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Published online before print March 27, 2003, 10.1148/radiol.2272012079
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(Radiology 2003;227:601-605.)
© RSNA, 2003


Technical Developments

Failing Hemodialysis Access Grafts: Evaluation of Complete Vascular Tree with 3D Contrast-enhanced MR Angiography with High Spatial Resolution: Initial Results in 10 Patients1

Kuo-Ming Han, MD, Lucien E. M. Duijm, MD, PhD, Guillaume R. P. Thelissen, MSc, Philippe W. M. Cuypers, MD, PhD, Petra Douwes-Draaijer, MD, PhD, Alexander V. Tielbeek, MD, PhD, John H. M. Wondergem, MD and Harrie C. M. van den Bosch, MD

1 From the Departments of Radiology (K.M.H., L.E.M.D., A.V.T., J.H.M.W., H.C. M.v.d.B.), Vascular Surgery (P.W.M.C.), and Nephrology (P.D.D.), Catharina Hospital, Michelangelolaan 2, 5602 ZA Eindhoven, the Netherlands; and Philips Medical Systems, Best, the Netherlands (G.R.P.T.). Received December 21 2001; revision requested February 27, 2002; final revision received August 22; accepted August 27. Address correspondence to L.E.M.D. (e-mail: l.duijm@worldonline.nl).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Ten patients with failing hemodialysis access underwent contrast material–enhanced magnetic resonance (MR) angiography within 7 days before digital subtraction angiography (DSA). MR angiography was performed at 1.5 T by using a multistation multiinjection three-dimensional technique, and contrast material was injected via intravenous cannula. In all patients, MR angiographic images displayed the complete arterial inflow tract from the subclavian artery and access proper. The complete venous outflow tract up to the superior caval vein could be evaluated in all but one patient. DSA showed hemodynamically significant stenoses in 13 segments. MR angiography depicted all 13 stenoses and two false-positive findings, resulting in sensitivity of 100% and specificity of 94%.

© RSNA, 2003

Index terms: Dialysis shunts, 81.42 • Digital subtraction angiography, 81.1243, 81.1244, 81.42 • Grafts, stenosis or thrombosis, 81.42 • Magnetic resonance (MR), vascular studies, 81.12142, 81.12143, 81.42


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Maintenance of adequately functioning vascular access is one of the challenges of long-term hemodialysis. The development of stenoses is a major cause of graft failure, and early treatment of stenoses with percutaneous intervention as an alternative to surgery has been shown to increase the survival period of dialysis shunts (1,2). Color Doppler flow ultrasonography (US) was demonstrated to be an accurate technique for detecting, locating, and characterizing vascular complications of hemodialysis grafts (3,4). Drawbacks of this modality are the inaccuracy for detecting proximal vein stenoses and the absence of an angiographic map necessary for surgery or percutaneous therapy. Therefore, digital subtraction angiography (DSA) is usually the technique of choice for patients with malfunctioning fistulas or grafts. However, DSA is invasive and exposes the patient to ionizing radiation. Iodinated contrast material may induce hypotension and allergic reactions and may worsen renal insufficiency because of direct nephrotoxic effects (5).

In contrast, magnetic resonance (MR) angiography is noninvasive and neither ionizing radiation nor nephrotoxic contrast material are necessary. Thus far, a major problem of MR angiography has been the inability to visualize the graft in combination with its runoff vessels to the superior caval vein. Although the majority of stenoses occur at or near the venous anastomosis, more than one-third are located in the venous outflow tract of the graft (6). In addition, intravenous contrast material was not used in most MR angiographic studies, which leads to a prolonged examination time and a tendency to overestimate stenoses as a result of flow artifacts (79).

The purpose of our study was to evaluate a contrast material–enhanced MR angiographic technique for detecting graft stenoses and depicting the arterial inflow tract, graft, and complete venous runoff.


