- Email: [email protected]
Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results
Clinical Radiology xxx (2014) 1e5
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Technical Report
Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results K. Kiguchi, A. Kido*, K. Fujimoto, F. Shitano, K. Takakura, S. Daido, Y. Himoto, A. Ninomiya, H. Kusahara, Y. Fushimi, T. Okada, K. Togashi Department of Diagnostic Imaging and Nuclear Medicine, Graduate School of Medicine, Kyoto University, Japan
art icl e i nformat ion Article history: Received 10 October 2013 Received in revised form 6 January 2014 Accepted 14 January 2014
Introduction Magnetic resonance imaging (MRI) has been widely utilized for gynaecological disorders. Gadolinium-based contrast agents has been used in the evaluation of vessels, e.g., for the visualization of arteriovenous malformation (AVM) or in the planning of a uterine artery embolization (UAE). However, concerns about adverse side effects of gadolinium-based contrast agents, such as nephrogenic systemic fibrosis or hypersensitivity reactions, have stimulated investigations into the use of non-contrast-enhanced MR angiography (MRA).1,2 Recently, selective visualization of non-contrast MRA of renal or hepatic arteries have been
* Guarantor and correspondent: A. Kido, Department of Diagnostic Imaging and Nuclear Medicine, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Tel.: þ81 75 751 3419; fax: þ81 75 771 9709. E-mail address: [email protected] (A. Kido).
reported by combining the time-spatial labelling inversion pulse (Time-SLIP) method with half-Fourier fast spin-echo or balanced steady-state free precession (bSSFP).3,4 TimeSLIP is one of the arterial spin labelling techniques that can provide selective inflow information by placing the inversion pulse anywhere independent of the imaging area before data acquisition and suppress the background signal.5 This method can control the extent of the inflowing blood signal by changing the inversion time (TI). Thus, the optimization of TI is essential to obtain good contrast in Time-SLIP imaging. The purpose of the present study was to investigate the feasibility of the selective visualization of uterine arteries using Time-SLIP, and determine the optimal TI at 3 T.
Materials and methods This study was approved by the institutional review board and was conducted in accordance with the ethical
0009-9260/$ e see front matter Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2014.01.018
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
2
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
standards of the World Medical Association (Declaration of Helsinki). Written informed consent was obtained from all participants before MRI examinations. From July 2012 to February 2013, 20 women (21e47 years old, average age 31 years old) of reproductive age were included in this study. MRI images were obtained outside of the menstrual period and no pre-medication was given to any participants before the MRI examination.
MRI technique All examinations were conducted using a 3 T MRI system (Toshiba Medical Systems, Otawara, Japan), equipped with a 16 channel coil placed at the front of the abdomen, 32 channel coil placed at the back of the abdomen. Two rows were used for both front and back coils, resulting in 16 channel outputs. In addition to a routine protocol on the pelvic area, which included an axial fast spin-echo T2weighted imaging (WI), sagittal T1WI and T2WI of the uterus, each patient also underwent a non-contrastenhanced MRA using 3D bSSFP combined with Time-SLIP (detailed below). The entire MRI examination was performed within 45 min in all volunteers.
Non-contrast enhanced MRA Non-contrast-enhanced MRA using 3D bSSFP imaging sequences with fat saturation by short TI recovery pulse was performed in the coronal plane with the following parameters: 4.8 ms repetition time (TR)/2.4 ms echo time (TE)/ 120 flip angle, 5 mm section thickness, 22 sections, no gap, 350 mm 200 mm field of view, 256 128 matrix size, number of averages ¼ 1, number of acquisition ¼ 2 (tag on/ off). Final images were reconstructed into an apparent spatial resolution of 0.7 mm 0.7 mm 5 mm. TIs equal to 1200, 1400, 1600, and 1800 ms were selected for evaluation. Respiratory triggering and electrocardiography (ECG)gating were not used. After branching at the aortic bifurcation, iliac arteries run posterolaterally. Branching at the proximal portion of the internal iliac arteries, uterine arteries go downward and run along the uterus from the cervix to the corpus. Based on these vascular anatomies, a spatial selective inversion pulse (i.e., tagged region) was placed with 6 cm thickness parallel to the aorta to include the aorta as much as possible in a coronal plane subsequently to the first non-selective pulse. Imaging plane for the uterine artery was set parallel to the tagged region to cover the whole cervix, which enables efficient inclusion of the uterine artery. When imaging plane was set parallel to this tag pulse, imaging of the anteflexed uterine fundus became difficult, although this did not hinder the depiction of the uterine artery (Fig 1). The examination consisted of interleaved tag-on and tag-off scans resulting in tag-on/off subtraction images. The subtraction images were then reconstructed for minimum intensity projection (MinIP) on the MRI console. The acquisition time for non-contrast MRI alone was about 3e4 min depending on the pulse wave rate. The analysis time was about 15 min per participant.
