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Cardiac Imaging |
1 From the Departments of Cardiology (S.E.L., H.W.V., J.W.J., E.E.v.d.W.) and Radiology (P.K., H.J.L., A.d.R.), Leiden University Medical Center, Albinusdreef 2, 2300 RC Leiden, the Netherlands; and the Interuniversity Cardiology Institute of the Netherlands, Utrecht (S.E.L, E.E.v.d.W., A.d.R.). Received March 10, 2000; revision requested April 26; revision received June 16; accepted July 25. S.E.L. supported by a grant from the Netherlands Heart Foundation (96.122). Address correspondence to A.d.R. (e-mail: A.de_Roos@LUMC.nl).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Aortic and internal mammary artery flow was measured in 11 healthy volunteers by using conventional cine gradient-echo imaging as a reference standard method and turbo-field echo-planar imaging (TFEPI). By using TFEPI, breath-hold flow mapping with a spatial and temporal resolution of 0.8 mm2 and 23 msec, respectively, can be performed. This sequence was applied in 20 angiographically normal grafts, and total blood flow at rest and during adenosine infusion (140 µg/kg/min) was measured.
RESULTS: Good agreement in aortic and internal mammary artery flow values between conventional fast-field echo and TFEPI techniques was found. The mean bypass graft total flow (± SD), as assessed with TFEPI, increased from 30.8 mL/min ± 13.5 to 76.7 mL/min ± 36.5 (P < .05) to yield a flow reserve of 2.7. Furthermore, this sequence revealed a difference in total flow between single and sequential grafts at rest (25.4 mL/min vs 40.9 mL/min; P < .05) and during stress (65.2 mL/min vs 98.3 mL/min; P < .05).
CONCLUSION: Breath-hold TFEPI provides fast accurate flow measurements with high temporal resolution and allows motion-compensated flow quantification in multiple coronary artery bypass grafts during one 6-minute adenosine infusion.
Index terms: Arteries, grafts and prostheses, 941.1269, 949.1269 • Arteries, MR, 941.129412, 941.129416, 941.12944 • Arteries, stenosis or obstruction, 941.721, 949.721 • Blood, flow dynamics • Coronary vessels, flow dynamics, 54.731 • Magnetic resonance (MR), vascular studies, 941.12944
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Magnetic resonance (MR) flow mapping of bypass grafts can be used as a noninvasive alternative for the assessment of bypass graft function (4–9). To our knowledge, previous MR studies have not focused on flow measurements in coronary artery bypass grafts during adenosine-induced stress. To measure flow in multiple coronary artery bypass grafts during a 6-minute adenosine infusion, a fast MR flow sequence with respiratory compensation and adequate temporal and spatial resolution is required. Previous MR flow sequences usually have not been respiratory compensated and thus might result in image blurring and a long imaging duration (4–6). Breath-hold flow mapping could meet the requirements of fast flow measurements and allow the functional assessment of flow and flow reserve in different bypass grafts in one patient during adenosine-induced stress. However, conventional breath-hold MR techniques have been of limited use because of their low temporal resolution (7–9), which may result in image blurring caused by cardiac motion during image acquisition and the underestimation of flow owing to low pass filtering (ie, undersampling) (10,11).
More recently, fast echo-planar imaging and turbo-field echo-planar imaging (TFEPI) MR flow sequences that allow the accurate assessment of blood flow in relatively large vessels during a single breath hold of nine (echo-planar imaging) (12) or 12 (TFEPI) (13) heartbeats have been described. TFEPI flow measurements enable one to perform fast image acquisition while maintaining a low echo time and thus improve temporal resolution. Improved temporal resolution may lead to less averaging of flow velocity over the time window and increase measurement accuracy (14).
