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(Circulation. 1995;91:2955-2960.)
© 1995 American Heart Association, Inc.

Articles

Assessment of Left-to-Right Intracardiac Shunting by Velocity-Encoded, Phase-Difference Magnetic Resonance Imaging

A Comparison With Oximetric and Indicator Dilution Techniques

W. Gregory Hundley, MD; Hong F. Li, BS; Richard A. Lange, MD; Dennis P. Pfeifer, PhD; Benjamin M. Meshack; John E. Willard, MD; Charles Landau, MD; Duwayne Willett, MD; L. David Hillis, MD; Ronald M. Peshock, MD

From the Departments of Internal Medicine (Cardiovascular Division) (W.G.H., R.A.L., B.M.M., J.E.W., C.L., D.W., L.D.H., R.M.P.) and Radiology (H.F.L., D.P.P., R.M.P.), University of Texas Southwestern Medical Center at Dallas.

Correspondence to Ronald M. Peshock, MD, Mary Nell and Ralph B. Rogers Magnetic Resonance Center, University of Texas Southwestern Medical Center, 5801 Forest Park, Dallas, TX 75235-9085. E-mail Peshock@rad-rogers.swmed.edu.

	Abstract

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Background Velocity-encoded, phase-difference magnetic resonance imaging (MRI) has been shown to provide an accurate assessment of shunt magnitude in patients with large atrial septal defects, but its ability to determine shunt magnitude in patients with intracardiac left-to-right shunts of various locations and sizes has not been evaluated in a prospective and blinded manner. The objective of the present study was to determine whether velocity-encoded, phase-difference MRI can assess the magnitude of intracardiac left-to-right shunting in humans.

Methods and Results Twenty-one subjects (15 women and 6 men; age range, 15 to 72 years) underwent velocity-encoded, phase-difference MRI measurements of flow in the proximal aorta and pulmonary artery, followed immediately by cardiac catheterization. The presence of left-to-right intracardiac shunting was assessed with hydrogen inhalation, after which shunt magnitude was measured by the oximetric and indocyanine green techniques. Of the 21 patients, 12 had left-to-right intracardiac shunting detected by hydrogen inhalation. There was a good correlation (r=.94) between the invasive and MRI assessments of shunt magnitude. In comparison to oximetry and indocyanine green, MRI correctly identified the 12 patients with a ratio of pulmonary to systemic flow (Qp/Qs) of <1.5 (9 without intracardiac shunting and 3 with small shunts) and the 9 patients with a Qp/Qs of 1.5 (6 with atrial septal defect, 1 with ventricular septal defect, 1 with patent ductus arteriosus, and 1 with both atrial septal defect and patent ductus arteriosus).

Conclusions Compared with measurements obtained during cardiac catheterization, velocity-encoded, phase-difference MRI measurements of flow in the proximal great vessels can reliably assess the magnitude of intracardiac left-to-right shunting.

Key Words: magnetic resonance imaging • imaging • catheterization

	Introduction

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The accurate measurement of the ratio of pulmonic to systemic flow (Qp/Qs) is important in the evaluation of the patient with left-to-right intracardiac shunting, since it is often used to determine subsequent therapy.¹ The asymptomatic patient with a Qp/Qs of <1.5 usually is managed conservatively, whereas the patient with a Qp/Qs of >1.5 whose pulmonary vascular resistance is not markedly elevated usually is referred for surgical correction.² The available methods of determining the magnitude of left-to-right intracardiac shunting include oximetry,^{3 4} indicator dilution,^{5 6} radionuclide scintigraphy,^{7 8} and Doppler echocardiography.^{9 10} The oximetric and indicator dilution techniques, although relatively easy to perform, are invasive. Radionuclide scintigraphy and Doppler echocardiography are noninvasive,¹¹ but the former requires the injection of a radionuclide,¹² and the latter may be technically difficult or impossible to perform in some patients.¹¹ Therefore, a rapid, accurate, noninvasive, and widely applicable method of estimating the magnitude of intracardiac left-to-right shunting is desirable.