Figure 1 A non-selective inversion-recovery pulse was placed followed by a second tag with 6 cm thickness, which covers the abdominal aorta in a coronal plane. The imaging area was set up to cover the whole cervix.
Data analysis Quantitative evaluation The signal intensity of the uterine artery was evaluated by manually placing the region of interest (ROI) on the uterine artery at the level of the parametrium for the subtraction image and on the internal iliac artery for the tag-on image (Fig 2). The ROI was placed by one of the authors with 5 years of experience in the diagnosis of gynaecological MRI. When the uterine artery was not detected at the level of the parametrium, the signal intensity was regarded as zero. The signal of the uterine artery obtained on the
Figure 2 The yellow circle shows the ROI, which was placed manually on the uterine artery at the level of the parametrium on the subtraction image. Bidirectional arrows represent the score of the tip of the uterine artery.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
subtraction image (SI uteA) was normalized by dividing it by the signal intensity of the internal iliac artery (SI iilA) obtained on the tag-on image. Thus, the relative signal intensity of the uterine artery was calculated as follows: Relative signal intensity of uterine artery (RSI uteA) ¼ SI uteA/SI iilA. The background signal was also measured. A representative background signal was determined from the absolute value (AbSI intestines) and the standard deviation of the signals of the intestines (SD intestines) in the area comprised between the bilateral internal iliac arteries on the subtraction image. Although the signals of both the intestines and the bladder can cause background noise, intestinal noise was the focus because the intestines have a larger overlap of the uterine arteries. The ROIs were placed on the section where the intestines were best visible and drawn to include as large a region of the intestines as possible.
Qualitative evaluation The non-contrast-MRA images were visually evaluated by two independent radiologists with 16 (reader A) and 5 (reader B) years of experience in female pelvic MRI. The reading radiologists evaluated the images with note of the imaging parameters. For evaluation of the uterine artery, the depiction of the uterine artery was scored on a five-point scale according to the location of the tip of the artery detected on the subtraction image. Anatomically, the uterine artery descends on the lateral wall of the pelvis, anterior to the internal iliac artery, and enters the root of the broad ligament. Here it passes medially to reach the lateral margin of the uterus immediately superior to the lateral part of the fornix of the vagina. For visual evaluation, the uterine artery was thus divided into five parts, as follows (Fig 2): the tip is (1) located in the proximal half beside the pelvic wall; (2) located in the distal half beside the pelvic wall; (3) located in the proximal half within the parametrium; (4) located in the distal half within the parametrium; or (5) within the uterine myometrium. The background signal was scored on a three-point scale (1, too much noise for diagnostic quality; 2, sufficiently little noise for diagnosis; 3, almost no noise) using the MinIP image of uterine arteries. Evaluation of the overall visualization quality was done using the MinIP image of the uterine arteries on a four-point scale (1, not visible and non-diagnostic image quality; 2, poor image quality and insufficient visualization; 3, good image quality sufficient for diagnosis; 4, excellent image quality with sharply defined uterine arteries).
Statistical analysis Statistical analyses were performed using a commercially available software package (Medcalc version 12.3.0, MedCalc Software, Ostend, Belgium). The relative signal intensity of the uterine artery, and the absolute value and the standard deviation of the signal intensity of the intestines were evaluated using one-way repeated-measures analysis of variance (ANOVA) followed by Bonferroni
3
correction for multiple comparisons. The relative signal intensities of the uterine arteries between the right and left sides were compared using paired Student’s t-test. The qualitative results of the different protocol groups were compared using Friedman’s non-parametric test. A p-value of less than 0.05 was considered significant. Interobserver variability was assessed by weighted kappa statistics.6
Results MRI was successfully performed in all volunteers. Two of the participants had fibroids (major axes were 1 and 3 cm), whereas the MRI appearance of the uterus was normal in the other volunteers.