The purpose of the present study was twofold: (a) to validate a breath-hold MR flow sequence with high temporal resolution in healthy volunteers and (b) to use this breath-hold TFEPI flow sequence to measure flow in coronary artery bypass grafts under short-duration stress induced by adenosine infusion.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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After obtaining scout images of the heart, we performed flow mapping in the transverse plane at the level of the ascending aorta by using both a conventional non–respiratory-compensated phase-contrast fast-field echo (FFE) MR sequence (15,16) and a breath-hold phase-contrast TFEPI MR sequence. The same level was used to evaluate both aortic flow and internal mammary artery flow, because both vessels follow a course perpendicular to this plane. Conventional FFE MR flow mapping was performed during free breathing and took approximately 3 minutes, depending on the heart rate. This sequence was retrospectively electrocardiographically gated. Imaging parameters included the following: 14.0/4.1 (repetition time msec/echo time msec), 6-mm section thickness with a 128 x 128 matrix, 200 x 170-mm field of view with an in-plane spatial resolution of 1.6 x 1.3 mm, 20° flip angle, and two signals acquired to result in a temporal resolution of 28 msec. To encompass the velocity ranges in both the aorta and the internal mammary artery, velocity sensitivity in the section-select direction was chosen so that a 180° phase shift corresponded to a flow velocity of 200 cm/sec.
Breath-hold TFEPI MR flow mapping involves multiple excitations within one heart phase interval, and each excitation is followed by echo-planar imaging readout. Owing to the use of multiple short echo-planar imaging readouts, this technique allows fast image acquisition while keeping the echo time low. In the present study, two alpha pulses, each of which was followed by three echo-planar imaging readouts, were applied per heart phase interval to result in a shot length of six k lines and a temporal resolution of 23 msec. Breath-hold TFEPI flow data were acquired in 10 shots; this resulted in an imaging duration of 20 heartbeats, because both flow velocity–compensated images and encoded images are obtained in a sequential order. A field of view of 200 x 100 mm and a data acquisition matrix of 128 x 60 rendered an in-plane spatial resolution of 1.6 x 1.6 mm, which was reconstructed to 0.8 x 0.8 mm by means of zero filling of k space. The following imaging parameters were used for this sequence: 11.0/4.6, 6-mm section thickness, 20° flip angle, and 200-cm/sec velocity-encoded gradient. This sequence was prospectively electrocardiographically triggered and performed during an end-expiratory breath hold. After receiving an instruction to breathe in and out several times, the volunteers were instructed to stop breathing after normal expiration. The respiratory maneuver was monitored, and care was taken to ensure that the volunteer first expired before cessation of breathing and subsequently did not breathe in anymore.
Coronary Artery Bypass Graft Flow
Patients who had one or more patent coronary artery bypass grafts with a patent native coronary arterial bed beyond the distal anastomosis at coronary angiography for evaluation of recurrent chest pain were screened from February to July 1999 for possible inclusion in the study. Patients with chronic obstructive pulmonary disease, sick-sinus syndrome, and/or a second- or third-degree atrioventricular block were excluded because of contraindication to adenosine infusion (17). Other exclusion criteria were unstable angina, the presence of a pacemaker or transcutaneous electronic nerve stimulation apparatus, atrial fibrillation, claustrophobia, and inability to lie flat. Eighteen patients were included in the present study. They were not allowed to have caffeine-containing beverages on the day of the MR examination. All patients gave written informed consent to participate in the protocol, which was approved by the medical ethical committee of Leiden University Medical Center. Three patients were excluded from further analysis because breath holding was not possible and thus degraded MR images were obtained.
In the remaining 15 patients (14 men, one woman; mean age, 66 years ± 8; age range, 57–79 years), 20 coronary artery bypass grafts—18 venous and two arterial—that were free of stenosis were analyzed. Thirteen bypass grafts had a single distal connection: Four of these grafts were attached to the left anterior descending coronary artery; six, to the left circumflex coronary artery; and three, to the right coronary artery. The mean time between coronary artery bypass graft surgery and MR examination was 8.8 years ± 4.7 (range, 1–18 years).
After scout views were obtained, venous and arterial bypass grafts were identified in the transverse plane at the level of the ascending aorta by using a breath-hold electrocardiographically triggered two-dimensional turbo field-echo MR angiographic sequence. K-space segmentation was used to obtain 10 k lines per cardiac cycle at the middle of the diastole (acquisition window, 138 msec); this resulted in an imaging duration of 16 heartbeats. A field of view of 250 x 175 mm and matrix of 256 x 160 yielded an in-plane spatial resolution of 1.0 x 1.1 mm. Other imaging parameters included 11.3/5.1, a 5-mm section thickness with a 1-mm intersection gap, and 50° flip angle. Oblique coronal views of bypass grafts in the left anterior descending and left circumflex coronary arteries also were obtained.
