Oral Radiol (2010) 26:9–15 DOI 10.1007/s11282-010-0036-7
ORIGINAL ARTICLE
Optimum conditions for detecting the inferior alveolar artery using phase-contrast magnetic resonance angiography Junichiro Sakamoto • Takuo Higaki • Sota Okamoto Takashi Kamio • Mika Otonari-Yamamoto • Keiichi Nishikawa • Tsukasa Sano
•
Received: 25 January 2010 / Accepted: 26 February 2010 / Published online: 31 March 2010 Ó Japanese Society for Oral and Maxillofacial Radiology and Springer 2010
Abstract Objectives The inferior alveolar artery (IAA), accompanied by the inferior alveolar nerve, runs through the mandibular canal. The mandibular canal can be observed by conventional radiography and computed tomography, although it is sometimes difficult to identify on these images. This study examined visualization of the IAA with phasecontrast magnetic resonance angiography (PC-MRA). Methods Phase-contrast magnetic resonance angiography images were obtained in the double oblique sagittal plane by using a two-dimensional, fast, low-angle shot (2D FLASH) sequence in five healthy volunteers. A flowencoding gradient was applied from anterior to posterior, with velocity-encoding numbers (VENCs) of 10, 8, 6, 4, 2, and 1 cm/s. Two observers subjectively evaluated the detectability of the IAA in three mandibular regions on all PC-MRA images. Results The IAA appeared as a line of high signal intensity on the PC-MRA images. In the mandibular ramus region, the rating scores at VENCs of 1 and 2 cm/s were significantly higher than those at VENCs of 8 and 10 cm/s (p \ 0.05). In the molar region, the scores at a VENC of J. Sakamoto (&) T. Kamio M. Otonari-Yamamoto K. Nishikawa T. Sano Department of Oral and Maxillofacial Radiology, Tokyo Dental College, 1-2-2 Masago, Mihama-ku, Chiba 261-8502, Japan e-mail:
[email protected] T. Higaki Chiba Hospital, Tokyo Dental College, 1-2-2 Masago, Mihama-ku, Chiba 261-8502, Japan S. Okamoto Department of Oral and Maxillofacial Surgery, Tokyo Metropolitan Tama Medical Center, 2-8-29 Musashidai, Fuchu, Tokyo 183-8524, Japan
1 cm/s were significantly higher than those at VENCs of 8 and 10 cm/s (p \ 0.05). However, in the premolar region, there was no significant difference among the VENCs (p = 0.0843), with scores of 0 (poor) or 1 (fair). Conclusions The IAA was visualized by using PC-MRA at appropriate VENC settings. The optimal condition for detecting the IAA appeared to be at a VENC of 1 cm/s, although the IAA was still not visible in the premolar region. Keywords Magnetic resonance imaging MR angiography Phase-contrast MRA Inferior alveolar artery Mandible
Introduction The inferior alveolar artery (IAA), accompanied by the inferior alveolar nerve (IAN), runs through the mandibular canal [1]. The mandibular canal can be observed by conventional radiography and computed tomography (CT), although it is sometimes difficult to identify the mandibular canal on radiographic images and even on CT [2, 3]. Magnetic resonance images enable the IAA and IAN to be visualized directly as the neurovascular bundle. Several studies have investigated the ability of MR imaging (MRI) to show this [2–5]. Magnetic resonance angiography (MRA) is commonly applied to evaluate intracranial vascular and cervical carotid artery disease [6–12]. Vessels appear on MRA without the use of enhancing materials. According to the imaging principle used, MRA can be classified into phase-contrast MRA (PC-MRA) and time-of-flight MRA (TOF-MRA). PC-MRA has excellent background suppression, allows variable velocity encoding, and provides directional flow
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Fig. 1 The maxillofacial fourchannel surface coil. a Front view, b three-quarters view
information [6–9, 12]. TOF-MRA is susceptible to saturation effects, and substances with short T1 may simulate flow [6, 7, 10–12]. Time-of-flight MRA is applied mainly to clinical diagnosis because of the advantages of its relative insensitivity to magnetic field inhomogeneities and the short acquisition time. However, this technique has the disadvantages of insensitivity to low flow rates and flow parallel to the slice plane. By contrast, PC-MRA can be sensitive to slow flow and flow parallel to the slice plane. The direction of blood flow in the IAA is parallel to the axial and sagittal planes of the body, and these flow rates may be low [4]. Therefore, we hypothesized that the IAA in the mandible could be visualized more clearly with PC-MRA than with TOFMRA. No studies have applied PC-MRA to the IAA in the mandible. This study examined visualization of the IAA by using PC-MRA.
