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AJR 2001; 176:913-918
© American Roentgen Ray Society


Ability of MR Cholangiography to Reveal Stent Position and Luminal Diameter in Patients with Biliary Endoprostheses

In Vitro Measurements and In Vivo Results in 30 Patients

Elmar M. Merkle1, Daniel T. Boll1, Hans Weidenbach2, Hans-Jürgen Brambs1 and Andreas Gabelmann1

1 Department of Radiology, University Hospitals of Ulm, Robert Koch Str. 8, 89081 Ulm, Germany.
2 Department of Internal Medicine I, University Hospitals of Ulm, 89081 Ulm, Germany.

Received June 26, 2000; accepted after revision September 28, 2000.

 
Address correspondence to E. M. Merkle.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Our goal was to evaluate the ability of MR cholangiography to show stent position and luminal diameter in patients with biliary endoprostheses.

MATERIALS AND METHODS. Susceptibility artifacts were evaluated in vitro in three different stent systems (cobalt alloy—based, nitinol-based, and polyethylene) using two breath-hold sequences (rapid acquisition with relaxation enhancement, half-Fourier acquisition single-shot turbo spin echo) on a 1.5-T MR imaging system. The size of the stent-related artifact was measured, and the relative stent lumen was calculated. In vivo stent position and patency were determined in 30 patients (10 cobalt alloy—based stents, five nitinol-based stents, and 15 polyethylene stents).

RESULTS. In vitro, the susceptibility artifact of the cobalt stent caused complete obliteration of the stent lumen. The relative stent lumens of the nitinol-based and polyethylene stents were 38-50% and 67-100%, respectively. In vivo, all stents were patent at the time of imaging. The position of the cobalt alloy—based stent could be determined in nine of 10 patients, but stent patency could not be evaluated. Stent position of nitinol stents could not be adequately evaluated in any of the five patients, and internal stent diameter could be visualized in only one patient. In nine of 15 patients, the fluid column within the implanted polyethylene stent was seen on MR cholangiography.

CONCLUSION. The internal stent lumen could be visualized in most patients with an indwelling polyethylene stent, but not in patients with cobalt alloy— or nitinol-based stents.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
During the past 10 years, MR cholangiography together with percutaneous sonography has gained general acceptance as the imaging method of choice for evaluation of diseases of the biliary system. This technique has replaced endoscopic retrograde cholangiography, particularly in those patients in whom an interventional approach seems unlikely at the outset [1]. The main applications of endoscopic retrograde cholangiography tend to be more therapeutic than diagnostic, including extracting bile duct calculi, obtaining biopsy material and, increasingly, for implanting temporary or permanent stents [2,3,4]. Literature reports concerning the role of MR cholangiography in monitoring patient progress after stent implantation are primarily case reports [5]. We sought to determine the potential of MR cholangiography for evaluating the biliary tracts of patients with biliary endoprostheses by measuring luminal stent diameter and stent position.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
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All MR imaging studies were performed using a closed 1.5-T high-field MR imaging system (Vision; Siemens, Erlangen, Germany).

Our first step consisted of determining in vitro the artifact behavior of the three biliary endoprostheses most commonly used in our hospital: Easy Wallstent (cobalt alloy-based; diameter, 8 mm) (Schneider, Buelach, Switzerland); Smart Stent (nitinol wire; diameter, 8 mm) (Cordis, Miami, FL); and the 11.5-French Cotton-Huibregtse biliary stent (polyethylene; diameter, 2.7 mm) (Cook, Moenchengladbach, Germany). Stents were first filled with water through a tube system and then immersed in a copper sulfate solution that exhibits an MR signal intensity equivalent to fat. For imaging, the plastic tubes containing the stents were positioned in the center of the bore parallel to the main magnetic field B0.

The in vitro imaging protocol consisted of the following sequences: multislice HASTE (half-Fourier acquisition single-shot turbo spin echo) (TR/TE, 1.9/95; acquisition time, 9 sec; in-plane resolution, 1 mm; slice thickness, 3 mm; scan orientation, perpendicular to the long stent axis); single-slice RARE (rapid acquisition with relaxation enhancement) (2800/1000; acquisition time, 7 sec; in-plane resolution, 1 mm; slice thickness, 50 mm; scan orientation, parallel to the long stent axis with frequency-encoding axis parallel to the stent axis); multislice HASTE (1.9/95; acquisition time, 9 sec; in-plane resolution, 1 mm; slice thickness, 3 and 5 mm; scan orientation, parallel to the long stent axis with frequency-encoding axis parallel to the stent axis); and multislice HASTE (1.9/95; acquisition time, 9 sec; in-plane resolution, 1 mm; slice thickness, 3 and 5 mm; scan orientation, parallel to the long stent axis with frequency-encoding axis perpendicular to the stent axis).