With magnetic resonance imaging (MRI), the cardiovascular system can be imaged with high spatial resolution.¹³ Velocity-encoded, phase-difference MR images have been used to measure flow in the carotid artery,¹⁴ proximal aorta and pulmonary artery,^{15 16} and abdominal aorta.¹⁷ Phase-difference methods are based on the principle that hydrogen nuclei moving through a magnetic field gradient accumulate a phase shift proportional to their velocity.¹⁸ Flow is calculated by multiplying blood velocity by the cross-sectional area of the vascular structure of interest. With this technique, flow can be measured quickly; scans can be performed in less than 2 minutes. This technique has been used to quantify intracardiac shunting in patients with large atrial septal defects,¹⁹ but its ability to assess shunt magnitude in patients with small shunts and those with shunts at other locations has not been evaluated. Accordingly, the present study was performed in patients with and patients without intracardiac left-to-right shunting to compare velocity-encoded, phase-difference MRI measurements of shunt magnitude with those obtained by the use of oximetry and indocyanine green.

	Methods

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Study Population
The study was approved by the Institutional Review Board for Human Experimentation at the University of Texas Southwestern Medical Center at Dallas, and all participants gave written, informed consent. The study population consisted of 23 patients (16 women and 7 men; age range, 15 to 72 years) referred for catheterization for hemodynamic evaluation. Patients were ineligible for study if they had an indwelling pacemaker, intracranial clips, intra-auricular or intraocular implants, a history of metal fragments in the eye, claustrophobia, marked ventricular ectopy, aortic or pulmonic stenosis, marked aortic or pulmonic regurgitation, or an unstable medical condition that precluded transport from an intensive care unit.

Study Design
Each patient underwent (1) velocity-encoded, phase-difference MRI measurements of flow in the proximal aorta and pulmonary artery, followed in 1 to 2 hours by (2) cardiac catheterization. Hydrogen inhalation was used to assess the presence of left-to-right intracardiac shunting, as this technique can reliably detect shunts with a Qp/Qs of >1.01.²⁰ Patients in group 1 had hydrogen appearance times of >4 seconds, indicating no left-to-right shunting, whereas those in group 2 had hydrogen appearance times of <4 seconds, indicating left-to-right shunting.²¹ During catheterization, all patients in group 2 underwent a detailed oximetric assessment, as described previously,⁴ followed by the administration of indocyanine green, as described previously.^{6 11} The MRI and invasive measurements were accomplished in close temporal proximity to ensure that similar hemodynamic conditions existed during both assessments. During MRI and catheterization, heart rate and blood pressure were monitored and recorded.

	MRI Technique

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MRI was performed with a 1.5-T Picker Vista HPQ whole-body imaging system (Picker International, Inc). MRI signal acquisition was performed using a method of k-space segmentation called phase-encoding grouping (PEG), which acquires multiple phase-encoding steps for each cardiac frame during each cardiac cycle.²² This technique allows for cardiac scan time to be reduced by a factor equal to the PEG size without a reduction in spatial resolution or a modification of the system hardware. Each line of k-space was acquired using a symmetrical, centrally ordered, PEG scheme. This ordering scheme has the effect of reducing the incidence of ghosting due to eddy current effects and minimizing blurring due to motion between low spatial frequency phase-encode steps.²²

Each patient was positioned supine on the MRI table after placement of ECG monitoring leads, a respiratory gating belt, and a brachial blood pressure cuff. All MR scans used prospective ECG and respiratory gating. Multislice coronal, gradient-echo PEG sequences were used to obtain scout images of the proximal aorta and pulmonary artery. These localizing scans were fast-field echo sequences with first-moment compensation in the read-out and slice-select directions, a repetition time (TR) of 20 milliseconds, and an echo time (TE) of 9.4 milliseconds. Eight-millimeter slices were used with a field of view (FOV) of 50 cm, a flip angle of 40 degrees, a 256x256 matrix, and voxel sizes of 3x2x8 mm.