Quantitative analysis The mean values and standard deviations of the RSI uteA on each side, AbSI intestines, and SD intestines are summarized in Fig 3. There was no significant difference between the right and the left RSI ute A (p ¼ 0.06). The highest RSI uteA value was obtained with a TI of 1400 ms for the right uterine artery, while a TI of 1600 ms was associated with the highest RSI uteA for the left uterine artery. On both sides, imaging using a TI of 1200 ms was associated with the lowest RSI. Significant differences were noted between TIs of 1200 and 1400 ms on both sides (p ¼ 0.0017 for the right, p ¼ 0.0004 for the left) and also between TIs of 1200 and 1600 ms on the left side (p ¼ 0.0005). There was no significant difference among TIs of 1400, 1600, and 1800 ms. Both AbSI intestines and SD intestines were the lowest at a TI of 1400 ms and the highest at a TI of 1800 ms. A significant difference was determined only between the SD intestines obtained at TI of 1400 and 1800 ms.
Qualitative analysis One example of MinIP images as well as the results of the qualitative evaluation performed by two readers are summarized in Figs 4 and 5. For both readers, the tip of the uterine artery was detected most distally at a TI of 1400 or 1600 ms, and most proximally at a TI of 1200 ms. The evaluation of the images at TIs of 1400, 1600, and 1800 ms were significantly higher than 1200 ms, except those at a TI of 1800 ms on the right side of the reader A (p < 0.05). Minimization of the background noise was best achieved at a TI of 1400 ms and least at a TI of 1800 ms for both readers. Significant differences were noted between TIs of 1800 and 1400 ms, and also between TIs of 1800 and 1600 ms (p < 0.05) for both readers. The overall visualization quality was highest at a TI of 1400 ms for reader A and 1600 ms for reader B, and was lowest at a TI of 1200 ms for both readers. The overall quality at both TIs of 1400 and 1600 ms was significantly higher compared with those obtained at TIs of 1200 and 1800 ms (p < 0.05). There was no significant difference between TIs of 1400 and 1600 ms.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
4
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
Figure 3 Quantitative evaluation of uterine arteries at various TIs. (a) Relative signal intensity of the right uterine arteries (right RSI uteA); (b) relative signal intensity of the left uterine arteries (left RSI uteA); (c) absolute value of the signal of the intestines (AbSI intestines); and (d) standard deviation of the signal of the intestines (SD intestines). Asterisks indicate the value pairs where significant differences were determined.
Weighted k for the assessment of the tip of the right uterine artery, left uterine artery, background signal, and overall visualization quality were scored 0.73, 0.70, 0.76, and 0.68, respectively. All the agreements were substantial.
Discussion The present study showed that Time-SLIP enables the selective visualization of uterine arteries. The poorest depiction of the uterine arteries at a TI of 1200 ms both in
the quantitative and qualitative evaluations was probably due to insufficient time for the arterial blood to enter the image acquisition area. Background signal was best suppressed at a TI of 1400 ms, and least at a TI of 1800 ms in both the quantitative and qualitative analyses. That might suggest that most of the background signal observed on the MinIP image was signal caused by intestinal movements and the null point of the intestines is around a TI of 1400 ms on average. As a result, the most amount of background signal recovery was observed at a TI of 1800 ms.
Figure 4 MinIP images of a 26-year-old participant. The images at (a) a TI of 1200 ms, (b) a TI of 1400 ms, (c) a TI of 1600 ms, and (d) a TI of 1800 ms are shown. The tip of the uterine artery was depicted most distally at a TI of 1400 or 1600 ms, and most proximally at a TI of 1200 ms. The background suppression was best achieved at a TI of 1400 ms and was poorest at a TI of 1800 ms. Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
5
Figure 5 Qualitative analysis by the readers. (a) Location of the tip of the uterine artery was scored (b) scores of background suppression, and (c) scores of overall image quality. Asterisks indicate the value pairs where significant differences were determined by both readers for both sides in (a), and by both readers in (b) and (c).
