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British Journal of Radiology (2005) 78, 292-298
© 2005 British Institute of Radiology
doi: 10.1259/bjr/16043862

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Full Paper

Perioperative monitoring of flow and patency in native and grafted internal mammary arteries using a combined MR protocol

N I Stauder, MD1, A M Scheule, MD2, U Hahn, MD1, M Fenchel, MD1, F S Eckstein, MD2, U Kramer, MD1, C D Claussen, MD1 and S Miller, MD1

1 Department of Diagnostic Radiology and 2 Department of Thoracic, Cardiac and Vascular Surgery, Eberhard-Karls-University, Tübingen, Hoppe Seyler-Str. 3, 72076 Tübingen, Germany


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 
The objective of this study was to evaluate graft flow (f) and patency (p) in patients with internal mammary artery (f,p) and venous (p only) grafts using a combined MR protocol with phase-contrast technique and MR angiography. 42 patients with 42 left internal mammary artery (LIMA) and 63 venous grafts were examined pre and 6 months post coronary artery bypass graft (CABG) surgery. Phase-contrast flow measurements were applied to the IMA. Post-operatively, a contrast enhanced MR angiogram was performed to assess bypass patency. LIMA/venous grafts were occluded in 3/42 and 13/63, respectively. Flow in LIMA decreased from 19.4±10.4 ml min–1 m–2 pre-operatively to 13.4±9.7 ml min–1 m–2 post-operatively (p<0.002). In contrast, flow in the native right IMA increased from 17.6±8.7 ml min–1 m–2 pre-operatively to 24.8±9.0 ml min–1 m–2 post-operatively (p<0.001). MRI allows a combined assessment of bypass patency and flow. This study protocol may be applicable to perioperative follow-up studies in patients after CABG surgery.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 
In patients with coronary artery disease (CAD) surgical re-vascularization is performed to treat angina and/or heart failure. Treatment is either by internal mammary artery (IMA) coronary artery bypass graft (CABG) or homologous venous CABG. Patients usually have a reduction of clinical symptoms and an increase in quality of life after re-vascularization [1]. However thoracic discomfort can persist in a subgroup of patients after surgical therapy. These symptoms are often difficult to distinguish from angina pectoris and the question of bypass occlusion or bypass stenosis may be raised. At present, the diagnostic method of choice in this situation is invasive catheter angiography to investigate coronary artery and bypass status. Here, previous studies revealed an incidence of bypass occlusion during the first year of up to 5% for IMA grafts and up to 20% for venous grafts [2, 3]. MRI has been tested as an early non-invasive alternative diagnostic tool [4, 5]. It was found, that information about patency of bypass grafts could be obtained by quantitative flow measurements [6, 7]. Furthermore, several authors demonstrated the feasibility of assessing the morphology of bypass grafts by MRI [810]. However, visualization of IMA bypass grafts was found to be difficult with two-dimensional (2D) spin echo and 2D gradient echo sequences. This was mainly due to the smaller diameter of IMA bypass grafts compared with venous bypass grafts [4, 7]. Even though the morphological delineation of the bypass grafts could be improved by contrast enhanced 3D MR angiography (ceMRA), the visualization of the vascular mediastinal course was still hampered by metallic clip artefacts and the depiction of the distal anastomosis remained problematic [9, 10]. A combination of flow measurements and ceMRA could be beneficial to improve the diagnostic evaluation of IMA grafts.

The purpose of this study was to evaluate a combined protocol for assessment of patency and flow quantification of LIMA bypass grafts, and patency alone for venous grafts. Also mean flow in the IMA vessels was followed before and after surgical re-vascularization.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 
Patient study
42 patients (39 males, 3 females; mean age of 61.4±8.5 years old) were studied with MRI before and 7.3±2.3 months after CABG surgery. A total of 105 grafts (42 LIMA and 63 venous grafts) were placed. The LIMA grafts were exclusively solitary grafts attached to the left anterior descending artery (LAD). Concerning the venous grafts, 31 were anastomosed to an area supplied by the LAD, 46 to an area supplied by the Ramus circumflexus (RCX) and 36 to an area supplied by the right coronary artery (RCA). The total number of distal anastomoses was n=155 (42 LIMA and 113 venous).