Whole-body transmit coils incorporated into the scanner were used for radiofrequency transmission, and a circular polarized body array coil was used for signal reception. Fat saturation was performed in all sequences using a chemical shift technique. Measurements of the diameter of the stent lumen were performed by a single observer and were based on signal-intensity plots drawn orthogonally to the long axis of the stent. Patent lumina were measured along histograms at half-maximum width [6]. Measurements were rounded to the nearest millimeter. The size of the stent-related artifact (signal void) was determined relative to the known diameter.

During a 9-month period, MR cholangiography was performed on 30 patients (average age ± SD, 63 ± 14 years) who had undergone implantation of a biliary endoprosthesis. After informed consent in accordance with institutional guidelines was obtained, all patients received oral administration of 600 mL of an iron-containing contrast medium (Lumirem; Guerbet, Sulzbach, Germany) to reduce interfering signals from the stomach and duodenum. Before MR cholangiography, a T2-weighted axial turbo spin-echo sequence (TR/TE, 8.2/66; acquisition time, 13 sec; slice thickness, 6 mm) was performed to localize the biliary system. The MR cholangiographic protocol consisted of the following sequences: single-slice RARE (2800/1100; acquisition time, 7 sec; in-plane resolution, 1.5 mm; slice thickness, 50 mm; chemical shift fat saturation; scan orientation, coronal and semicoronal [angulation of 20° from the coronal toward the sagittal plane clockwise and counter-clockwise]); and multislice HASTE (1.9/95; acquisition time, 11 sec; in-plane resolution, 1.5 mm; slice thickness, 3 mm; chemical shift fat saturation; scan orientation, coronal and semicoronal [angulation of 20° from the coronal toward the sagittal plane clockwise and counterclockwise]).

Underlying diseases included chronic pancreatitis (n = 6), pancreatic carcinoma (n = 5), carcinoma of the biliary tract (n = 7), hepatocellular carcinoma (n = 1), liver metastases (n = 9), and enlarged lymph nodes in the liver hilum (n = 2). Fifteen patients underwent endoscopic placement of polyethylene stents (11.5-French [n = 11], 7-French [n = 4]), whereas another 15 patients underwent percutaneous placement of a metallic stent (Easy Wallstent [n = 10]; Smart Stent [n = 5]). All stents were patent at the time of examination. Percutaneous transhepatic cholangiography or endoscopic retrograde cholangiography was performed within 48 hr of MR cholangiography and served as the gold standard.

MR cholangiographic findings regarding the diameter of the stent lumen and position were evaluated independently by two examiners. By definition, the stent lumen was considered adequately evaluated in those cases in which a "water column" could be visualized throughout the length of the stent. Stent position was evaluated as "good" (demarcated along its entire length with clear localization of the stent ends), "moderate" (stent not clearly demarcated in all its segments), or "missing." In cases in which the examiners returned divergent opinions, a consensus was reached. All other coincidental abnormal findings revealed on MR cholangiography were documented.


Results
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Results
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In vitro, the stent lumen was best visualized in the polyethylene stent, which showed no appreciable susceptibility artifact. Internal stent lumen was 2-3 mm, whereas the actual diameter was 2.7 mm. In the Smart Stent, which is composed of nitinol, in vitro measurements revealed a visualized, internal stent lumen diameter of 3-4 mm, although the actual diameter was 8 mm. In the case of the cobalt alloy—based Easy Wallstent, the entire internal stent lumen was overlain by artifacts (Fig. 1A,1B,1C). Changes in phase and frequency-encoding direction had no significant effect on the extent of the susceptibility artifacts.



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Fig. 1A. In vitro artifact behavior of three biliary endoprostheses. One asterisk = Smart Stent (Cordis, Miami, FL), two asterisks = polyethylene stent (Cook, Moenchengladbach, Germany), three asterisks = Easy Wallstent (Schneider, Buelach, Switzerland). Half-Fourier acquisition single-shot turbo spin-echo source image (TR/TE, 1.9/95; in-plane resolution, 1 mm; slice thickness, 3 mm; scan orientation, parallel to long stent axis).