The results of the overall image quality correspond to the results mentioned above. That is, the uterine artery depiction was insufficient at a TI of 1200 ms, whereas the background suppression was unsatisfactory at a TI of 1800 ms. A limitation of the present study is that comparison with well-established contrast-enhanced MRA or commonly used time-of-flight (TOF) MRA was not undertaken. In the authors’ experience, the proximal uterine artery was visualized using TOF within approximately 2 min, which was shorter than that of Time-SLIP. However, both the visualization and acquisition time of uterine arteries should be compared under the same conditions between the two sequences for a conclusive comparison. A comparative study with TOF or contrastenhanced MRA should be undertaken in future studies. In conclusion, this report showed that the combination of the 3D bSSFP sequence with Time-SLIP technique enables selective MRA of the uterine artery. The optimal TI for visualizing the uterine artery may be between 1400 and 1600 ms.
Acknowledgements The authors thank Mr Naotaka Sakashita (Toshiba Medical Systems Corporation) and Mr Hajime Sagawa, RT, for
technical assistance. This study was supported by a sponsored research programme, “ Research for improvement of MR visualization (no. 150100700014)” provided to one of the authors, K.T., by Toshiba Medical Systems Incorporated, Japan.
References 1. Marckmann P, Skov L, Rossen K, et al. Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J Am Soc Nephrol 2006;17:2359e62. 2. Miyazaki M, Lee VS. Nonenhanced MR angiography. Radiology 2008;248:20e43. 3. Shimada K, Isoda H, Okada T, et al. Non-contrast-enhanced hepatic MR angiography with true steady-state free-precession and time spatial labeling inversion pulse: optimization of the technique and preliminary results. Eur J Radiol 2009;70:111e7. 4. Shonai T, Takahashi T, Ikeguchi H, et al. Improved arterial visibility using short-tau inversion-recovery (STIR) fat suppression in non-contrastenhanced time-spatial labeling inversion pulse (Time-SLIP) renal MR angiography (MRA). J Magn Reson Imaging 2009;29:1471e7. 5. Garcia DM, Duhamel G, Alsop DC. Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 2005;54:366e72. 6. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159e74.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
Contents lists available at ScienceDirect
Clinical Radiology journal homepage: www.clinicalradiologyonline.net
Technical Report
Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results K. Kiguchi, A. Kido*, K. Fujimoto, F. Shitano, K. Takakura, S. Daido, Y. Himoto, A. Ninomiya, H. Kusahara, Y. Fushimi, T. Okada, K. Togashi Department of Diagnostic Imaging and Nuclear Medicine, Graduate School of Medicine, Kyoto University, Japan
art icl e i nformat ion Article history: Received 10 October 2013 Received in revised form 6 January 2014 Accepted 14 January 2014
Introduction Magnetic resonance imaging (MRI) has been widely utilized for gynaecological disorders. Gadolinium-based contrast agents has been used in the evaluation of vessels, e.g., for the visualization of arteriovenous malformation (AVM) or in the planning of a uterine artery embolization (UAE). However, concerns about adverse side effects of gadolinium-based contrast agents, such as nephrogenic systemic fibrosis or hypersensitivity reactions, have stimulated investigations into the use of non-contrast-enhanced MR angiography (MRA).1,2 Recently, selective visualization of non-contrast MRA of renal or hepatic arteries have been
* Guarantor and correspondent: A. Kido, Department of Diagnostic Imaging and Nuclear Medicine, Graduate School of Medicine, Kyoto University, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Tel.: þ81 75 751 3419; fax: þ81 75 771 9709. E-mail address: [email protected] (A. Kido).
reported by combining the time-spatial labelling inversion pulse (Time-SLIP) method with half-Fourier fast spin-echo or balanced steady-state free precession (bSSFP).3,4 TimeSLIP is one of the arterial spin labelling techniques that can provide selective inflow information by placing the inversion pulse anywhere independent of the imaging area before data acquisition and suppress the background signal.5 This method can control the extent of the inflowing blood signal by changing the inversion time (TI). Thus, the optimization of TI is essential to obtain good contrast in Time-SLIP imaging. The purpose of the present study was to investigate the feasibility of the selective visualization of uterine arteries using Time-SLIP, and determine the optimal TI at 3 T.
Materials and methods This study was approved by the institutional review board and was conducted in accordance with the ethical
0009-9260/$ e see front matter Ó 2014 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2014.01.018
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
2
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
standards of the World Medical Association (Declaration of Helsinki). Written informed consent was obtained from all participants before MRI examinations. From July 2012 to February 2013, 20 women (21e47 years old, average age 31 years old) of reproductive age were included in this study. MRI images were obtained outside of the menstrual period and no pre-medication was given to any participants before the MRI examination.