Interleaved, velocity-encoded, phase-difference PEG sequences positioned across proximal vessel segments were used to measure flow in the aorta and pulmonary artery. A PEG size of 2 (yielding 8 to 12 frames per cardiac cycle) was used in 18 of the 23 patients. In 1 patient, a PEG size of 3 (yielding 9 frames per cardiac cycle) was used, and in 4 patients, a PEG size of 1 (yielding 20 to 26 frames per cardiac cycle) was used. These scans were 10-mm-thick slices with 256x256 matrices and had a FOV ranging from 32 to 45 cm (yielding voxel sizes of 1x1.3x10 mm to 1x1.7x10 mm), a flip angle of 40 degrees, a TR of 19.5 milliseconds, and a TE of 11 milliseconds. For the proximal aorta, an oblique slice was positioned from a coronal scout image perpendicular to the course of the aorta, approximately 2 to 4 cm above the aortic valve and distal to the coronary arterial ostia. Except for patients 10 and 13, the slice positions used for the pulmonary artery were selected from the coronal scout images and corresponded to a plane that produced a circular appearance of the pulmonary artery to minimize partial volume effects during image acquisition. The position was distal to the pulmonic valve but proximal to the bifurcation. In patients 10 and 13, echocardiography suggested the presence of a patent ductus arteriosus, and therefore two flow scans (one of each major branch of the pulmonary artery) were performed. The total pulmonic blood flow for these 2 patients was measured as the sum of flow calculated in the two branches.

After acquisition, the first-order, motion-compensated reference scan and the velocity-sensitized scan were Fourier-transformed to produce two sets of images (magnitude and corresponding phase image). These images were transferred to an image-processing workstation for further analysis. A velocity map was generated by (1) pixel-to-pixel subtraction of the velocity-sensitized and velocity-compensated phase images and (2) application of a correction algorithm designed to remove background phase error. The background correction involved three steps: (1) an operator identified the stationary pixels on the magnitude image of the velocity-compensated acquisition; (2) the processing software fit the background phase onto a two-dimensional plane; and (3) the estimated linear background phase shift was subtracted from the phase-difference image. To complete the generation of the velocity map, we multiplied the background-corrected, phase-difference image by a constant to create a velocity image where pixel gray-scale intensity is represented in millimeters per second. Magnitude images and corresponding velocity maps for the aorta and pulmonary artery in patient 12 are displayed in Figs 1 and 2. After producing the velocity maps, we transferred the digital data to a second image-processing workstation for flow calculations.

View larger version (104K): [in this window] [in a new window]   Figure 1. Magnitude (top) and corresponding velocity maps (bottom) acquired for measuring flow in the proximal aorta. Frames 4 and 6 from the 9 frames acquired during the cardiac cycle of patient 12 are displayed. The letter A indicates the lumen of the proximal aorta. On the velocity map, the gray scale intensity for each pixel encodes for velocity. For each frame of the cardiac cycle, velocity within the vessel is calculated as the average velocity for all the pixels within the lumen.

View larger version (176K): [in this window] [in a new window]   Figure 2. Magnitude (top) and corresponding velocity maps (bottom) of the pulmonary artery in the same two frames for patient 12. The letter P indicates the lumen of the main pulmonary artery. In frame 4, the area of the vessel and velocity of the blood flowing through it are larger than in frame 6, thus indicating substantially higher flows for earlier frames of the cardiac cycle. Patient 12 had substantial left-to-right intracardiac shunting (pulmonary-to-systemic flow ratio of 2.1 by magnetic resonance imaging).