Medical history was obtained from patients pre- and post-operatively concerning chest discomfort and amount of tolerable exercise. Participation in the study was voluntary and patients were enrolled after giving written informed consent. The study was approved by the review board of our hospital.

MRI
MR examinations were performed with a 1.5 T whole-body system Magnetom Vision (Siemens Medical Systems, Erlangen, Germany) using a phased-array surface coil and prospective ECG-triggering. Pre-operatively, all patients had flow quantification (FQ) through the ascending aorta and both the IMA. Post-operatively besides the FQ, ceMRA was also performed. At first, a transverse T1 weighted fast spin echo sequence (repetition time (TR)=RR interval (cardiac cycle between two R waves on electrocardiogram), echo time (TE) 12 ms, field of view (FOV) 320 mm x 320 mm, matrix 256 x 256, slice thickness 5 mm, length of echo-train n=3 echos) was applied for the examination of mediastinal anatomy and location of the bypass grafts. After that the aortic arch was localized, flow measurement was performed perpendicular to the ascending aorta, 1 cm proximal to the branching of the brachiocephalic trunk. A phase contrast FLASH 2D sequence (TR 24 ms, TE 5 ms, flip angle 20°, FOV 250 mm x 250 mm, matrix 256 x 256, slice thickness 5 mm, velocity encoding 250 cm s–1, spatial resolution 0.98 mm x 0.98 mm, two signal averaging measurements) was applied. The number of phases over the cardiac cycle was adapted to the heart rate of the patient and calculated as follows:Go


{780292E001}

with TR=24 ms.

Furthermore, flow measurements of the IMA were performed at the level of the bifurcation of the pulmonary trunk perpendicular to the course of the vessel. Velocity encoding was 75 cm s–1. Flow was determined for the left (LIMA) as well as for the right IMA (RIMA). Identical protocols were used for pre- and post-operative examinations.

Post-operatively for the ceMRA a 3D FLASH sequence (TR 3.8 ms, TE 1.4 ms, flip angle 30°, FOV 300 mm x 300 mm, matrix 160 x 256, slab thickness 132 mm, 44 partitions, interpolated to 88 partitions and a resulting voxel size of 1.5 mm x 1.9 mm x 1.2 mm, no ECG-triggering) was used. The determination of transit time was done with a Turbo FLASH 2D sequence. A power injector (Medrad Spectris, Volkach) was used to inject 3 ml Gd-DTPA (Magnevist®) for the evaluation of transit time and 25 ml Magnevist® for the ceMRA, respectively, both followed by 30 ml 0.9% NaCl into an antecubital vein at a flow rate of 2.5 ml s–1. Calculation of the delay time between injection of contrast agent and start of image acquisition was done according to the formula:Go


{780292E002}

Data analysis of ceMRA
Two experienced investigators reading localization and patency of bypass grafts by source images as well as maximal intensity projections (MIP) in a consensus mode. Information about the type of the bypass graft and the supplied areas of the bypass grafts was present at the time of reading.

For data analysis the IMA graft was subdivided into five segments: branching from the subclavian artery, proximal third, middle segment, distal third and anastomosis to LAD. An IMA graft was considered "open" if the full course of the vessel including the distal anastomosis was visible or if blood flow with a biphasic flow curve could be measured in the IMA graft although the vessel was not be continuously depicted at ceMRA (e.g. anastomosis of the vessel to the LAD). The vessel was rated "occluded", if there was a visualization stop in the graft course without contrasted areas in the more distal parts of the graft and no measurable flow in the graft.

Venous bypasses were evaluated and subdivided in segments as follows: branching from the ascending aorta, proximal segment, distal segment, anastomosis. The vessel was considered "open", if the graft was continuously visible distal to the aortic anastomosis. The venous graft was rated "occluded", if only the proximal anastomosis and/or a short proximal stub was seen, or if the vessel was not visible at all.