    Materials and Methods
 TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Patients
From August 2001 to November 2001, all patients seen in our dialysis department with a failing hemodialysis access were considered candidates for our study. Clinical parameters suggestive of a failing access were a gradual increase in venous pressure during hemodialysis over a period of time or increased difficulty in obtaining graft access. Written informed consent was obtained before a patient could qualify for the study. Patients with contraindications to MR angiography (eg, those who underwent pacemaker placement, heart valve surgery, or stent placement within 6 weeks before MR angiography and those with claustrophobia) and those with dementia were excluded from the study. Initially, color Doppler US was performed. MR angiography and DSA were scheduled for all patients in whom US depicted a lesion that might be suitable for percutaneous transluminal angioplasty or surgical intervention and in patients when the cause of graft failure could not be determined at US. MR angiography was performed within 7 days before DSA. The study was approved by our hospital ethical review board.

MR Angiography
All MR angiographic examinations were performed with a 1.5-T unit (Gyroscan Intera, software release 8.1; Philips Medical Systems, Best, the Netherlands) with Master gradients (maximum amplitude, 30 mT/m; maximum field of view, 530 mm). Patients were placed in a semioblique supine position on the side of the shunt arm, with the upper extremities lying next to the body. A venous cannula was inserted into the contralateral arm. Because of the complicated and elongated structure of the hemodialysis graft, three-dimensional (3D) time-of-flight surveys of the inflow-outflow tracts and shunt region were performed after the hemodialysis graft was marked with a lipoid marker to accurately plan for high-spatial-resolution contrast-enhanced MR angiography. With this protocol, it was easy for the technician to perform the examination.

A test bolus of 2 mL of gadoteridol (Prohance; Bracco, Milan, Italy) and a subsequent 10-mL saline flush (injection rate, 0.6 mL/sec) were injected via the venous cannula by using an MR imaging–compatible injector (Spectris; Medrad, Indianola, Pa). The test bolus injection and timing image were started simultaneously. A thick coronal slab was imaged in real time (acquisition time for each image, 1.5 seconds). The interval between the start of injection and the maximum of the time-intensity curve, in a region of interest placed in the hemodialysis fistula, helped determine the contrast material bolus arrival time at the level of the fistula. The latter was used as the time delay between the start of contrast material injection and the start of high-spatial-resolution acquisition.

Thirty-nine milliliters of gadoteridol was injected in two subsequent volumes: 20 mL for the shunt region and 19 mL for the inflow-outflow tract (subclavian, axillary, and upper arm arteries and veins); the flow rate was 0.6 mL/sec for both.

Two overlapping 3D contrast-enhanced MR angiographic volumes of the shunt region and inflow-outflow tract were acquired. An optimized elliptic centric profile order was used for k-space filling (contrast-enhanced timing robust angiography). In contrast-enhanced timing robust angiography, the central region of k space is filled during the first 4 seconds of volume acquisition in random order. Subsequently, the k = 0 profile is obtained, and the periphery of k space is acquired in an outward direction. Acquisition of the exact center of k space after 4 seconds of volume imaging makes this technique less sensitive for early timing errors.

A 3D T1-weighted fast-field-echo sequence was used in the shunt region with the following parameters: 4.4/1.5 (repetition time msec/echo time msec), 20° flip angle, and 430 x 129 x 72-mm volume with a matrix of 432 x 346 x 60, which was interpolated to a 512 x 512 x 120 matrix. The acquisition voxel size was 1.0 x 1.2 x 1.1 mm, and the calculated voxel size was 0.8 x 0.8 x 0.55 mm. The 3D data set was obtained in 32 seconds.

In the 3D volume for the inflow-outflow tract, the following parameters were used for: 3.9/1.3, 20° flip angle, and volume of 430 x 215 x 86 mm with a 368 x 294 x 48 matrix, which was interpolated to a 512 x 512 x 96 matrix. The acquisition voxel size was 1.2 x 1.5 x 1.8 mm, and the calculated voxel size was 0.8 x 0.8 x 0.9 mm. The 3D data set was obtained in 35 seconds. Maximum intensity projections were calculated from the 3D data sets with a remote dedicated workstation (Easy Vision; Philips Medical Systems). The mean examination time—including the time for patient preparation, the timing bolus test, and postprocessing—was 37 minutes (range, 30–51 minutes). The MR angiographic examinations were tolerated well by all patients.

