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Original Research |
1 Department of Radiology, Mayo Clinic, 4500 San Pablo Rd., Jacksonville, FL
32224.
2 Biostatistics Unit, Mayo Clinic, Jacksonville, FL 32224.
3 Division of Cardiovascular Diseases, Mayo Clinic, Jacksonville, FL
32224.
Received April 18, 2006;
accepted after revision August 1, 2006.
Address correspondence to R. S. Kuzo
(rskuzo{at}hotmail.com).
Abstract
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SUBJECTS AND METHODS. Quantitative measurements of SVC and IVC flow per R-R interval were performed on 10 healthy volunteers (six men, four women; median age, 30 years; range, 25-55 years) with a retrospectively ECG-gated velocity-encoded gradient-echo cine sequence on a 1.5-T MRI unit with axial slices at the level of the diaphragm and just below the azygous vein confluence during free breathing, continuous inspiration, breath-hold at end inspiration, Valsalva maneuver, and breath-hold at end expiration.
RESULTS. Median flow during free breathing was 38.9 mL in the SVC and 74.3 mL in the IVC, during continuous inspiration was 43.9 mL in the SVC and 113.7 mL in the IVC, during breath-hold at end inspiration was 31.0 mL in the SVC and 56.1 mL in the IVC, during a Valsalva maneuver was 28.9 mL in the SVC and 53.9 mL in the IVC, and during breath-hold at end expiration was 35.3 mL in the SVC and 61.2 mL in the IVC.
CONCLUSION. MRI measurements showed a significant increase in caval flow during inspiration and a greater relative increase in blood flow in the IVC than in the SVC. For thoracic CT performed with IV contrast enhancement, deep inspiration before scanning leads to a large influx of IVC blood that does not contain contrast medium and dilutes the contrast bolus, causing poor vascular opacification. Avoiding initial inspiration before scanning is suggested as a way to limit the transient interruption of the contrast bolus artifact.
Keywords: cardiopulmonary imaging contrast media CT angiography MRI
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Changes in intrathoracic pressure during the respiratory cycle can affect the diameter of and flow velocity in the inferior vena cava (IVC) [3-5]. An increase in unopacified venous return from the IVC during inspiration resulting in dilution of the contrast column may be an explanation for poor contrast opacification during some pulmonary CT angiographic studies [2].
Noninvasive quantitative measurement of blood flow through a vessel can be performed with velocity-encoded cine MRI [6-9]. The purpose of our observational study was to use MRI to examine changes in blood flow in the superior vena cava (SVC) and IVC during respiratory maneuvers to improve understanding of the possible effects of respiration on contrast dynamics and of transient interruption of contrast artifact on pulmonary CT angiographic studies.
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Blood flow in the SVC was measured on transaxial slices obtained at a level between the azygous confluence and the right atrium (Fig. 1). Blood flow in the IVC was measured on transaxial slices obtained at the level of the diaphragm between the right atrium and hepatic vein confluence (Fig. 2). The orientation of the slices was perpendicular to the direction of flow. For both locations, the table was repositioned so that the slice level was within 3 cm of isocenter.
For the baseline free-breathing measurements, a non-breath-hold retrospectively gated sequence was used with the following parameters: TR/TE, 42.0/3.3; matrix size, 192 x 256; flip angle, 30°; number of segments, three; number of signals averaged, three; slice thickness, 6 mm; velocity encoding, 100 cm/s; average scan duration, 2 minutes 56 seconds to ensure adequate sampling of the entire respiratory cycle. For the respiratory maneuver measurements, the breath-hold retrospectively gated imaging sequence parameters were 74.0/2.8; matrix size, 96 x 256; flip angle, 30°; number of segments, 6; number of signals averaged,1; slice thickness, 6 mm; velocity encoding, 100 cm/s. The data were acquired over 16 cardiac cycles, and each measurement lasted approximately 12-16 seconds depending on the subject's heart rate. These sequences provided both phase and magnitude images. If aliasing was observed on the images, the measurement was repeated with velocity encoding of 150 cm/s.
Each measurement was performed twice, and the average of the two measurements was used to represent venous blood flow during each respiratory maneuver at each anatomic location. To allow hemodynamic equilibration after each respiratory maneuver, 2 minutes was allowed before each new measurement.