 


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Fig. 1B. In vitro artifact behavior of three biliary endoprostheses. One asterisk = Smart Stent (Cordis, Miami, FL), two asterisks = polyethylene stent (Cook, Moenchengladbach, Germany), three asterisks = Easy Wallstent (Schneider, Buelach, Switzerland). Half-Fourier acquisition single-shot turbo spin-echo source image (1.9/95; in-plane resolution, 1 mm; slice thickness, 3 mm; scan orientation, perpendicular to long stent axis).

 


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Fig. 1C. In vitro artifact behavior of three biliary endoprostheses. One asterisk = Smart Stent (Cordis, Miami, FL), two asterisks = polyethylene stent (Cook, Moenchengladbach, Germany), three asterisks = Easy Wallstent (Schneider, Buelach, Switzerland). Rapid acquisition with relaxation enhancement image (2800/1000; in-plane resolution, 1 mm; slice thickness, 50 mm; scan orientation, parallel to long stent axis). Lumen of cobalt alloy—based Easy Wallstent is completely overlain with artifact formation. Relative interior lumen of the nitinol-based Smart Stent is visualized at about 50%, and relative interior lumen of polyethylene stent stands at 100%.

 

In vivo examinations of the 10 patients with Easy Wallstents failed to reveal the stent lumen in all patients. The stents themselves, however, because of their significant susceptibility artifacts, were more amenable to visualization and were rated as good in seven patients and as moderate in two others (Fig. 2A,2B,2C,2D). In one case, neither of the two sequences revealed the patient's implanted Wallstent due to motion and respiratory artifacts.



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Fig. 2A. 46-year-old woman with breast and gastric carcinoma. Percutaneous transhepatic cholangiogram shows occlusion in prepapillary segment of common bile duct (arrow).

 


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Fig. 2B. 46-year-old woman with breast and gastric carcinoma. Percutaneous transhepatic cholangiogram shows cobalt alloy—based Easy Wallstent (10-mm diameter, 70-mm length) (Schneider, Buelach, Switzerland) implanted in common bile duct.

 


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Fig. 2C. 46-year-old woman with breast and gastric carcinoma. Percutaneous transhepatic cholangiogram reveals that stent shown in B is located in transpapillary position in which distal stent end is in contact with opposite wall of duodenum and appears to perforate it (arrow).

 


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Fig. 2D. 46-year-old woman with breast and gastric carcinoma. MR cholangiogram (half-Fourier acquisition single-shot turbo spin-echo source image [TR/TE, 1.9/95; in-plane resolution, 1.5 mm; slice thickness, 3 mm]) reveals stent position, including intraduodenal position of stent end (arrow), whereas stent lumen cannot be evaluated because of artifact formation. Patient's postinterventional course was uneventful.

 

In the five patients who received nitinol stents, MR cholangiography failed to reveal the stent lumen in four patients (Figs. 3A,3B and 4A,4B,4C). Because of the low degree of the associated susceptibility artifacts, even the stent position proved difficult to visualize. MR cholangiography localized stents with a rating of moderate in only four of five patients. In one patient, neither of the two sequences revealed the patient's implanted Smart Stent.



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Fig. 3A. 62-year-old man with gastric carcinoma. Endoscopic retrograde cholangiogram shows patent lumen of nitinol-based Smart Stent (Cordis, Miami, FL).

 


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Fig. 3B. 62-year-old man with gastric carcinoma. MR cholangiogram (rapid acquisition with relaxation enhancement; TR/TE, 2800/1000; in-plane resolution, 1.5 mm; slice thickness, 50 mm) shows that lumen of Smart Stent is totally overlain by artifact formation, whereas stent itself, because of weak associated susceptibility artifact, is inadequately visualized in cranial section of image.

 


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Fig. 4A. 61-year-old man with gastric carcinoma. Radiograph shows nitinol-based Smart Stent (Cordis, Miami, FL) implanted in common bile duct (arrow).

 


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Fig. 4B. 61-year-old man with gastric carcinoma. Percutaneous transhepatic cholangiogram shows patent lumen of nitinol-based Smart Stent (arrow).

 


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Fig. 4C. 61-year-old man with gastric carcinoma. MR cholangiogram (rapid acquisition with relaxation enhancement image; TR/TE, 2800/1000; in-plane resolution, 1.5 mm; slice thickness, 50 mm) shows adequate visualization of inner lumen, whereas stent itself, because of weak susceptibility artifact, is not demarcated.

 

In the 15 patients with polyethylene stents, the lumen was clearly visualized in nine patients, although the stent itself, because of the lack of susceptibility artifacts, could not be demarcated (Fig. 5A,5B).



