(Radiology. 2000;214:902-907.)
© RSNA, 2000
Ligating Clips for Three-dimensional MR Angiography at 1.5 T: In Vitro Evaluation1
Dominik Weishaupt, MD,
Harald H. Quick, MSc,
Daniel Nanz, PhD,
Michaela Schmidt, RT,
Paolo C. Cassina, MD and
Jörg F. Debatin, MD
1 From the Institute of Diagnostic Radiology (D.W., H.H.Q., D.N., M.S., J.F.D.) and the Department of Surgery (P.C.C.), University Hospital Zürich, Switzerland. Received January 20, 1999; revision requested April 5; revision received June 18; accepted August 12. Address reprint requests to J.F.D., Department of Diagnostic Radiology, University Hospital Essen, Hufelandstrasse 55, D-45122 Essen, Germany (e-mail: debatin@uni-essen.de).
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Abstract
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Artifact size on three-dimensional (3D) magnetic resonance (MR) angiograms and safety of various vascular clips (15 titanium and three absorbable polydioxanone clips) were assessed. All evaluated clips were completely safe. Biodegradable clips rendered no artifacts; titanium clips were associated with susceptibility effects. Artifact size was dependent on clip size, clip orientation, echo time, and degree of k-space coverage. In the presence of titanium vascular clips, fast 3D MR angiography should be performed with the shortest echo time and full k-space coverage.
Index terms: Magnetic resonance (MR), artifact, 9*.129422 • Magnetic resonance (MR), safety, 9*.12942
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Introduction
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Magnetic resonance (MR) angiography is emerging as a credible noninvasive alternative to digital subtraction angiography for assessment of the entire arterial system including the thoracic and abdominal aorta and its branches (1–4). More recently, following the introduction of multistation three-dimensional (3D) MR angiography (5), the run-off vessels are also being targeted with this technique.
In addition to use in identification of vascular disease, contrast material–enhanced 3D MR angiography can also be used to help monitor therapeutic effectiveness following percutaneous angioplasty, stent placement (6), or arterial vein bypass grafting. To date, digital subtraction angiography and x-ray angiography are considered the standard of reference in the assessment of stenosis in infrainguinal vein bypass grafting in arteriocclusive disease of the leg. A 21% incidence of bypass graft stenosis within the first 18 postoperative months (7) mandates frequent imaging for these patients. Noninvasive contrast-enhanced 3D MR angiography would therefore be an alternative to invasive digital subtraction angiography.
The assessment of vascular grafts can be complicated by the presence of vascular clips used for either vessel ligation or tissue marking. Although most commercially available vascular clips are made of nonferrous (titanium) materials, they are associated with susceptibility artifacts of varying magnitude and appearance that may simulate graft stenosis (8). Furthermore, the integrity of the graft could potentially be endangered by torque and heating of the clips. Thus, prior to use of 3D MR angiography for assessment of graft stenosis in clinical practice, the MR compatibility of vascular clips needs to be addressed regarding safety and artifacts.
The purpose of this in vitro study was to assess various commercially available clips for magnetic-field–induced torque, radio-frequency–associated heating, and artifact size on fast 3D MR angiographic images. The effects of echo time, clip orientation within the magnetic field, and degree of k-space sampling on artifact size were evaluated.
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Materials and Methods
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Eighteen different ligating clips were evaluated. As summarized in Table 1, 15 clips consisted of chemically pure titanium metal, and three clips were made of the absorbable polymer polydioxanone (9).
Assessment of Magnetic Field Attraction
Attraction to the static magnetic field was evaluated in a manner similar to that used by Nogueira et al (10). After closure with appropriate clip pliers, all clips were placed on a plastic Petri dish with a millimeter scale etched in its underside. The long axis of the examined clip was aligned with the axis of the main magnetic field. The Petri dish was placed on the table of the MR imager 2 m from the bore of the magnet. The dish was introduced slowly into the center of the 1.5-T MR system. Displacements of the clips were quantified relative to the millimeter scale.
Assessment of Heating
Potential heating of the clips due to the deposition of radio-frequency power was assessed in a manner similar to that used by Ladd et al (11). Each metallic clip was embedded in a plastic container filled with agar gel. Since heating of small slim metallic bodies is primarily influenced by deposition of radio-frequency power, temperature measurements were collected during imaging with a radio-frequency–intensive, fast spin-echo sequence with a specific absorption rate of 1.41 W per kilogram of body weight (patient body weight, 114 kg). A fluoroptic thermometer (model 790; Luxtron, Santa Clara, Calif) was used to monitor the temperature directly at the edge surface of the clip at a rate of four measurements per second during imaging.