The subjective quality of bypass delineation (visibility) was ranked with a five-step scale: excellent=4, good=3, fair=2, poor=1 and not visible=0.

Flow measurement by MRI
The standard software of the MR system (Numaris, Siemens, Version 3B 31A) was used for image post-processing and flow quantification analysis. The lumens of the native IMA vessels and grafted LIMA were identified on magnitude images of the flow quantification sequence. A region of interest (ROI) was drawn manually around the lumen, and a reference ROI to correct flow measurements against cephalocaudal respiratory motion was placed into adjacent mediastinal fat. Both ROIs were automatically transferred to phase images by the software.

The IMA flow values were determined as absolute values in millilitres per minute, as index values corrected for body surface area, and as a percentage of aortic flow (FIMA/Aorta).

Statistical analysis
Mean and standard deviation of functional parameters were calculated from pre- and post-operative measurements. The significance regarding changes of functional parameters was determined by a student's t-test. The level of significance was set to p<0.05. Interobserver and intraobserver variability of flow measurements before and after re-vascularization were determined by two independent investigators using the Bland and Altman approach [11].


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 
Complete pre-operative and follow up data could be obtained in all patients. Duration of the examination was 40–50 min pre-operatively, and 45–55 min post-operatively, and was well tolerated by all patients.

In five cases selective visualization of the bypass grafts by coronary artery angiography and in three cases a spiral multidetector CT of the thorax (Volume Zoom, Siemens, 4 x 1 mm, 120 ml Imeron 400®) was performed due to chest pain (i.e. angina, atypical chest pain, intermittent thoracic discomfort).

MR angiography
At ceMRA, 38 of 42 (93%) LIMA grafts were rated open and 4 of 42 occluded. 13 of 42 (31%) distal LIMA anastomosis could be detected (visualization=0.7±1.3). In Figure 1aGo MIP reconstruction of an IMA graft including the distal anastomosis to the LAD is given. Figure 1bGo demonstrate single slice images of the MRA in the same patient.



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Figure 1. (a) Maximum intensity projection (MIP) reconstruction of an internal mammary artery (IMA) graft including the distal anstomosis to the left anterior descending artery. Discontinuity through clip artefacts. (b) Single slice images of the MR angiography of the same patient.

 
50 of 63 (80%) venous grafts were rated open and 13 of 63 (20%) for occluded. 12 of 34 (35%) sequentially bypasses and 7 of 113 (6%) distal anastomosis of venous grafts could be detected. Detailed results of the ceMRA are summarized in Table 1Go. One of four LIMA vessels which were rated occluded by ceMRA demonstrated sudden disruption in the middle segment. However, flow measurement revealed a residual flow of 5 ml min–1 m–2 suggesting that the vessel was highly stenosed but patent. Owing to clinical symptoms, a selective catheter examination was performed confirming a pronounced stenosis of the LIMA graft and occlusion of the sequential venous graft. The solitary venous CABG had a small diameter but was patent as seen in the ceMRA. A biphasic flow pattern with a flow of 26 ml min–1 m–2 was present in the LIMA graft of another patient with poor contrast enhancement and disrupted LIMA bypass by ceMRA (Figure 2Go). Due to the flow measurement the LIMA graft was rated open. Selective bypass catheterization proved the patency of the LIMA bypass (Figure 3Go).


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Table 1. Graft patency of 63 (with 113 distal anastomoses) venous and 42 LIMA grafts by MRA versus MRI (MRA combined with IMA graft flow measurements)

 


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Figure 2. MR angiography maximum intensity projection poorly demarcated left internal mammary artery graft with disruption.

 


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Figure 3. Selective bypass catheterization of the same patient: left internal mammary artery (LIMA) graft well contrasted. Short black arrows: LIMA graft. Long white arrow: anastomosis to left anterior descending artery.

 
The assessment of the visual quality of LIMA and venous bypass grafts in the various segments of the vessels is demonstrated in Table 2Go.