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Fig. 5A. 65-year-old man with chronic pancreatitis. MR cholangiogram (rapid acquisition with relaxation enhancement image; TR/TE, 2800/1000; in-plane resolution, 1.5 mm; slice thickness, 50 mm) inadequately shows patent polyethylene stent (arrows).

 


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Fig. 5B. 65-year-old man with chronic pancreatitis. Half-Fourier acquisition single-shot turbo spin-echo source image (1.9/95; in-plane resolution, 1.5 mm; slice thickness, 3 mm) permits unequivocal evaluation of interior lumen of stent (arrows).

 

In 12 of the 30 patients, MR cholangiography yielded important coincidental findings (i.e., dilatation of Wirsung's duct, pancreatic pseudocyst, cholecystolithiasis, cavernous transformation of the portal vein, pancreatic tumor, and liver tumor), which, although already known in some cases from patient histories, were not visualized on percutaneous transhepatic cholangiography or endoscopic retrograde cholangiography performed as the gold standard in the respective patients.


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
At many imaging centers, MR cholangiography has essentially replaced both IV cholangiography and endoscopic retrograde cholangiography as the imaging method of choice for visualization of the biliary tract. The preference is clear, based on the fact that MR cholangiography is noninvasive, does not subject the patient to radiation exposure, and does not require IV contrast medium. Although IV cholangiography has thus become obsolete, endoscopic retrograde cholangiography remains indicated primarily in the interventional field in which, aside from stone extraction and harvesting biopsy material for cytology and chemical analysis, its use for endoscopic stent implantation has increased in importance. This includes temporary polyethylene stents placed in the common bile duct and permanent metallic stents placed endoscopically in the bile duct system. These endoprostheses require regular follow-up because, in cases of malignancy-related stenoses, they may become occluded by tumor growth, whereas their lumina are subject to sludge incrustation that threatens their patency regardless of the patient's diagnosis.

A further problem is that of stent dislocation [7]. Although percutaneous sonography offers a simple, cost-effective, and noninvasive method for evaluating the intrahepatic biliary tract, the ability of this method to show extrahepatic biliary structures is significantly less than that of MR cholangiography [8]. The capabilities of sonography are further diminished because of its difficulty in penetrating the stent cage—a problem that complicates assessment of the vascular lumen and the vessel wall—and the quality of the examination is operator-dependent [6, 8, 9]. In such cases, endoscopic retrograde cholangiography remains the method of choice because this modality also offers the option of performing interventional procedures during the same session. However, because patients with biliary tract abnormalities are often multimorbid, a noninvasive imaging technique free of potential complications would be desirable in light of the other concomitant risk factors.

There are many reasons why MR cholangiography is not used more frequently in patients with biliary stents. The image quality of MR cholangiography is often severely compromised by susceptibility artifacts associated with the stent. In addition, aside from the composition of the stent alloy, other factors, such as the magnetic field strength B0, the orientation of the stent in relation to the magnetic field, and the individual sequence parameters of sequence type and echo time, must be taken into consideration [10,11,12,13]. In addition, the internal stent mesh structure may cause signal deflection from the interior lumen (Melzer et al., presented at the International Meeting of the Society of Magnetic Resonance in Medicine, April 2000). Furthermore, particularly in patients with indwelling metallic stents, there are certain safety issues to consider, such as the potential movement or dislodging of the stent by magnetic field interactions and the heating of the endoprosthesis by radiofrequency power deposition [14]. However, because stents are increasingly manufactured with MR-compatible materials, even MR imaging—guided percutaneous or endoscopic stent implantation is increasingly possible. Wacker et al. [15] performed percutaneous transhepatic cholangiography without complication in an animal model using a 0.2-T low-field MR imaging system for guidance; Wacker et al. then confirmed these positive findings in three patients (presented at the third international meeting of the Society for Magnetic Resonance in Medicine, April 2000). Also, MR-compatible, custom-made endoscopes have recently become available [16].

Our in vitro results show that even with the current state-of-the-art breath-hold MR cholangiographic sequences (RARE and HASTE), only with the polyethylene stent is it possible to routinely visualize the inner lumen to an adequate degree for evaluation (Fig. 1A,1B,1C). Only with this stent type could MR cholangiography consistently correctly show the inner lumen of the stent independent of the sequence type and the direction of the frequency-encoding axis.