Assessment of Clip-associated Artifacts
All 18 clips were embedded in a plastic container filled with agar gel. To simulate the signal intensity characteristics of blood on contrast-enhanced 3D MR angiographic images, the gel was spiked with gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) in a concentration of 20 mmol/L (1:20). After closure with appropriate clip pliers, all 18 clips were embedded in the phantom with their long axis oriented parallel to the long axis of the phantom (Fig 1).
All MR imaging was performed with a 1.5-T imager (Signa Horizon LX; GE Medical Systems, Milwaukee, Wis) equipped with a fast three-axis gradient system characterized by a maximum amplitude of 40 mT/m and slew rate of 150 mT/m/msec. The phantom was placed in the center of an anteroposterior phased-array surface coil (torso array coil), which was used for signal reception. On the basis of coronal gradient-recalled localizing images, fast 3D Fourier transform spoiled gradient-recalled images were obtained. The latter sequence was performed with a bandwidth of plus or minus 62.5 kHz, a section thickness of 2 mm, and a field of view of 28 x 28 cm. The 3D data sets were collected with use of a partial-echo technique (repetition time msec/echo time msec = 5.7/1.7) and a full-echo technique (6.2/2.3). Imaging was repeated with different degrees of k-space sampling in the phase direction (0.5, 1.0, and 2.0 signals acquired). The k-space sampling along the phase-encoding direction covered 8% or more than the nominal k space in relation to full-space coverage. Homodyne reconstruction was used for images obtained with 0.5 signal acquired. Initially, the phantom was imaged with the long axis of the clips parallel to the z axis of the main magnetic field. Subsequently, the phantom was imaged again with the long axis of the clips oblique (45° angle) and perpendicular (90° angle) to the main magnetic field.
Clip-induced artifacts were quantified by measuring the area of signal intensity distortion. The latter was accomplished with use of IDL routines (Interactive Data Language; Research Systems, Boulder, Colo) implemented on a workstation (Sparc 10; Sun Microsystems, Mountain View, Calif). Signal intensity distortion was defined as signal intensity that differed from the baseline signal intensity of agar in the immediate vicinity by more than 4 SDs. Artifact area was defined as the area of signal intensity distortion minus clip area (long axis x short axis) (Fig 2). Measurements were made on the one image that contained the largest artifact area.
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Figure 2a. Three-dimensional gradient-recalled MR images depict quantification of artifact size. (a) Clip-induced susceptibility artifact. (b) The areas of signal intensity more than 4 SDs lower or higher than that of the baseline agar in the immediate vicinity of the clip are shown in white and black, respectively. The sum of the black and white areas was defined as "signal intensity distortion." Artifact size was defined as the area of signal intensity distortion minus the clip area.
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Figure 2b. Three-dimensional gradient-recalled MR images depict quantification of artifact size. (a) Clip-induced susceptibility artifact. (b) The areas of signal intensity more than 4 SDs lower or higher than that of the baseline agar in the immediate vicinity of the clip are shown in white and black, respectively. The sum of the black and white areas was defined as "signal intensity distortion." Artifact size was defined as the area of signal intensity distortion minus the clip area.
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Statistical analysis of the MR data was based on the Student t test, with a cut-off value of .05 for statistical significance.
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Results
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The in vitro MR investigation with regard to magnetic field attraction revealed no detectable displacement of the clips during the Petri dish evaluation.
Simultaneous measurement of the temperature during imaging with a radio-frequency–intense imaging sequence revealed no measurable heating of the clips.
The three evaluated biocompatible clips were not associated with any signal intensity distortions on any of the evaluated images, regardless of echo time, degree of k-space coverage, or clip orientation within the magnetic field. On the other hand, all 15 metallic titanium clips induced susceptibility artifacts on all images. As evidenced by a correlation coefficient of 0.96, the degree of signal intensity distortion associated with the titanium clips on the 3D gradient-recalled images was directly dependent on clip length (Fig 3). Clips with a long axis greater than 6 mm (n = 7) were associated with larger areas of signal intensity distortion than were clips less than 6 mm long, independent of k-space sampling and echo time (P values from .003 to .02).
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Figure 3. Graph depicts excellent correlation between clip length and artifact size on the basis of images obtained with 1.0 signal acquired, with the phantom positioned at a 45° angle to the main magnetic field.
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All three evaluated variables—clip orientation within the magnetic field, echo time, and degree of k-space coverage—had a measurable influence on artifact size (Table 2, Fig 4). The most pronounced artifacts for all 15 metallic clips, which averaged an area of 97.6 mm2, were associated with an imaging position perpendicular to the main magnetic field in conjunction with partial-k-space sampling and a long echo time.