Flow was calculated by multiplying the cross-sectional area of the vessel lumen by the mean blood flow velocity for each point sampled in the cardiac cycle. The cross-sectional area of the vessel lumen was defined on the magnitude image of the reference scan by a region of interest (ROI), where

This same ROI was superimposed on the velocity map for each corresponding frame of the cardiac cycle, and the mean velocity was obtained by measuring the average pixel intensity within the ROI. For each frame sampled in the cardiac cycle, F_i=flow per frame of the cardiac cycle (cm³ per frame)=mean velocity (cm/s)xarea (cm²)x2xPEG sizexTR of sequence (seconds per frame), with the TR (pulse repetition time) being multiplied by 2 because the sequence consists of a reference followed by a velocity-sensitized pulse. With prospective gating, images were not acquired during the last 30 to 80 milliseconds of diastole. For this terminal portion of the cardiac cycle, we estimated flow to be half the flow of the previously imaged frame. Thus,

where F_i equals the flow in frame i, and n equals the number of frames in the cycle plus the last interval of the cycle. By multiplying heart rate by the sum of the flow for all frames of the cardiac cycle, we determined flow per minute through the vessel.

All data, including heart rate, blood pressure, and pulmonic and aortic flows, were compiled, analyzed, and stored without knowledge of the findings during subsequent catheterization. MR images were stored on optical disks for subsequent recall and analysis. To determine the interobserver variability of analyzing the MR images, they were analyzed by two investigators who were blinded to the other's results as well as to the results of catheterization. After completion of the MRI scanning procedure, patients were transferred immediately to the catheterization laboratory.

Cardiac Catheterization
In each patient, an 8F sheath was inserted percutaneously into the femoral vein, and a cannula was placed in the femoral artery. A platinum-tipped pacing electrode was advanced to the main pulmonary artery and connected to a standard DC amplifier (Electronics for Medicine) for the recording of an electrical potential. The patient was administered a single breath of hydrogen, and the elapsed time from inhalation to the detection of an electrical potential was measured according to previously described techniques.^{21 22 23} The platinum-tipped electrode was withdrawn from the body, and an 8F Goodale-Lubin catheter was advanced to the pulmonary artery. In less than 10 minutes, multiple blood samples were obtained from the right-side heart chambers, and their oxygen saturations measured and contents calculated, after which the criteria of Dexter et al²⁴ were used to determine the location of intracardiac left-to-right shunting. Subsequently, pulmonic and systemic blood flows were quantified by using the Fick principle,^{4 6 20} and Qp/Qs was calculated.

Immediately afterward, in the patients who had hydrogen appearance times of less than 4 seconds (group 2), the Goodale-Lubin catheter was readvanced to the pulmonary artery, and 5 mg of indocyanine green was injected through the catheter as blood was withdrawn from the femoral artery through a densitometer cuvette.⁶ From the inscribed curve, shunt magnitude was quantified in accordance with the equation of Carter et al.⁵ For all the patients studied, catheterization measurements were completed within 15 to 20 minutes of one another, and no change in heart rate or systemic arterial pressure occurred during this time. The catheterization Qp/Qs value was calculated by averaging the oximetric and indocyanine green measurements.

Statistical Analysis
Without knowledge of the flow data, we excluded patients from analysis if there was a substantial change in heart rate or systemic arterial pressure between the time of MRI and invasive measurements, specifically, if (1) the patient's heart rate varied by >15% or (2) mean systemic arterial pressure varied by >20%. All data are expressed as mean±1 SD. The values for Qp/Qs obtained invasively were compared with those measured by the use of MRI with a two-variable linear regression analysis. In addition, the difference between catheterization and MRI measurements of Qp/Qs were compared using the analysis of Bland and Altman.²⁵

	Results

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MRI studies were well tolerated and completed in 22 of the 23 subjects. One patient had marked claustrophobia and was withdrawn from the magnet. In all patients, the heart rate varied by 15% (range, 0% to 15%), and mean systemic arterial pressure varied by <20% (range, 1% to 18%) during MRI and catheterization. One subject was excluded from analysis because an error in acquisition rendered the flow measurements uninterpretable. The remaining 21 subjects (15 women and 6 men; age range, 15 to 72 years) formed the study population—9 without evidence of intracardiac shunting (group 1) and 12 with intracardiac shunting (group 2). Twenty patients had normal sinus rhythm, and 1 (patient 20, group 2) had atrial fibrillation. The duration of the flow scans was 1 to 3 minutes for those in sinus rhythm. The patient with atrial fibrillation was scanned with two averaged acquisitions, thereby lengthening the flow scans to 4 to 6 minutes.