To measure flow, the previously described breath-hold TFEPI sequence was performed during end expiration. This breath-hold protocol was identical to that used for the healthy volunteers. Flow mapping was performed perpendicular to the bypass graft segment. Optimal section position was determined according to findings on transverse and oblique coronal images of bypass grafts to the left anterior descending and left circumflex arteries, whereas flow mapping in the right coronary artery bypass grafts was performed in the transverse plane because of this vessel’s vertical course in the thoracic cavity (18). Both at baseline and during pharmacologic stress, a velocity encoding of 75 cm/sec was used.
After quantification of the bypass graft total flow at rest, an intravenous adenosine infusion (140 µg/kg/min) was started. Breath-hold flow mapping was started 2 minutes after the onset of continuous adenosine infusion at maximal vasodilatation. Blood pressure and electrocardiographic monitoring and registration (Millennia 3500; Invivo Research, Orlando, Fla) were performed at rest and during adenosine infusion in all patients.
Data Analysis
Paired modulus and phase images of both the aorta and internal mammary artery and bypass graft flow images were displayed on an image-processing SPARC workstation (Sun Microsystems, Mountain View, Calif) by using the FLOW analytic software package (Medis, Leiden, the Netherlands) (Figs 1, 2) (19). The luminal area was traced manually on the modulus image and transferred to the velocity map by an experienced operator (S.E.L.). The position and size of each contour was adjusted according to the cardiac time frame. The mean velocity (in centimeters per second) within each region of interest and the area of the region of interest (in centimeters squared) were determined. For each cardiac time frame, the flow rate (in milliliters per second) was calculated by multiplying the mean velocity within the region of interest by the region of interest area. Subsequently, curves of velocity and flow rate versus time were reconstructed (Figs 3, 4).
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In all coronary artery bypass grafts, total flow, peak systolic velocity and flow rate, and peak diastolic velocity and flow rate were determined both at rest and during pharmacologic stress. Total flow was calculated as the integrated volumetric flow per minute. In addition, peak systolic and diastolic velocity and flow rate were assessed from velocity and flow rate versus time curves as the maximum velocity and flow rate, respectively, during systole and diastole. Flow reserve was defined as the ratio of total flow during adenosine infusion to total flow at baseline. The mean graft area was calculated as the mean size of the region of interest on the modulus flow images obtained during the cardiac cycle. One observer (S.E.L.) performed flow analyses of all the bypass grafts twice on separate occasions more than 6 months apart.
Statistical Analysis
Analysis of the limits of agreement between conventional FFE MR flow mapping and breath-hold TFEPI MR flow mapping, as described by Bland and Altman (20), was performed. All values were expressed as means plus or minus the SD and mean differences plus or minus the SD. The intraclass correlation coefficient was used as the parameter of agreement of values. Comparisons between systolic and diastolic peak flow values in the bypass grafts and between flow values at baseline and those during adenosine infusion were made by using a two-tailed paired Student t test. The graft area, peak systolic velocity and flow rate, peak diastolic velocity and flow rate, and total flow in single bypass grafts were compared with these values in sequential bypass grafts by using a two-tailed unpaired Student t test. Intraobserver variability in total bypass graft flow was calculated as the absolute difference in flow between the two TFEPI flow analyses divided by the mean flow of both analyses (in percentage) and depicted on a Bland-Altman plot.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Validation Study
To validate the TFEPI flow sequence, we compared it with conventional FFE flow mapping (15,16,21–23) in both large and small vessels that are relatively stationary during respiration—that is, the aorta and internal mammary artery. Because conventional free-breathing FFE is a non–respiratory-compensated flow technique, it cannot be used as a reference standard for validation purposes in coronary artery bypass grafts that move considerably during respiration (24). Therefore, the fast TFEPI MR flow sequence was validated in the aorta and internal mammary artery of healthy volunteers by comparing it with the accepted conventional FFE technique. Moreover, conventional FFE involves a relatively long acquisition duration, which does not allow respiratory-compensated assessment of multiple coronary artery bypass grafts in a patient under short-duration pharmacologic stress.