MRI technique All examinations were conducted using a 3 T MRI system (Toshiba Medical Systems, Otawara, Japan), equipped with a 16 channel coil placed at the front of the abdomen, 32 channel coil placed at the back of the abdomen. Two rows were used for both front and back coils, resulting in 16 channel outputs. In addition to a routine protocol on the pelvic area, which included an axial fast spin-echo T2weighted imaging (WI), sagittal T1WI and T2WI of the uterus, each patient also underwent a non-contrastenhanced MRA using 3D bSSFP combined with Time-SLIP (detailed below). The entire MRI examination was performed within 45 min in all volunteers.
Non-contrast enhanced MRA Non-contrast-enhanced MRA using 3D bSSFP imaging sequences with fat saturation by short TI recovery pulse was performed in the coronal plane with the following parameters: 4.8 ms repetition time (TR)/2.4 ms echo time (TE)/ 120 flip angle, 5 mm section thickness, 22 sections, no gap, 350 mm 200 mm field of view, 256 128 matrix size, number of averages ¼ 1, number of acquisition ¼ 2 (tag on/ off). Final images were reconstructed into an apparent spatial resolution of 0.7 mm 0.7 mm 5 mm. TIs equal to 1200, 1400, 1600, and 1800 ms were selected for evaluation. Respiratory triggering and electrocardiography (ECG)gating were not used. After branching at the aortic bifurcation, iliac arteries run posterolaterally. Branching at the proximal portion of the internal iliac arteries, uterine arteries go downward and run along the uterus from the cervix to the corpus. Based on these vascular anatomies, a spatial selective inversion pulse (i.e., tagged region) was placed with 6 cm thickness parallel to the aorta to include the aorta as much as possible in a coronal plane subsequently to the first non-selective pulse. Imaging plane for the uterine artery was set parallel to the tagged region to cover the whole cervix, which enables efficient inclusion of the uterine artery. When imaging plane was set parallel to this tag pulse, imaging of the anteflexed uterine fundus became difficult, although this did not hinder the depiction of the uterine artery (Fig 1). The examination consisted of interleaved tag-on and tag-off scans resulting in tag-on/off subtraction images. The subtraction images were then reconstructed for minimum intensity projection (MinIP) on the MRI console. The acquisition time for non-contrast MRI alone was about 3e4 min depending on the pulse wave rate. The analysis time was about 15 min per participant.
Figure 1 A non-selective inversion-recovery pulse was placed followed by a second tag with 6 cm thickness, which covers the abdominal aorta in a coronal plane. The imaging area was set up to cover the whole cervix.
Data analysis Quantitative evaluation The signal intensity of the uterine artery was evaluated by manually placing the region of interest (ROI) on the uterine artery at the level of the parametrium for the subtraction image and on the internal iliac artery for the tag-on image (Fig 2). The ROI was placed by one of the authors with 5 years of experience in the diagnosis of gynaecological MRI. When the uterine artery was not detected at the level of the parametrium, the signal intensity was regarded as zero. The signal of the uterine artery obtained on the
Figure 2 The yellow circle shows the ROI, which was placed manually on the uterine artery at the level of the parametrium on the subtraction image. Bidirectional arrows represent the score of the tip of the uterine artery.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
subtraction image (SI uteA) was normalized by dividing it by the signal intensity of the internal iliac artery (SI iilA) obtained on the tag-on image. Thus, the relative signal intensity of the uterine artery was calculated as follows: Relative signal intensity of uterine artery (RSI uteA) ¼ SI uteA/SI iilA. The background signal was also measured. A representative background signal was determined from the absolute value (AbSI intestines) and the standard deviation of the signals of the intestines (SD intestines) in the area comprised between the bilateral internal iliac arteries on the subtraction image. Although the signals of both the intestines and the bladder can cause background noise, intestinal noise was the focus because the intestines have a larger overlap of the uterine arteries. The ROIs were placed on the section where the intestines were best visible and drawn to include as large a region of the intestines as possible.