Data regarding the 21 subjects are displayed in Table 1. Table 2 summarizes the mean blood flow and Qp/Qs obtained with catheterization and MRI for all 21 patients. As displayed in Fig 3, there was a good correlation between the measurements of shunt magnitude obtained with catheterization and those obtained with MRI. Furthermore, MRI reliably determined whether Qp/Qs was <1.5 or 1.5 in all 21 subjects. The difference between Qp/Qs measured with MRI and that measured with catheterization was 0±0.3 for the patients in group 1, -0.2±0.7 for the patients in group 2, and -0.1±0.55 for all patients combined (Fig 4).

View this table: [in this window] [in a new window]   Table 1. Summary of Patient Data

View this table: [in this window] [in a new window]   Table 2. Summary of Flow Data

View larger version (70K): [in this window] [in a new window]   Figure 3. Pulmonary-to-systemic flow ratios (Qp/Qs) by catheterization (horizontal axis) and by magnetic resonance imaging (MRI) (vertical axis) for the 21 subjects. Each symbol represents the data from 1 patient. The regression line is shown. All points fall within the two shaded areas, indicating that compared with oximetry and indocyanine green, MRI correctly identified all subjects with a Qp/Qs < or 1.5.

View larger version (9K): [in this window] [in a new window]   Figure 4. The mean pulmonary-to-systemic flow ratio (Qp/Qs) by catheterization and magnetic resonance imaging (MRI) (horizontal axis) and the difference between catheterization and MRI measurements of Qp/Qs (vertical axis) for the 21 subjects. The open circles represent data from patients in group 1, whereas the triangles represent data from patients in group 2. The mean difference (solid line) and ±2 SD from this difference (dashed lines) are shown. For Qp/Qs ratios 3, there is good agreement between MRI and catheterization measurements. In patients with very large intracardiac left-to-right shunts, the level of agreement decreases, most likely due to potentially imprecise oximetric measurements of Qp when pulmonary flow is extremely high.

The interobserver variability for the MRI measurements of flow was 3±3% in the aorta and 5±3% in the pulmonary artery.

	Discussion

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In adults with left-to-right intracardiac shunting, several methods may be used to quantify shunt magnitude, including oximetry,⁴ indicator dilution,⁶ radionuclide scintigraphy,⁸ and Doppler echocardiography.⁹ Each technique has advantages and limitations. The oximetric assessment of oxygen contents or saturations in the various right-side heart chambers is relatively easy to perform and allows one to determine both shunt location and magnitude. However, it is invasive; it is insensitive for detecting small shunts; and its estimate of shunt magnitude may be somewhat imprecise in patients with large shunts.^{4 11} The indicator dilution technique requires the injection of a substance, such as indocyanine green, into a right-side heart chamber as blood is withdrawn simultaneously from a systemic artery through a densitometer cuvette. Similar to oximetry, it is invasive, and its sensitivity is only modestly better than oximetry in detecting small shunts.^{5 11} With radionuclide techniques, a pulmonic time–activity curve is obtained after the intravenous injection of a radiopharmaceutical.⁸ Although this method allows the detection of Qp/Qs as small as 1.2, it requires the injection of a radioactive isotope.¹¹ Doppler echocardiography can quantify left-to-right intracardiac shunting by measuring Qp/Qs from Doppler-derived pulmonic and aortic blood flows, by semiquantitatively assessing the size of the left-to-right color flow jet on color flow mapping, or by determining the velocities constituting the left-to-right flow jet.¹⁰ Although this technique is noninvasive, it provides only a rough estimate of shunt magnitude; adequate acoustic windows cannot be obtained in all patients; and small errors in the measurement of diameter introduce large errors into flow calculations.¹¹