(FOV) of 113 9 150 mm, matrix size of 384 9 512, section thickness of 5 mm, and internal section gap of 0.5 mm. In this study, T1-weighted spin echo sequences with fat suppression were used to clearly visualize the neurovascular bundle as a narrow high-signal-intensity line. The repetition and echo times were set at 500 and 15 ms, respectively. No image distortion due to metallic dental material was seen on the localizer images in any volunteer. Phase-contrast magnetic resonance angiography images were obtained in the double oblique sagittal plane [13] by using a two-dimensional, fast, low-angle shot (2D FLASH) sequence, with a FOV of 113 9 150 mm, matrix size of 384 9 512, and section thickness of 5 mm at the section where the maximum length of the neurovascular bundle
Patients and methods Patients Five healthy volunteers underwent MRI, including PCMRA. The volunteers were four men and one woman with a mean age of 31.8 years (range 26–38 years). The study protocol was approved by our institutional review board, and informed consent was obtained from all of the volunteers. MRI techniques A 1.5-Tesla MR unit (Magnetom Symphony Maestro Class; Siemens, Erlangen, Germany) and a maxillofacial four-channel surface coil developed by our department were used to obtain all MR images (Fig. 1). The horseshoeshaped surface coil was used to increase the signal-to-noise ratio and spatial resolution. It was fixed on the maxillofacial region with a band. Before PC-MRA, localizer images were obtained in the axial and oblique sagittal planes, with a field of view
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Fig. 2 A schematic lateral oblique view showing the mandible neurovascular bundle divided into three areas (mandibular ramus, molar, and premolar) by lines a and b. Line a was in contact with the distal surface of the second molar. Line b was in contact with both the medial surface of the first molar and distal surface of the second premolar
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Fig. 3 IAA on the left side in a 35-year-old man. a A normal neurovascular bundle is seen on the T1-weighted image with fat suppression (arrowheads). PCMRA images at VENCs of 1 (b), 2 (c), 4 (d), 6 (e), 8 (f), and 10 (g) cm/s. The inferior alveolar arteries are seen as regions of high signal intensity on the PC-MRA images at all VENCs (arrowheads). On the image at a VENC of 4 cm/s (d), one observer scored the detectability of the IAA as 2 (good) in the premolar region, 4 (excellent) in the molar region, and 2 (good) in the mandibular ramus region; the other observer gave scores of 4, 4, and 3 (very good), respectively
was seen on the T1-weighted image. The repetition time, echo time, and flip angle were set at 42–74 ms, 8–24 ms, and 15°, respectively. The 5-mm slice thickness was selected because of the increasing signal-to-noise ratio, so as to show as much of the IAA as possible in one slice and reduce the scan time. Phase-contrast magnetic resonance angiography is most sensitive to the specific flow direction and velocity, which
are determined using the imaging parameters for a flowencoding gradient [6, 9, 12]. The flow direction is specified with the applied direction of the gradient. The flow velocity is specified with the amplitude of the gradient, which is set as a velocity-encoding number (VENC). In this study, a flow-encoding gradient was applied from the anterior to posterior direction with VENCs of 10, 8, 6, 4, 2, and 1 cm/s.
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Fig. 4 IAA on the left side in a 26-year-old man. a A normal neurovascular bundle is seen on the T1-weighted image with fat suppression (arrowheads). PCMRA images at VENCs of 1 (b), 2 (c), 4 (d), 6 (e), 8 (f), and 10 (g) cm/s. The inferior alveolar arteries are indicated on the PC-MRA images (arrowheads). In the premolar region, the IAA was not detected at a VENC of 4 cm/s or higher
Image quality evaluation Magnitude images were reconstructed and used for image analysis (hereafter, PC-MRA images refer to the reconstructed magnitude images).
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Two observers subjectively evaluated the detectability of the IAA in three areas of the mandible (mandibular ramus, molar, and premolar) on all PC-MRA images (Fig. 2). The observers scored the detectability on a fivepoint rating scale: 0, poor; 1, fair; 2, good; 3, very good;
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Table 1 Results of the imaging analysis in the premolar region 5-Point rating scale
VENC (cm/s) 1
2
4
6
8
10
0 (poor)
9
8
8
7
10
10
1 (fair)
1
2
0
3
0
0
2 (good)
0
0
1
0
0
0
3 (very good)
0
0
1
0
0
0
4 (excellent)
0
0
0
0
0
0
Median
0.00
0.00
0.00
0.00
0.00
0.00
each VENC and each region. A p value less than 0.05 was considered to indicate a significant difference. Analyses were performed with the statistical software package ‘‘R’’ for Macintosh, version 2.9.2 [14].
Results
The rating score at a VENC of 1 cm/s was significantly higher than that at a VENC of 8 or 10 cm/s
Phase-contrast magnetic resonance angiography images were obtained from all volunteers. The IAA was seen as a line of high signal intensity on the PC-MRA images. On the PC-MRA images at VENCs of 6 cm/s and higher, background noise from peripheral stationary tissues was suppressed. By contrast, at VENCs of 4 cm/s and lower, significant background noise appeared on the images. Representative cases are shown in Figs. 3 and 4. The results of the subjective evaluation of image quality are shown in Tables 1, 2, and 3. The distributions of the rating scores for the detectability of the IAA in each region are shown in Fig. 5. In the mandibular ramus region, the rating scores at VENCs of 1 and 2 cm/s were significantly higher than those at VENCs of 8 and 10 cm/s (p \ 0.05). In the molar region, the scores at a VENC of 1 cm/s were significantly higher than those at VENCs of 8 and 10 cm/s (p \ 0.05). By contrast, in the premolar region there was no significant difference in the scores among the VENCs (p = 8.43 9 10-2), with scores of 0 (poor) or 1 (fair).