The aortic and internal mammary artery flow measurements obtained by using the breath-hold TFEPI and conventional free-breathing FFE flow techniques closely agreed in the current study. To avoid increased or decreased intrathoracic pressure and a Valsalva or Müller effect, breath holding was performed during end expiration after the patients, following clear instructions, had practiced, as described earlier (in Materials and Methods). The breath hold, which had a duration of 20 cardiac cycles, was easily performed in all volunteers and patients. Recently, similar aortic flow values were obtained by using both a breath-hold approach at shallow inspiration without a Valsalva maneuver and a free-breathing flow technique (25). The similar values indicated that venous blood return to both ventricles was not substantially influenced by breath holding. Our study results showed that the breath-hold TFEPI MR flow sequence is an accurate noninvasive tool for the measurement of absolute flow and flow rate in both large and small vessels that have a pulsatile flow pattern and are relatively stationary during respiration.
Coronary Artery Bypass Graft Flow
Subsequently, breath-hold TFEP flow mapping was applied in angiographically patent coronary artery bypass grafts to assess normal bypass graft function at baseline and during adenosine-induced stress. The typical biphasic flow pattern was demonstrated in bypass grafts both at rest and during adenosine-induced stress. This bypass graft flow pattern was also reported by others, who used Doppler US (26–28) and MR flow mapping at baseline (5,6,9).
Several functional parameters, such as absolute coronary flow reserve (29,30), relative coronary flow reserve, and fractional flow reserve (31), have been correlated with stenosis severity in coronary arteries. In the present study, total flow, peak systolic and diastolic flow parameters, and flow reserve—defined as the maximum-to-baseline total flow—were evaluated in normal coronary artery bypass grafts. A disadvantage of the flow reserve parameter is that it accounts for both the epicardial resistance, which is affected in cases of stenosis, and the myocardial resistance. A 2.7-fold increase in bypass graft total flow was demonstrated during adenosine stress in the current study. All bypass grafts were free of stenosis, both in the conduit and in the native coronary arterial bed beyond the distal graft anastomosis, as determined by using coronary angiography. This flow reserve corresponds to values reported by others (32), who used an intravascular Doppler flow wire in bypass grafts. Flow reserve was based on significant increases in both the systolic and diastolic velocity and the bypass graft area (Table 2). In two bypass grafts, no increase in total flow was observed during adenosine infusion. Some variation in vasodilator capacity may exist as a result of normal physiologic variation in individuals on one hand and as a result of variation in myocardial resistance on the other (33).
A substantial difference in bypass graft total flow at baseline has been demonstrated between single grafts and sequential grafts to three myocardial regions (5). In the present study, flow quantification at fast TFEPI revealed a significantly higher total flow in sequential grafts than in single grafts not only at baseline but also during adenosine-induced stress. An obvious explanation is that sequential grafts supply a larger coronary arterial bed than do single grafts, which are connected to only a single coronary artery. Therefore, the resistance to flow is lower in sequential grafts, so they have a higher volumetric flow per minute.
The bypass grafts’ total flow measured by using TFEPI in the present study was lower than the flow values obtained by others who used conventional FFE flow mapping (5,6). This may be explained by the artifactual enlargement of vessels with non–respiratory-compensated flow sequences, which results in overestimation of flow (24,34). In-plane vessel motion during non–respiratory-compensated image acquisition results in a variation in the MR signal intensity within voxels near the vessel boundary over time. Modulation of MR signal intensity amplitude results in vessel ghost artifacts and blurring on magnitude flow images and thus an overestimation of vessel area. Previously reported measurements of mean bypass graft area at baseline obtained by using conventional FFE imaging were larger (28–37 mm2) (5) than the mean baseline bypass graft area that we measured by using breath-hold TFEPI flow mapping (single grafts, 12.2 mm2 ± 2.9; sequential grafts, 14.4 mm2 ± 3.9) (Table 2). Moreover, the mean bypass graft area obtained by using breath-hold TFEPI in our study was similar to previous reports of bypass graft area obtained by using quantitative coronary analysis (mean reference diameter, 3.87 mm ± 0.58 to result in a mean reference area of 11.8 mm2 ± 1.7) (35).