Qualitative evaluation The non-contrast-MRA images were visually evaluated by two independent radiologists with 16 (reader A) and 5 (reader B) years of experience in female pelvic MRI. The reading radiologists evaluated the images with note of the imaging parameters. For evaluation of the uterine artery, the depiction of the uterine artery was scored on a five-point scale according to the location of the tip of the artery detected on the subtraction image. Anatomically, the uterine artery descends on the lateral wall of the pelvis, anterior to the internal iliac artery, and enters the root of the broad ligament. Here it passes medially to reach the lateral margin of the uterus immediately superior to the lateral part of the fornix of the vagina. For visual evaluation, the uterine artery was thus divided into five parts, as follows (Fig 2): the tip is (1) located in the proximal half beside the pelvic wall; (2) located in the distal half beside the pelvic wall; (3) located in the proximal half within the parametrium; (4) located in the distal half within the parametrium; or (5) within the uterine myometrium. The background signal was scored on a three-point scale (1, too much noise for diagnostic quality; 2, sufficiently little noise for diagnosis; 3, almost no noise) using the MinIP image of uterine arteries. Evaluation of the overall visualization quality was done using the MinIP image of the uterine arteries on a four-point scale (1, not visible and non-diagnostic image quality; 2, poor image quality and insufficient visualization; 3, good image quality sufficient for diagnosis; 4, excellent image quality with sharply defined uterine arteries).
Statistical analysis Statistical analyses were performed using a commercially available software package (Medcalc version 12.3.0, MedCalc Software, Ostend, Belgium). The relative signal intensity of the uterine artery, and the absolute value and the standard deviation of the signal intensity of the intestines were evaluated using one-way repeated-measures analysis of variance (ANOVA) followed by Bonferroni
3
correction for multiple comparisons. The relative signal intensities of the uterine arteries between the right and left sides were compared using paired Student’s t-test. The qualitative results of the different protocol groups were compared using Friedman’s non-parametric test. A p-value of less than 0.05 was considered significant. Interobserver variability was assessed by weighted kappa statistics.6
Results MRI was successfully performed in all volunteers. Two of the participants had fibroids (major axes were 1 and 3 cm), whereas the MRI appearance of the uterus was normal in the other volunteers.
Quantitative analysis The mean values and standard deviations of the RSI uteA on each side, AbSI intestines, and SD intestines are summarized in Fig 3. There was no significant difference between the right and the left RSI ute A (p ¼ 0.06). The highest RSI uteA value was obtained with a TI of 1400 ms for the right uterine artery, while a TI of 1600 ms was associated with the highest RSI uteA for the left uterine artery. On both sides, imaging using a TI of 1200 ms was associated with the lowest RSI. Significant differences were noted between TIs of 1200 and 1400 ms on both sides (p ¼ 0.0017 for the right, p ¼ 0.0004 for the left) and also between TIs of 1200 and 1600 ms on the left side (p ¼ 0.0005). There was no significant difference among TIs of 1400, 1600, and 1800 ms. Both AbSI intestines and SD intestines were the lowest at a TI of 1400 ms and the highest at a TI of 1800 ms. A significant difference was determined only between the SD intestines obtained at TI of 1400 and 1800 ms.
Qualitative analysis One example of MinIP images as well as the results of the qualitative evaluation performed by two readers are summarized in Figs 4 and 5. For both readers, the tip of the uterine artery was detected most distally at a TI of 1400 or 1600 ms, and most proximally at a TI of 1200 ms. The evaluation of the images at TIs of 1400, 1600, and 1800 ms were significantly higher than 1200 ms, except those at a TI of 1800 ms on the right side of the reader A (p < 0.05). Minimization of the background noise was best achieved at a TI of 1400 ms and least at a TI of 1800 ms for both readers. Significant differences were noted between TIs of 1800 and 1400 ms, and also between TIs of 1800 and 1600 ms (p < 0.05) for both readers. The overall visualization quality was highest at a TI of 1400 ms for reader A and 1600 ms for reader B, and was lowest at a TI of 1200 ms for both readers. The overall quality at both TIs of 1400 and 1600 ms was significantly higher compared with those obtained at TIs of 1200 and 1800 ms (p < 0.05). There was no significant difference between TIs of 1400 and 1600 ms.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
4
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
Figure 3 Quantitative evaluation of uterine arteries at various TIs. (a) Relative signal intensity of the right uterine arteries (right RSI uteA); (b) relative signal intensity of the left uterine arteries (left RSI uteA); (c) absolute value of the signal of the intestines (AbSI intestines); and (d) standard deviation of the signal of the intestines (SD intestines). Asterisks indicate the value pairs where significant differences were determined.