DSA Examination
All DSA images (Multistar T.O.P. [time operation performance]; Siemens Medical Engineering, Forchheim, Germany) were obtained with nonionic contrast material (iomeprol, Iomeron 350; Bracco). A 4-F dilator was inserted after puncture of the venous part of the loop graft or Cimino-Brescia fistula. DSA images of the complete venous outflow tract were obtained with repeated manual injection of 5–10 mL of contrast material. The graft and its inflow tract were visualized during manual compression of the venous outflow tract. Magnification images and angled views of suspected stenoses were obtained. All DSA examinations were performed by one of two interventional radiologists (L.E.M.D., A.V.T.), who also performed the blinded reading of the DSA images.

Image Analysis
For image analysis, the vascular tree was divided into the following segments: arterial inflow tract from the subclavian artery (segment I), arterial anastomosis (segment II, with a loop graft), loop graft (segment III), venous anastomosis (segment IV, with a loop graft), venous outflow tract up to the superior caval vein (segment V), and arteriovenous anastomosis (segment VI, with a Cimino-Brescia fistula). Thus, the vascular trees of a loop graft and a Cimino-Brescia fistula were divided into five and three segments, respectively. The diameter of the residual lumen at the point of maximal narrowing in a segment (D) was compared with the diameter at a normal point in that segment (N) by using the following equation: percentage stenosis = (1 - [D/N]) x 100%. The stenosis was graded at a workstation with enlarged maximum intensity projections or DSA images by using electronic calipers. Stenoses with a luminal narrowing of more than 50% were considered to be hemodynamically significant.

Analysis of the contrast-enhanced MR angiographic and DSA images, including postprocessing and measurement of the stenoses with electronic calipers, was done by two MR radiologists (J.H.M.W., H.C.M.v.d.B.) and two interventional radiologists (L.E.M.D., A.V.T.), respectively. The MR radiologists assessed the MR angiographic images independently and were blinded to the findings at DSA. In case of disagreement, consensus was reached after mutual consultation. This assessment technique was also used by the two interventional radiologists, who were unaware of the findings at MR angiography. With regard to the experience of the radiologists, each MR radiologist assesses more than 2,500 MR examinations a year and each interventional radiologist performs about 300 interventional procedures a year.

Statistical Analysis
DSA was used as the standard of reference. Sensitivity, specificity, predictive values, and likelihood ratios for MR angiography in the depiction of vascular segments containing at least one significant (>=50%) stenosis were calculated according to standard procedures.


    Results
 TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Eleven patients had a failing access and, thus, qualified for our study. One patient was excluded because of claustrophobia. Of the remaining 10 patients (six women, four men; mean age, 62 years; age range, 39–86 years), eight had a polytetrafluoroethylene (Goretex; W. L. Gore, Ekton, Md) graft interposition (loop graft) and two had a Cimino-Brescia fistula. In one patient, a 50-mm pseudoaneurysm obscured the arterial anastomosis of a loop graft on multiple DSA projections. In all other patients, DSA revealed the exact topography of the feeding artery, anastomosis, and draining vein or veins. Sixteen significant stenoses were identified (Table).


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Comparison of Findings at DSA and MR Angiography according to Vascular Segment

 
High-spatial-resolution images could be obtained with MR angiography in all patients. Maximum intensity projections displayed the shunt with the feeding artery, anastomoses, and outflow tract up to the superior caval vein in every patient. Forty-six vascular segments were analyzed. In one patient, the brachial and axillary veins could not be assessed properly with MR angiography because they were compressed by the patient’s body. MR angiography showed an 8-cm-long stenotic lesion with smooth outlines, which was easily identified as a pseudostenosis. MR angiography depicted all 16 significant stenoses identified at DSA (Figure). There were two false-positive findings with MR angiography, and these were located in the middle of a loop graft and in the upper arm outflow tract of a Cimino-Brescia fistula, respectively. At DSA, the stenosis rate of both false-positive findings was just under 50%. If each vascular segment was assessed for the presence of significant stenoses and the two segments that could not be interpreted properly with DSA or MR angiography were excluded, the sensitivity and specificity of MR angiography in the detection of these stenosed segments is 100% and 94%, respectively. We found a positive predictive value of 87%, negative predictive value of 100%, positive likelihood ratio of 15.5, and negative likelihood ratio of 0.



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Images in patient 4 show a loop shunt with two stenoses. A, Semicoronal DSA image. B, Semicoronal 3D contrast-enhanced MR angiographic image. a = artery, s1 = stenosis in the distal part of the loop, s2 = stenosis of the venous anastomosis, and v = vein.