Limitations and Considerations for Improvement
The purpose of our study was to apply a fast breath-hold MR flow sequence with high temporal resolution in coronary artery bypass grafts under short-duration pharmacologic stress. The optimized TFEPI sequence was validated in healthy volunteers. Because we compared this segmented echo-planar imaging sequence with a conventional FFE flow technique, slightly different echo and repetition times were used. The TFEPI sequence was optimized for breath-hold duration and temporal resolution, and the pixel resolution in the x direction was similar for the TFEPI sequence, as compared with the pixel resolution on the x axis for the FFE approach. However, a slightly different pixel resolution on the y axis was achieved, and this might have influenced the comparison between the two flow techniques.
Breath-hold TFEPI flow mapping was performed in patent coronary artery bypass grafts at baseline and during pharmacologic stress. Future studies should focus on the assessment of flow, peak systolic and diastolic flow parameters, and flow reserve in both patent grafts and grafts with intermediate and severe stenosis. Moreover, a noninvasive evaluation of graft function during adenosine-induced stress in all coronary artery bypass grafts in a single patient should be undertaken.
Technical improvements in coronary artery bypass graft flow sequences may allow correction for through-plane motion. Through-plane motion may result in overestimation of systolic flow values and underestimation of diastolic flow values (36). However, motion correction achieved by subtracting the velocity of adjacent myocardium from the velocities within the vessel (37,38) is not applicable to bypass grafts, because no adjacent myocardial tissue is present. A correction method for heart-valve flow measurements that allows the section position to be adapted according to the cardiac phase was recently introduced (39). This approach might offer the opportunity for motion-corrected flow measurements in coronary artery bypass grafts.
We conclude that breath-hold TFEPI MR flow mapping with high temporal resolution proved to be accurate for flow quantification in the internal mammary artery and aorta of healthy volunteers. Furthermore, breath-hold TFEPI flow mapping allows noninvasive respiratory-compensated quantification of blood flow in multiple coronary artery bypass grafts under short-duration pharmacologic stress. Additional evaluation is required to determine the predictive value of several MR flow parameters at baseline and during adenosine-induced stress in the detection of hemodynamically significant stenosis in coronary artery bypass grafts.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Abbreviations: FFE = fast-field echo, TFEPI = turbo-field echo-planar imaging
Author contributions: Guarantors of integrity of entire study, H.W.V., E.E.v.d.W., A.d.R.; study concepts and design, S.E.L., H.W.V., E.E.v.d.W., A.d.R.; definition of intellectual content, S.E.L., P.K., H.W.V., H.J.L., E.E.v.d.W., A.d.R.; literature research, S.E.L., P.K., clinical studies, S.E.L., P.K., J.W.J.; experimental studies, P.K., H.J.L.; data acquisition, S.E.L., H.W.V., P.K.; data analysis, S.E.L., P.K., H.J.L.; statistical analysis, S.E.L., P.K., H.J.L.; manuscript preparation, S.E.L.; manuscript editing, S.E.L., P.K., H.J.L.; manuscript review, H.W.V., J.W.J., E.E.v.d.W., A.d.R.; manuscript final approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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) represents the flow rate versus time curve obtained by using the conventional FFE flow technique, and the thin line (
) represents the flow rate versus time curve obtained by using the breath-hold TFEPI flow sequence. Each point represents a single measurement. The flow curves obtained by using the two sequences were almost superimposable in both the aorta and the internal mammary artery.
), which were free of stenosis both in the conduit and in the native coronary artery bed beyond the distal anastomosis at rest and during intravenous adenosine infusion (140 µg/kg/min). The bypass graft total flow increased from 30.8 mL/min ± 13.5 initially to 76.7 mL/min ± 36.5 during adenosine stress to result in a flow reserve of 2.7 ± 1.2. The vertical bars represent the mean plus or minus one SD at baseline (left) and during adenosine-induced stress (right).