Image Analysis
The images were sent to an independent workstation (Leonardo, Siemens
Medical Solutions), and flow measurement data were obtained with commercially
available software (Argus, Siemens Medical Solutions). A region of interest
was drawn manually on one image with visible flow and then propagated across
all of the phases. The region of interest was then manually corrected on each
phase to account for changes in vessel position and contour during the cardiac
cycle.
Statistical Analysis
Numeric data were summarized with the sample median and range. A paired
Student's t test was used to make all pairwise comparisons in blood
flow between the stages of breathing. For comparisons of blood flow at more
than two stages of breathing, a mixed-effects model was used with a fixed
effect included for stage of breathing and a random effect included for
patient. The following comparisons were considered: total systemic venous
return during free breathing was compared with the total systemic venous
return during the other four respiratory maneuvers; blood flow in the SVC and
IVC at baseline was compared with blood flow in the SVC and IVC during the
other four respiratory maneuvers; changes in blood flow from baseline to the
other four respiratory maneuvers, expressed both as a difference and as a
ratio, were compared between the SVC and the IVC; ratio between blood flow in
the IVC and blood flow in the SVC at baseline was compared with the IVC to SVC
blood flow ratio during the other four respiratory maneuvers. To partially
account for the number of tests performed, only p <0.01 was
considered statistically significant.
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Changes in Blood Flow Between SVC and IVC
Table 2 shows the changes in
blood flow from baseline to the other four respiratory maneuvers represented
as both differences and as ratios for the SVC and the IVC. The increase in
blood flow from baseline to continuous inspiration was higher (p <
0.001) in the IVC than in the SVC. The ratio of blood flow during continuous
inspiration to blood flow during baseline was higher for the IVC than for the
SVC (p = 0.009).
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Ratio Between Blood Flow in the IVC and Blood Flow in the SVC
Table 3 shows the IVC to SVC
blood flow ratio for different respiratory maneuvers. IVC to SVC blood flow
ratio was higher (p = 0.009) than at baseline during continuous
inspiration and lower than at baseline during the Valsalva maneuver
(p = 0.008). A trend toward lower IVC to SVC blood flow ratio during
breath-hold at end inspiration than during baseline was not statistically
significant (p = 0.016).
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Pulmonary CT angiograms are typically obtained with one or more preparatory breaths and then a deep inspiration a few seconds after injection of contrast medium has begun, just before image acquisition begins. The blood volume with a lesser concentration of contrast medium produced by these initial deep inspirations travels to the pulmonary arteries by the time scans at the level of the pulmonary arteries are acquired resulting in the observed decrease in pulmonary artery opacification while opacification in the right atrium and aorta may be satisfactory.
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The breath-hold at end inspiration and the end-expiration maneuvers were included because they correspond with verbal instructions that typically are given to patients for routine clinical CT examinations, such as "take a deep breath in and hold it" and "breath out and hold your breath out." Our study subjects were all medical professionals who understood the concept and performance of the Valsalva maneuver. The Valsalva maneuver produced the greatest decrease in venous return and therefore would be expected to result in the best contrast opacification of the pulmonary arteries. It would be difficult, however, for most patients to sustain a Valsalva maneuver for the entire length of a pulmonary CT angiogram, from the beginning of contrast injection to completion of the scan.
The small number of study subjects limited the power of our study. Our findings in healthy volunteers may not apply to patients with elevated right atrial pressure, such as patients with tricuspid disease, pericardial disease, or pulmonary hypertension. The extent of changes in venous flow during respiratory maneuvers varies with respiratory effort, but we did not use a spirometer to quantify or normalize for the respiratory effort. The MR sequence we used gave an average of flow over several cardiac cycles and did not provide instantaneous, real-time measurements. To generate negative intrathoracic pressure continuously for the length of the acquisition for the inspiration measurements, study subjects were asked to breath in slowly against resistance. This maneuver may not accurately simulate the physiologic mechanism of the initial inspiration before thoracic CT scans.
The results of our velocity-encoded MRI study of blood flow in the SVC and IVC during different respiratory maneuvers support the hypothesis that dilution of contrast material resulting from a greater increase in blood flow in the IVC than in the SVC during inspiration can cause transient interruption of the contrast bolus on pulmonary CT angiograms. On the basis of these findings, we recommend that pulmonary CT angiography be performed with only a small inspiration or no inspiration before scanning. Deep inspiration immediately before scanning should be avoided. If the transient interruption of contrast artifact is recognized by the technologist at the time of the examination, the examination can be repeated with no inspiration (Fig. 4A, 4B) to improve opacification of the pulmonary artery.
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