat suppression of bilateral breast MRI at 3T. Conflict of interest The authors declare that they had no conflict of interest in this study.

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Bilateral breast MRI by use of dual-source parallel radiofrequency excitation and image-based shimming at 3 Tesla: improvement in homogeneity on fat-suppression imaging.

In this study, we aimed to compare fat-suppression homogeneity on breast MR imaging by using dual-source parallel radiofrequency excitation and image-...
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