DOI:10.2214/AJR.06.5035
AJR 2007; 188:839-842
© American Roentgen Ray Society
Measurement of Caval Blood Flow with MRI During Respiratory Maneuvers: Implications for Vascular Contrast Opacification on Pulmonary CT Angiographic Studies
Ronald S. Kuzo1,
Robert A. Pooley1,
Julia E. Crook2,
Michael G. Heckman2 and
Thomas C. Gerber1,3
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
OBJECTIVE. Transient interruption of the contrast bolus has been
described as a physiologic artifact that can sometimes result in poor
opacification of the pulmonary arteries on pulmonary CT angiographic studies.
To better understand the mechanism underlying this artifact, we used
velocity-encoded cine MRI to measure flow in the inferior vena cava (IVC) and
superior vena cava (SVC) during respiratory maneuvers.
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
Introduction
For CT angiographic studies, optimal contrast opacification of the
vasculature depends on several factors, including injection delay and
duration, scan duration, injection rate, total volume of contrast medium
administered [1], and
concentration or iodine content of the contrast medium. Poor contrast
opacification can result in an examination that does not yield enough
information for diagnosis or lead to misdiagnosis. Optimal opacification of
the pulmonary arteries is necessary for confident CT evaluation of pulmonary
emboli. In 37% of CT pulmonary angiograms, however, varying degrees of a
transient decrease in pulmonary artery opacification can occur during scanning
[2] despite use of a contrast
injection rate and scan delay that should have been sufficient. This transient
interruption of contrast enhancement has been described as a physiologic
artifact associated with initial inspiration immediately before the scan.
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.
Subjects and Methods
Study Subjects
Ten healthy subjects (six men, four women) with no history or symptoms of
heart disease participated in the study. Their median age was 30 years (range,
25-55 years). The study was approved by the institutional review board, and
informed consent was obtained from the subjects. Blood flow in the SVC and IVC
was measured in each subject during five respiratory maneuvers: free breathing
(baseline), continuous inspiration, breath-hold at end inspiration, Valsalva
maneuver, and breath-hold at end expiration. To perform the Valsalva maneuver,
the subjects were instructed to perform a forced expiration against a closed
glottis. To prolong continuous inspiration for the duration of MRI data
acquisition, the subjects were instructed to hold their lips loosely apposed
and to breathe in continuously against this resistance. The respiratory
maneuvers were practiced outside of the MRI unit before the MRI
examination.
Velocity-Encoded Cine MRI
Quantitative measurements of blood flow in the SVC and IVC per cardiac
cycle were performed with a retrospectively ECG-gated, velocity-encoded cine
gradient-echo sequence on a 1.5-T MRI unit (Espree, Siemens Medical Solutions)
with a phased-array torso coil.
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.
Results
Total Systemic Venous Return
Table 1 shows systemic
venous return during the five respiratory maneuvers. Total systemic venous
return was higher (p < 0.001) than at baseline during continuous
inspiration and was lower than at baseline during the Valsalva maneuver
(p = 0.007) and during breath-hold at end inspiration (p =
0.003).
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Fig. 3 —Graph shows blood flow measured with velocity-encoded MRI in
superior vena cava (black bars) and inferior vena cava (white
bars) during respiratory maneuvers in 10 healthy volunteers. Asterisks
indicate p < 0.01 versus baseline (free breathing).
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Blood Flow in the SVC and IVC
Figure 3 shows blood flow in
the SVC and the IVC during the five respiratory maneuvers. Blood flow in the
SVC was higher during continuous inspiration than at baseline (p
<0.001). Blood flow in the IVC was higher (p < 0.001) than at
baseline during continuous inspiration and lower (p = 0.004) than at
baseline during the Valsalva maneuver. A trend toward lower blood flow in the
IVC during breath-hold at end inspiration than during baseline was not
statistically significant (p = 0.026).
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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TABLE 2: Changes in Blood Flow from Baseline to Other Respiratory Maneuvers
Between Superior and Inferior Venae Cavae
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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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TABLE 3: Ratio of Blood Flow in the Inferior Vena Cava (IVC) to Blood Flow in the
Superior Vena Cava (SVC) During Respiratory Maneuvers
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Discussion
In this study we used MRI for noninvasive evaluation of the manner in which
the SVC and IVC contributions to systemic venous return to the thorax vary
with different respiratory maneuvers. When intrathoracic pressure remains
constant, as during breath-holds at end inspiration and end expiration, the
IVC to SVC flow ratio is very similar to that during free breathing, the ratio
of IVC flow to SVC flow being approximately 2:1. During continuous
inspiration, however, intrathoracic pressure becomes negative. This change in
pressure gradient increased venous return to the right atrium nearly 50%
according to our measurements. The percentage increase in IVC flow during
inspiration is significantly greater than the increase in SVC flow. Therefore
the contribution of IVC flow to total systemic venous return is transiently
greater during inspiration, the IVC to SVC flow ratio being 2.4:1 according to
our measurements. Because contrast material is almost always administered
through an arm vein, this relative increase in unopacified blood from the IVC
dilutes contrast medium injected at a constant rate.
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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Fig. 4A —42-year-old man with anxiety and dyspnea. Initial pulmonary CT
angiogram obtained with deep prescan inspiration shows poor pulmonary artery
opacification but dense contrast enhancement in superior vena cava and aorta
consistent with transient interruption of contrast artifact.
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Fig. 4B —42-year-old man with anxiety and dyspnea. Pulmonary CT angiogram
obtained 5 minutes after A with same contrast injection volume, rate,
and timing delay but in expiration with no preliminary inspiration shows
opacification of pulmonary artery is markedly better than in A.
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Individual variation in the manner in which patients follow breathing
instructions and the forcefulness of their inspiratory effort may explain why
this artifact is seen on some but not all pulmonary CT angiograms. For
example, in two of our subjects, inspiratory IVC flow increased only 15%, but
in one subject it increased 140%. The physiologic reason for this relative
increase in IVC flow is not explained by our results. A possible mechanism may
be that diaphragmatic descent during inspiration increases intraabdominal
pressure [10]. With positive
intraabdominal pressure and negative intrathoracic pressure, the greater
pressure gradient along the IVC than along the SVC results in greater
augmentation of IVC flow.
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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Abstract
Introduction