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Table 2. Visibility of the left internal mammary artery (LIMA) and venous grafts by magnetic resonance angiography

 
Comparison of pre- and post-operative flow measurements in LIMA and RIMA
Pre-operatively the flow pattern of the IMA vessels had a systolic maximum (Figure 4aGo). Quantitative assessment of pre-operative flow in LIMA grafts revealed a range of 15–92 ml (19.4±10.4 ml min–1 m–2). Characteristic changes of flow patterns were observed, when comparing pre- and post-operative IMA flow curves, with a post-operative biphasic flow pattern having a lower systolic and a maximum diastolic peak (Figure 4bGo). Post-operatively there was a significant decrease in quantitative flow values, with a range of 5–90 ml (13.4±9.7 ml min–1 m–2, p<0.002). A significant decrease (p<0.02) in FLIMA/Aorta was present pre-operatively (0.76±0.38) compared with post-operatively (0.54±0.37). In contrast, there was a significant increase in mean flow in the native RIMA from 17.6±8.7 ml min–1 m–2 pre-operatively to 24.8±9.0 ml min–1 m–2 post-operatively (p<0.001). Similarly there was a significant increase (p<0.005) of FRIMA/Aorta from 0.76±0.38 pre-operatively to 1.1±0.59 post-operatively. An identical flow pattern in the RIMA was observed pre- and post-operatively, with a monophasic early systolic flow maximum. Representative flow measurement in a LIMA graft is shown in Figure 5Go.



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Figure 4. Representative left internal mammary artery (LIMA) flow quantification pre- and post-operatively of the same patient. (a) Pre-operatively monophasic flow pattern with systolic maximum. (b) Post-operatively biphasic flow pattern in LIMA graft with maximum diastolic peak.

 


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Figure 5. (a) Magnitude- and (b) Phase-Image of the post-operative flow quantification sequence. The arrows show the left internal mammary artery graft.

 
The intraobserver variability of flow measurements was 5.6±3.7% in the native IMA vessels (pre-operative LIMA/RIMA, post-operative RIMA) and 17.2±9.4% in the LIMA graft. The interobserver variability was 10.5±5.7% for the evaluation of the native IMA vessels and 22.4±12.1% for the LIMA grafts.


    Discussion
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 
In the present study MRI was used to non-invasively follow up patients after surgical myocardial re-vascularization. The imaging protocol comprised several important determinants of the patients cardiovascular condition, such as bypass patency as well as the flow in the IMA at several time points. As a key finding we observed a significant decrease of mean flow in the LIMA graft post-operatively, whereas mean flow in the native RIMA increased after surgery. 93% of LIMA grafts and 80% of venous grafts were considered patent and 31% of distal LIMA anastomosis could be demonstrated. There was a decrease in visibility of graft segments near the heart.

MR angiography
Since the beginning of the 1990s various MRI methods have been investigated in the assessment of CABG. MRI studies of CABG have been performed comparing the role of spin-echo and gradient-echo techniques. Here spin-echo techniques revealed a sensitivity ranging between 79% and 98% and a specificity between 72% and 85% [4, 13]. Using gradient-echo techniques sensitivities between 88% and 98% and specificities between 86% and 91% were found [5, 13]. Kalden et al [8] recently reported on the use of HASTE imaging in the assessment graft patency with a sensitivity of 95% and a specificity of 93%. A major limitation was the reduced spatial resolution and difficulty in the assessment of the small diameter IMA grafts (sensitivity 80–93%, specificity 50–100%). The authors proposed that this method might be used as a localizer for subsequent ceMRA.

Contrast enhanced 3D MR angiographic methods have been available since the middle of the 1990s. Studies employing ceMRA yielded sensitivities for bypass patency of between 93% and 95% and specificities of between 67% and 97% [9, 10, 14].

Several studies have reported difficulties in the evaluation of IMA grafts because of the small vessel diameter and numerous surgical clips [4, 7]. Clips in the region of the LIMA also proved to be the limiting factor in the evaluation of our data, especially when MIP reconstructions were evaluated (Figure 1aGo). In patent vessels, the proximal segment of the bypass was clearly visible (2.8±1.2). The distal anastomosis of the LIMA could be detected in 31% of all cases, whereas in previous studies this region could not be assessed [5, 10]. The individuals' breath holding capability was a limiting factor considering the duration of ceMRA-sequence (21 s). ECG-triggering would probably improve the assessment of bypass segments adjacent to the heart owing to the reduction of pulsation artefacts, however this would further prolong the data acquisition and scan times.