MRI with spin-echo or gradient-echo techniques has been used to detect and localize atrial and ventricular septal defects with a sensitivity of 90% to 100% and a specificity of 90%.^{26 27} Although velocity-encoded, phase-difference cine MRI scans of the proximal aorta and pulmonary artery have been used to quantify the magnitude of left-to-right intracardiac shunting in patients with large intracardiac shunts,¹⁹ no previous study has assessed the usefulness of this technique in distinguishing patients with no or small intracardiac shunts from those with large shunts. Data from the present study demonstrate that MRI can rapidly and accurately quantify shunt magnitude in patients with intracardiac left-to-right shunting and, furthermore, that it can reliably differentiate those with Qp/Qs of <1.5 from those with Qp/Qs of 1.5 (Figs 3 and 4).

Several features make MRI attractive for evaluating patients suspected of having left-to-right intracardiac shunting. First, it is safe, reasonably comfortable, noninvasive, and easily performed in an outpatient setting without the need for ionizing radiation or intravascular injections. Second, single flow measurements are performed rapidly (in less than 3 minutes), thereby allowing a complete hemodynamic assessment in less than 10 minutes. Third, excellent visualization of the area and velocity profile within the proximal aorta and pulmonary artery is obtained; therefore, impediments presented by body shape and size are of little concern. Fourth, high-resolution tomographic imaging for visualizing the entire thorax can be obtained concomitant with the flow analysis. This information can be used to detect associated anomalies, such as anomalous pulmonary venous drainage or patent ductus arteriosus; to visualize intracardiac structures before and after surgical intervention; and to reconstruct three-dimensional images of the heart and great vessels in patients whose anatomy is complex.

The present study has limitations. First, most of our patients were in sinus rhythm. None had frequent ventricular ectopy, and only one had atrial fibrillation. We are uncertain whether this technique provides reliable results in patients with irregular rhythms. Second, we excluded patients with aortic or pulmonic stenosis, since they have turbulent, high-velocity flow jets in the proximal great vessels. As other investigators have suggested,²⁸ the acquisition of data in these patients may require careful alignment of the velocity-encoded slice parallel to the direction of flow and the use of very short echo times (TE of 3 to 4 milliseconds). Third, we did not enroll patients with marked pulmonic or aortic regurgitation. With our method of calculating flow in these patients, negative flow in the proximal great vessels during diastole would interfere with the determination of forward flow. Fourth, MRI did not allow discrimination of patients without shunts from those with small amounts of left-to-right shunting. The discrepancy in systemic and pulmonary artery flows in the patients with no shunting could have been caused by technical factors related to the sensitivity of the MR flow measurements.²⁹ Finally, in the patients with hydrogen appearance times of more than 4 seconds (group 1, Table 1), Qp/Qs by catheterization was assumed to be 1. In these patients, the oxygen saturation of pulmonary venous blood was not measured, and therefore, Qp could not be precisely quantified oximetrically. In addition, no prominent early recirculation was seen after injection of indocyanine green, and therefore the percentage of left-to-right shunting could not be measured by indicator dilution.

In conclusion, velocity-encoded, phase-difference cine MRI measurements of forward flow in the proximal aorta and pulmonary artery can accurately and rapidly quantify intracardiac left-to-right shunting, thereby providing a reliable, noninvasive method for determining which patients should be considered for surgical correction.

	Acknowledgments

 
This work was supported in part by a National Institutes of Health Special Center of Research grant (Ischemic SCOR grant HL-17669), the Moss Heart Fund, a grant from the Society of Cardiac Angiography and Intervention and Squibb Diagnostics, and a grant from Picker International, Inc. The authors thank Alison Russell, Dorothy Smith, and Ginny Vaughn for their assistance in preparing the figures for the manuscript and Lynn Nelson and Kay Thomas for their assistance during the MRI process.

Received October 10, 1994; revision received December 19, 1994; accepted December 21, 1994.

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