Table 3 Results of the imaging analysis in the mandibular ramus region
Discussion
Data are numbers of scores. There were no significant differences among the VENCs Table 2 Results of the imaging analysis in the molar region 5-Point rating scale
VENC (cm/s) 1a
2
4
6
8a
10a
0 (poor)
0
1
5
5
6
6
1 (fair)
3
5
2
1
1
4
2 (good)
7
3
1
2
3
0
3 (very good)
0
1
0
0
0
0
4 (excellent)
0
0
2
2
0
0
Median
2.00
1.00
0.50
0.50
0.00
0.00
Data are numbers of scores a
5-Point rating scale
VENC (cm/s) 1a
2b
4
6
8a,b
10a,b
0 (poor)
0
0
3
5
7
8
1 (fair)
2
5
3
2
1
0
2 (good) 3 (very good)
1 6
3 1
1 1
1 1
1 1
1 1
4 (excellent)
1
1
2
1
0
0
Median
3.00
1.50
1.00
0.50
0.00
0.00
Data are numbers of scores a
The rating score at a VENC of 1 cm/s was significantly higher than that at a VENC of 8 or 10 cm/s
b
The rating score at a VENC of 2 cm/s was significantly higher than that at a VENC of 8 or 10 cm/s
and 4, excellent. The image was evaluated on a liquid crystal display in the MRI unit. Statistical analysis Friedman and multiple comparison tests were used to statistically compare differences among the rating scores at
In PC-MRA, it is important to estimate the flow velocity of the vessel in order to determine the appropriate VENC settings. From previous studies [15, 16], the flow velocity of the IAA was considered to be less than 10 cm/s. Therefore, a VENC of 10 cm/s or less was adopted in this study. In this study, a four-channel maxillofacial surface coil was used for PC-MRA imaging. This surface coil is needed to visualize narrow arteries such as the IAA, because a high signal-to-noise ratio and high spatial resolution are required. Although no comparison of the signal-to-noise ratios among MR coils, including this surface coil, was conducted, with this surface coil, PC-MRA imaging could be performed at a high resolution, such as a FOV of 113 9 150 mm and matrix size of 384 9 512 (voxel size, 0.3 9 0.3 9 5 mm). The results demonstrated that the IAA could be visualized by using PC-MRA. A VENC of less than 4 cm/s produced strong background noise from stationary peripheral tissues. This might have been be due to the small difference in the phase shift at low VENCs and the resultant small difference in signal intensity between the IAA
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Fig. 5 The distributions of the detectability ratings for the IAA in the a premolar, b molar, and c mandibular ramus regions
and peripheral stationary tissues. From the results of this prior evaluation, the IAA in the mandibular ramus and molar areas was clearly seen at a VENC of 2 or 1 cm/s. By contrast, the IAA in the premolar region of many volunteers could not be visualized at any VENC. There are two possible reasons for this. First, the internal diameter of the IAA in the premolar region is smaller than that in the other areas. Second, the winding course of the IAA to the submental foramen in the premolar area produces flow that is too slow to be detected. The PC-MRA technique used here has limitations in terms of slice thickness and imaging time. A thicker slice was required to increase the signal-to-noise ratio, as well as to delineate as much of the IAA as possible in one slice. The imaging time of PC-MRA also increased proportionally, and nearly 5 min were required to obtain one image at a VENC of 1 cm/s. A long time is required to obtain several thin-slice images. Considering these limitations, we chose a 5-mm slice thickness, which was slightly thicker than that used in previous studies [2–5, 13, 15, 17]. Ikeda et al. [2] reported that imaging of the IAN and artery with MR may help to determine the risk for injury to the nerve during tooth extraction, to diagnose neoplastic infiltration in cases of metastatic carcinoma, and to facilitate microsurgery involving the IAN. Izumi et al. [13]
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reported that the mandible was a frequent site of inflammation, primary malignant tumors, and invasion by oral cancers. They concluded that their MRA technique may be useful for diagnosing and planning treatment for these diseases. From our results, PC-MRA imaging may help to diagnose lesions adjacent to the IAA. However, our study included only five healthy volunteers. Furthermore, we do not know whether the IAA can be seen on PC-MRA images in patients in whom the mandibular canal cannot be identified on CT. Therefore, further studies are needed to modify the PC-MRA technique and develop a diagnostic system showing the relationship between lesions and the IAA. In conclusion, the IAA was visualized by using PCMRA at appropriate VENC settings. The optimal condition for detecting the IAA appeared to be at a VENC of 1 cm/s, although the IAA was still not visible in the premolar region.
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