Another alternative used in the morphological examination of bypass grafts by MRI is the navigator technique [15]. However, such sequences require long period of data acquisition.

True fast imaging with steady-state precession (true FISP) is another promising new technique for cardiac MRI. True FISP images have a higher contrast to noise ratio (CNR) than images acquired with FLASH sequences [16]. Bunce et al [17] recently reported that the accuracy for detection of coronary artery bypass graft patency was similar with gadolinium-enhanced MRA and true FISP angiography, with a trend toward more false-positive findings for occlusion and reduced visualization of arterial grafts with true FISP angiography.

Flow measurements
Beyond the morphological delineation of bypass grafts flow measurements were found to be accurate in quantifying blood flow in CABG [6, 7]. In contrast to its application for assessment of major thoracic vessels, such as the aorta or the pulmonary arteries, partial volume effects are of major relevance in the determination of flow volumes in small vessels such as coronary arteries and bypass grafts. At the vessel boundary, voxels may contain both signal from vessel and from surrounding tissue. Partial volume effects can degrade the results of this technique and may lead to an overestimation of flow volumes [18]. Nevertheless, phase contrast flow measurements in small diameter phantom models, as well as in the coronary arteries of animals, were proven to be feasible and provided accurate reproducibility [19]. While Tang et al [18] first proposed that 9–16 pixels would be necessary in order to acquire exact flow measurement results, Hofmann et al [20] proposed that 4 pixels covering the vessel diameter would produce acceptable accuracy. These conditions were used in the present study, and the IMA flow values and flow patterns observed confirm in this. Kreitner et al [21] also found absolute flow values in IMA grafts of 53.3±51.2 ml min–1.

In our patients, LIMA flow was significantly higher pre-operatively compared with post-operative flow values. This may be due to the dissection of peripheral LIMA branches post-operatively. Other groups reported higher flow values post-operatively in the native RIMA compared with the LIMA bypass graft [6, 22]. The significant increase of native RIMA blood flow post-operatively may be due to a compensatory blood flow to territories supplied by the dissected LIMA branches beforehand. This finding has never previously been reported. Ishida et al [12] recently noted, that velocity encoded cine MR blood flow measurement at baseline is highly useful in predicting significant stenosis in IMA grafts. Severe stenoses were detected with a sensitivity of 86% and a specificity of 88% [12]. A clinical application could be the serial assessment of graft function, which is useful in detecting gradual increases in graft stenosis before the onset of total occlusion. Even more information can be obtained by measurement of the flow reserve. Langerak et al [23] recently reported, that a newly developed turbo field echo planar imaging (TFEPI)-technique allowed accurate assessment of flow reserve in bypass grafts without breath holding [23].

A major limitation of our study is the absence of a gold standard for comparison, as for ethical reasons, cardiac catheterization or CT was only performed in symptomatic patients. As such we may be under-reporting false negative results. This emphasizes the fact that the results of patency and flow on both MRA and flow quantification may not reflect the true graft status in all patients. The lower values of flow volume in the post-operative LIMA grafts may represent stenosis [12] even in the absence of symptoms.

In the present study the combination of MRA and 2D-phase contrast flow quantification was beneficial in clinical practice and their individual limitations reduced.

In summary the present study demonstrates the feasibility of MRI in following up patency and flow in LIMA grafts with an acceptable examination time. Patients with persisting ischaemic symptoms after surgical myocardial re-vascularization, could be offered a non-invasive method to evaluate their bypass graft patency and this would used to help identify those patients who need re-intervention.


    Acknowledgments
 
The study was promoted by the Dr Karl-Kuhn foundation in Tübingen, Germany.

Received for publication October 15, 2003. Revision received September 16, 2004. Accepted for publication September 26, 2004.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 References
 

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