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Figure 4a. Dependence of artifact size on the clip orientation within the main magnetic field. (a-c) Three-dimensional gradient-recalled MR images (5.7/1.7, flip angle of 30°, 0.5 signal acquired) illustrate embedded clips. The phantom is positioned parallel to the main magnetic field in a, at a 45° angle in b, and perpendicular in c. The size of the artifact for titanium clips 1-15 (top five rows) depends on the orientation of the phantom to the main magnetic field. Biocompatible clips 16-18 (bottom row) caused no artifacts. Scale of ruler is centimeters.
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Figure 4b. Dependence of artifact size on the clip orientation within the main magnetic field. (a-c) Three-dimensional gradient-recalled MR images (5.7/1.7, flip angle of 30°, 0.5 signal acquired) illustrate embedded clips. The phantom is positioned parallel to the main magnetic field in a, at a 45° angle in b, and perpendicular in c. The size of the artifact for titanium clips 1-15 (top five rows) depends on the orientation of the phantom to the main magnetic field. Biocompatible clips 16-18 (bottom row) caused no artifacts. Scale of ruler is centimeters.
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Figure 4c. Dependence of artifact size on the clip orientation within the main magnetic field. (a-c) Three-dimensional gradient-recalled MR images (5.7/1.7, flip angle of 30°, 0.5 signal acquired) illustrate embedded clips. The phantom is positioned parallel to the main magnetic field in a, at a 45° angle in b, and perpendicular in c. The size of the artifact for titanium clips 1-15 (top five rows) depends on the orientation of the phantom to the main magnetic field. Biocompatible clips 16-18 (bottom row) caused no artifacts. Scale of ruler is centimeters.
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With partial-k-space sampling in the phase-encoding direction, signal intensity distortions were significantly less pronounced in data sets collected with a shorter partial-echo technique than in those collected with a longer full echo (P values from less than .001 to .003). Partial k-space sampling (0.5 signals acquired) was associated with significantly larger artifacts (P values from less than .001 to .006) than was full k-space sampling (1.0 or 2.0 signals acquired) for all three phantom positions (Fig 5). Differences in artifact size between 1.0 and 2.0 signals acquired, on the other hand, were not statistically significant regardless of whether partial- or full-echo techniques were used. The clip orientation also had a major effect on the degree of signal intensity distortion: an oblique clip axis relative to the main field yielded a less pronounced artifact compared with a perpendicular position but a more pronounced artifact compared with the parallel position. The differences between 0° and 45°, 0° and 90°, and 45° and 90° were statistically significant for all titanium clips (P values from less than .001 to .007) independent of the degree of k-space sampling and echo time, with the exception of the differences between 45° and 90° with partial echo and 0.5 and 1.0 signal acquired. The differences between these two measurements were almost statistically significant (P = .06 and .07, respectively).
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Figure 5. Dependence of artifact size on the degree of k-space sampling. Three-dimensional gradient-recalled MR image of the phantom was obtained with full-k-space coverage (1.0 signals acquired) with the clip positioned at a 45° angle to the main magnetic field. Compared with the appearance on an image obtained with 0.5 signals acquired (Fig 4b), the artifact of titanium clips 1-15 (top five rows) is smaller. Scale of ruler is centimeters.
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Discussion
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High-performance gradient systems are capable of reducing data collection times sufficiently to permit the collection of complex 3D MR angiographic image sets during the intraarterial phase after intravenous administration of extracellular paramagnetic contrast agents (1–3). Absence of ionizing radiation and use of nonnephrotoxic contrast materials (12) permit repetitive use of 3D MR angiography in patients with impaired renal function. Contrast-enhanced 3D MR angiography thus constitutes a valuable imaging method for the close follow-up frequently required following vascular bypass surgery.
The introduction of metallic conducting materials into an MR system can potentially lead to hazardous mechanical and thermal effects (13). For this reason, the metallic clips were subjected to a safety assessment. Findings in this study confirm all examined vascular clips are unequivocally safe in a high-field-strength 1.5-T MR environment. Lack of any measurable heating, even under extreme imaging conditions, supports the hypothesis that the induction of electrical currents is negligible for small implants at magnetic field strengths used clinically (14,15). The small longitudinal extension of the clips in relation to the wavelength of the radio-frequency radiation at 1.5 T impedes the build-up of resonant oscillating currents that could lead to heating (16). Similarly, findings in this study failed to document any mechanical clip motion induced by the field strength. Largely this reflects the titanium basis of the examined clips. Titanium is a biocompatible nonferromagnetic metal that is used as a base material in a large number of bioimplants, including most commercially available vascular clips. Virtually all other titanium implants are safe in the MR environment (15,17–20).