 

    Discussion
 TOP
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 
Results of our study show that 3D contrast-enhanced MR angiography can depict hemodialysis grafts and fistulas, including their complete inflow-outflow tract. Our approach to MR angiography enabled us to obtain MR images with submillimeter resolution. MR angiography depicted all substantial stenoses and produced images of all but one vascular segment—a draining vein in one patient. During MR angiography, patients were placed in the semioblique supine position on the side of the shunt arm, with the upper extremities lying next to the body. This position caused outflow tract compression; therefore, the draining vein could not be measured in one patient. This artifact could be prevented by performing the examination with the patient in the prone or lateral position with the shunt arm stretched overhead (8,9). However, this position is much more uncomfortable and may lead to substantial motion artifacts (10). Currently at our institution, we use a dedicated phased-array coil to image the extremities. This surface coil enables better positioning of the shunt arm in slight abduction and, thus, may reduce the chance of outflow tract compression.

In two patients, the severity of vessel stenosis was overestimated with MR angiography compared with that with conventional angiography. With flow-based MR angiographic techniques (eg, phase-contrast and time-of-flight angiography), flow artifacts frequently occur in stenotic regions or bends (11,12). Although contrast-enhanced MR angiography has been shown to be less sensitive to these artifacts (13), overestimation of stenoses should still be regarded as a known limitation (14). We assume that the introduction of a dedicated phased-array coil, which increases the signal-to-noise ratio and thus yields a better spatial resolution, will decrease the tendency to overestimate stenoses. To our knowledge, only one other study (15) was performed with intravenous injection of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) to image hemodialysis accesses. With use of a 0.5-T MR unit, only limited segments of the inflow-outflow tract were depicted, and the sensitivity for the detection of significant stenoses was 91%.

In our study, contrast material was administered via a venous cannula. Bos et al (16) obtained detailed images by injecting gadopentetate dimeglumine directly into the access while a cuff was used to reduce and subsequently interrupt access flow. Drawbacks of this approach are the invasive character of the procedure and the inability to provide complete venous outflow.

In the method of analysis we used to detect stenosis, independence of the readings within a patient is assumed. We acknowledge that the use of this approach may have affected the results because the existence of dependency cannot be ruled out.

The combination of contrast-enhanced MR angiography and MR velocity mapping may be especially useful because they can provide both a vascular map and quantitative measurements of blood flow via hemodialysis accesses (1719). We are now incorporating blood flow measurements in MR studies of failing grafts and fistulas and believe that this velocity mapping will provide additional value for the detection of a hemodialysis access at risk.

To validate the exact value of our high-spatial-resolution MR angiographic approach, larger patient cohorts are necessary to determine which diagnostic strategy (duplex US, DSA, MR angiography, or a combination of modalities) is most cost-effective for planning therapy.

In summary, our preliminary results indicate that 3D contrast-enhanced MR angiography with high spatial resolution is a promising diagnostic modality for evaluating the complete vascular tree of failing hemodialysis grafts.


    FOOTNOTES
 
Abbreviations: DSA = digital subtraction angiography, 3D = three dimensional

Author contributions: Guarantors of integrity of entire study, K.M.H., L.E.M.D.; study concepts and design, K.M.H., L.E.M.D.; literature research, K.M.H., L.E.M.D.; clinical studies, K.M.H., L.E.M.D., P.W.M.C., P.D.D.; data acquisition, K.M.H., L.E.M.D., G.R.P.T., A.V.T., J.H.M.W., H.C.M.v.d.B.; data analysis/interpretation, K.M.H., L.E.M.D., P.W.M.C., P.D.D., A.V.T., J.H.M.W., H.C.M.v.d.B.; statistical analysis, K.M.H., L.E.M.D.; manuscript preparation, K.M.H., L.E.M.D., H.C.M.v.d.B.; manuscript definition of intellectual content and editing, K.M.H., L.E.M.D., G.R.P.T., H.C.M.v.d.B.; manuscript revision/review, L.E.M.D., P.W.M.C., P.D.D., H.C.M.v.d.B.; manuscript final version approval, all authors.


    REFERENCES
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 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 REFERENCES
 

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