Weighted k for the assessment of the tip of the right uterine artery, left uterine artery, background signal, and overall visualization quality were scored 0.73, 0.70, 0.76, and 0.68, respectively. All the agreements were substantial.
Discussion The present study showed that Time-SLIP enables the selective visualization of uterine arteries. The poorest depiction of the uterine arteries at a TI of 1200 ms both in
the quantitative and qualitative evaluations was probably due to insufficient time for the arterial blood to enter the image acquisition area. Background signal was best suppressed at a TI of 1400 ms, and least at a TI of 1800 ms in both the quantitative and qualitative analyses. That might suggest that most of the background signal observed on the MinIP image was signal caused by intestinal movements and the null point of the intestines is around a TI of 1400 ms on average. As a result, the most amount of background signal recovery was observed at a TI of 1800 ms.
Figure 4 MinIP images of a 26-year-old participant. The images at (a) a TI of 1200 ms, (b) a TI of 1400 ms, (c) a TI of 1600 ms, and (d) a TI of 1800 ms are shown. The tip of the uterine artery was depicted most distally at a TI of 1400 or 1600 ms, and most proximally at a TI of 1200 ms. The background suppression was best achieved at a TI of 1400 ms and was poorest at a TI of 1800 ms. Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018
K. Kiguchi et al. / Clinical Radiology xxx (2014) 1e5
5
Figure 5 Qualitative analysis by the readers. (a) Location of the tip of the uterine artery was scored (b) scores of background suppression, and (c) scores of overall image quality. Asterisks indicate the value pairs where significant differences were determined by both readers for both sides in (a), and by both readers in (b) and (c).
The results of the overall image quality correspond to the results mentioned above. That is, the uterine artery depiction was insufficient at a TI of 1200 ms, whereas the background suppression was unsatisfactory at a TI of 1800 ms. A limitation of the present study is that comparison with well-established contrast-enhanced MRA or commonly used time-of-flight (TOF) MRA was not undertaken. In the authors’ experience, the proximal uterine artery was visualized using TOF within approximately 2 min, which was shorter than that of Time-SLIP. However, both the visualization and acquisition time of uterine arteries should be compared under the same conditions between the two sequences for a conclusive comparison. A comparative study with TOF or contrastenhanced MRA should be undertaken in future studies. In conclusion, this report showed that the combination of the 3D bSSFP sequence with Time-SLIP technique enables selective MRA of the uterine artery. The optimal TI for visualizing the uterine artery may be between 1400 and 1600 ms.
Acknowledgements The authors thank Mr Naotaka Sakashita (Toshiba Medical Systems Corporation) and Mr Hajime Sagawa, RT, for
technical assistance. This study was supported by a sponsored research programme, “ Research for improvement of MR visualization (no. 150100700014)” provided to one of the authors, K.T., by Toshiba Medical Systems Incorporated, Japan.
References 1. Marckmann P, Skov L, Rossen K, et al. Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J Am Soc Nephrol 2006;17:2359e62. 2. Miyazaki M, Lee VS. Nonenhanced MR angiography. Radiology 2008;248:20e43. 3. Shimada K, Isoda H, Okada T, et al. Non-contrast-enhanced hepatic MR angiography with true steady-state free-precession and time spatial labeling inversion pulse: optimization of the technique and preliminary results. Eur J Radiol 2009;70:111e7. 4. Shonai T, Takahashi T, Ikeguchi H, et al. Improved arterial visibility using short-tau inversion-recovery (STIR) fat suppression in non-contrastenhanced time-spatial labeling inversion pulse (Time-SLIP) renal MR angiography (MRA). J Magn Reson Imaging 2009;29:1471e7. 5. Garcia DM, Duhamel G, Alsop DC. Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 2005;54:366e72. 6. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159e74.
Please cite this article in press as: Kiguchi K, et al., Non-contrast-enhanced MR angiography of uterine arteries with balanced steady-state free precession and time-space labelling inversion pulse: Technical optimization and preliminary results, Clinical Radiology (2014), http:// dx.doi.org/10.1016/j.crad.2014.01.018