The effects of bioimplants on MR images can be grouped into two categories: displacement of water by the implant itself and artifacts created as a result of differences in magnetic susceptibility between implants and human tissue. The former is virtually negligible as it results in a signal void that corresponds to the exact size of the implant. This effect was discounted by subtracting the device size from the measured area of signal intensity distortion. On the other hand, artifacts caused by susceptibility differences are highly variable and depend on a number of different object- and imaging-related factors (21). Differences in magnetic susceptibility cause local inhomogeneities in the static magnetic field. These inhomogeneities in turn lead to geometric distortion and intravoxel dephasing. The resultant artifacts can manifest as local or regional distortions or as complete signal voids. If they are present in the vicinity of vascular structures, they can simulate the presence of a stenosis (8). This possibility can introduce a considerable degree of uncertainty in the assessment of the arterial vasculature following bypass surgery.
Size and appearance of associated signal intensity distortions are primarily related to the underlying implant material (21,22). Thus, biodegradable polydioxanone clips caused virtually no susceptibility artifacts. In contrast, all titanium-based clips were associated with typical artifacts on the spoiled 3D gradient-recalled images. The artifacts caused by the metallic clips consist of a central signal void, referred to as the black hole artifact (23), surrounded by a high-signal-intensity rim and an area of spatial distortion that extends well beyond the high-signal-intensity rim (Fig 3). The central signal void is caused by an off-resonance condition during signal acquisition (24), but the high-signal-intensity rim and the surrounding spatial distortion result from smaller variations in local magnetic field strength that lead to ill-positioned signals along the frequency-encoding direction. On the basis of this observation alone, surgeons should be encouraged to use the polydioxanone clips whenever possible.
Implant geometry also influences size and appearance of the artifacts (18,19): Longer clips caused more signal intensity distortion than did shorter clips. In fact, the presented data revealed a direct relationship between the length of the long axis of the clips and the associated artifact size (Fig 2). To minimize artifacts on follow-up MR angiograms, surgeons should be encouraged to use the shortest possible clip. Reflecting susceptibility characteristics, the artifact size is strongly dependent on the clip orientation in the main magnetic field. The most pronounced artifacts were associated with a clip orientation with the long axis perpendicular to the axis of the main magnetic field. The signal intensity distortions were less pronounced when the long axis of a clip was oriented parallel to the static field. Unfortunately, clinical reality does not permit adjustment of the clip orientation for MR imaging.
Other parameters that influence artifact size that can be adjusted relate to the circumstances of the actual imaging experiment itself. Thus, the magnitude of susceptibility effects is known to be directly proportional to the magnetic field strength (25). Since most imagers operate at a given strength, the choice of imaging parameters such as echo time and k-space coverage is a more practical means to adjust artifact size (18–20).
The magnitude of underlying susceptibility effects is also directly dependent on the echo time (24). Thus, it was not surprising that partial-echo 3D MR angiograms contained smaller clip-related artifacts than did full-echo images obtained with partial and full k-space sampling. Lengthening of the echo time enhances dephasing effects, thereby enlarging the clip-related signal voids. The very short echo time of less than 2 msec inherent in partial-echo 3D MR angiographic acquisitions limits the clip-related magnetic susceptibility artifacts associated with other sequences (21,23). Findings in a recently published clinical study of patients after endovascular treatment of abdominal aortic aneurysms support this observation (26). In addition to the echo time, artifact size was also significantly effected by the degree of k-space coverage. Partial k-space coverage is frequently used in conjunction with fast 3D MR angiographic vascular imaging to reduce imaging times or enhance spatial resolution or volume coverage. Signal averaging had no effect on the appearance of the examined clips, but imaging with 0.5 signal acquired resulted in significantly more clip-related signal intensity distortion along the phase-encoding direction. This was due to the lack of measured data and use of a different reconstruction algorithm in fractional-echo, partial k-space imaging. Hence, in the presence of metallic vascular clips, fast 3D MR angiographic data sets should be collected with partial-echo techniques, and reconstruction should be based on a complete set of k-space data.
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Footnotes
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9*. Vascular system, location unspecified. 
Abbreviation: 3D = three-dimensional
Author contributions: Guarantor of integrity of entire study, J.F.D.; study concepts, D.W., H.H.Q., D.N., J.F.D.; study design, D.W., H.H.Q., J.F.D., P.C.C.; definition of intellectual content, H.H.Q., D.N., J.F.D.; literature research, D.W.; experimental studies, D.W., H.H.Q., M.S.; data acquisition, D.W., H.H.Q., M.S.; data analysis, D.W., D.N.; statistical analysis, D.W., J.F.D.; manuscript preparation, D.W., D.N., J.F.D.; manuscript editing, D.W., J.F.D.; manuscript review, D.N., P.C.C., J.F.D.
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TOP
Abstract
Introduction