In imaging the nitinol-based Smart Stent, MR cholangiography revealed the inner stent lumina to be in the range of 3-4 mm, which represents a relative inner lumen of 38-50% of the actual known stent lumen. Because the difference of 1 mm corresponds to one pixel at this imaging level, the difference is probably most accurately described as a measurement inaccuracy. The inner lumen of the cobalt alloy—based Easy Wallstent could not be evaluated during breath-hold MR cholangiography sequences; the relative interior stent lumen was 0% at all measurements.

To our knowledge, there are no published reports in the literature describing the in vitro artifact behavior of biliary stents in routine MR cholangiographic sequences. This subject is, however, drawing increased attention in the field of MR angiography as the development of fast three-dimensional gradient-echo sequences, the availability of specific surface coils, and the bolus-triggered application of contrast medium have combined to permit a satisfactory visualization of both the arterial and venous vascular systems. Baum et al. [17] found that using a three-dimensional fast imaging with steady-state precession (FISP) sequence with an effective slice thickness of 1.3 mm (anterior-to-posterior, 80 mm, 60 partitions, scan orientation parallel to the long stent axis), the size of the relative stent lumen can vary from 0% to 100% depending on the composition of the stent alloy and its design. These findings were confirmed by Buecker et al. (ISMRM meeting, April 2000) who, using a similar sequence, reported relative stent lumina of 0-55%. In addition, the same group was able to show that the extent of susceptibility artifacts depends on the orientation of the stent in relation to the magnetic field B0, which had previously been shown only for MR imaging—compatible biopsy needles [10]. This point may, however, be primarily of theoretic interest, because in vivo stent position is determined by the course of the vessel, whereas the patient's positioning in a closed, high-field system permits only minimal adaptation.

Using a three-dimensional gradient-recalled echo sequence, Hilfiker et al. [6] were able to see the interior lumen of the nitinol-based Cragg (Mintec, Freeport, Bahamas) stent with a relative stent lumen of approximately 80%. One reason for the difference between our results and theirs may be differences in the design of the nitinol-based Smart Stent, although the more probable explanation may be the short TE of the three-dimensional gradient-recalled echo sequence (approximately 2 msec), because the extent of the susceptibility artifact increases with TE [11, 13]. Corresponding to our data, the relative interior lumen of the cobalt alloy—based Easy Wallstent stood at 0% in the MR angiographic measurements reported by Hilfiker et al. As expected, in vivo localization was most reliable with the Easy Wallstent (Fig. 2A,2B,2C,2D), for which the associated susceptibility artifacts are sufficiently large. The artifact formation is, however, not large enough to compromise the evaluation of the stent surroundings (i.e., the portal region and the pancreatic head). This confirms the findings of Girard et al. [18] who performed MR imaging using mid-field systems in eight patients with indwelling biliary Wallstents and reported that visualization of adjacent structures was not influenced by any significant artifact overlay when spin-echo sequences were used. The signal of the interior lumen of the Easy Wallstent is, however, totally obliterated; hence, no evaluation with regard to sludge incrustation or tumor infiltration is possible using this stent system.

Because of the lesser extent of the associated susceptibility artifact, evaluation of the interior lumen of the nitinol-based Smart Stent should theoretically be possible. However, this was not confirmed in four of the five patients we examined; demarcation of the stent itself was only partially possible because the extent of artifact was not sufficiently large (Figs. 3A,3B and 4A,4B,4C).

Our best results were obtained in patients with indwelling polyethylene stents. The interior stent lumen was adequately visualized in nine of 15 patients (Fig. 5A,5B). The stent itself, because of the general lack of susceptibility artifact, was predictably not delineated.

Whether using MR cholangiography in patients with biliary endoprostheses may offer superior results using mid- or low-field MR imaging scanners, because of the lesser extent of associated susceptibility artifact formation, remains to be addressed in future studies [19, 20]. A totally new concept is being studied by Melzer et al. (ISMRM meeting, April 2000), who have developed a new type of stent with integrated capacity and conductivity adjusted and tuned as a resonance circuit to the frequency of the MR imaging system.

In conclusion, the internal stent lumen may be visualized only in those patients who have an indwelling polyethylene stent. Although MR cholangiography can reveal at least the position of a cobalt alloy—based stent, our findings suggest that MR cholangiography cannot show either the exact position or the internal lumen diameter of nitinol stents. However, MR cholangiography in patients with biliary stents is a safe and effective imaging technique that can provide valuable information. When there are positive findings, the use of MR cholangiography may often spare a severely ill patient from having to undergo an invasive procedure such as endoscopic retrograde cholangiography. We must emphasize that only a limited number of biliary stents have been evaluated in our study, and thus, the results are not applicable to all types of biliary stents.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

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