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DOI:10.2214/AJR.04.1738
AJR 2006; 187:439-444
© American Roentgen Ray Society

Original Research

MRI Measurement of the Hemodynamics of the Pulmonary and Systemic Arterial Circulation: Influence of Breathing Maneuvers

Sebastian Ley1,2, Christian Fink1,3, Michael Puderbach1, Julia Zaporozhan1, Christian Plathow1,4, Monika Eichinger1, Waldemar Hosch5, Karl-Friedrich Kreitner6 and Hans-Ulrich Kauczor1

1 Department of Radiology (E010), German Cancer Research Center, (DKFZ), Im Neuenheimer Feld 280, 69120 Heidelberg, Germany.
2 Department of Pediatric Radiology, University Hospital Heidelberg, In Neuenheimer Feld 153, 69120 Heidelberg, Germany.
3 Department of Clinical Radiology, University Medical Center Grosshadern, Ludwigs-Maximilians-University Munich, Germany.
4 Department of Radiology, University Tuebingen, Hoppe-Seyler-Strasse 3, 72076 Tuebingen, Germany.
5 Department of Radiology, University Hospital Heidelberg, Im Neuenheimer Feld 110, 69120 Heidelberg, Germany.
6 Department of Radiology, University Hospital Mainz, Langenbeckstrasse 1, 55131 Mainz, Germany.

Received November 10, 2004; accepted after revision May 29, 2005.

 
Supported by German National Research Agency (DFG) (FOR 474).

Address correspondence to S. Ley (ley{at}gmx.de).


Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to use phase-contrast MRI to evaluate the influence of various breathing maneuvers on the hemodynamics of the pulmonary and systemic arterial circulation.

SUBJECTS AND METHODS. Twenty-five volunteers were examined with phase-contrast MRI. Flow measurements were acquired in the aorta, pulmonary trunk, and left and right pulmonary arteries during deep, large-volume inspiratory breath-hold, expiratory breath-hold, and smooth respiration (no breath-hold). Parameters assessed were peak velocity, blood flow, velocity gradient, and acceleration time.

RESULTS. Pulmonary blood flow and peak velocity were significantly reduced during inspiratory breath-hold and expiratory breath-hold compared with no breath-hold (p < 0.01). Pulmonary velocity gradient in inspiratory breath-hold was significantly (p ≤ 0.01) lower than in expiratory breath-hold and no breath-hold. There was no difference in velocity gradient between expiratory breath-hold and no breath-hold. Peak velocity in the aorta was lowest with no breath-hold. Velocity gradient was highest in expiratory breath-hold, and no breath-hold had the smallest SD. Acceleration time in the pulmonary trunk showed no difference between inspiratory breath-hold, expiratory breath-hold, and no breath-hold. Blood flow distribution to the left (45-47%) and to the right (53-55%) lung was not influenced by breathing maneuver.

CONCLUSION. Measurements during smooth respiration showed the smallest SD. Therefore, no-breath-hold measurements should be considered for assessment of hemodynamics in clinical practice.

Keywords: blood flow • hemodynamics • phase-contrast MRI • pulmonary circulation • systemic circulation


Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Pulmonary blood flow and right ventricular function are impaired in many diseases, such as primary and secondary pulmonary hypertension, pulmonary embolism, and fibrosis [1]. Echocardiography has been used most often for evaluation of right and left ventricular function. However, the acoustic window is often reduced, and sidewise evaluation of blood flow to the right and left pulmonary arteries is not possible with echocardiography. MRI is gaining ground in the diagnostic evaluation of pulmonary parenchymal and vascular disease. The method of choice for precise MRI assessment of blood flow and velocity is phase-contrast flow measurement [2, 3]. The technique is easily performed in the large pulmonary and systemic vessels, and acquisition time is short. It has been shown that noninvasive velocity profiles of the right ventricular outflow tract, assessed with pulsed Doppler technique, correlate with invasively measured mean pulmonary arterial pressure [4]. Phase-contrast flow measurements in MRI are most often obtained with no breath-hold for a rather long acquisition time of 3-4 minutes [5]. Short acquisition times of 20-30 seconds can be achieved only during inspiratory or expiratory breath-hold. Pulmonary arterial blood flow has been reported to be significantly reduced during inspiration [6], but the effect during expiration is not known. The effect of either type of breath-hold on bronchosystemic shunting is unknown. The aim of this study was to evaluate the influence of various breathing maneuvers on pulmonary arterial and systemic blood flow and velocity.


Subjects and Methods
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Twenty-five volunteers (8 women, 16 men; mean age, 27.9 ± 8 years [range, 20-55 years]) with no history of cardiovascular disease were examined with whole-body 1.5-T MRI (Magnetom Symphony, Siemens Medical Solutions) after approval by our local ethics committee. Before examination, informed consent was obtained from each volunteer. Mean body weight was 73.3 ± 8.5 kg, and mean height was 179.1 ± 8.1 cm. The calculated body mass index was 18 ± 3 (range, 23-31).


Figure 1
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  		Fig. 1A —Blood flow in ascending aorta. Box plot diagrams show peak velocity (A) and absolute blood flow (B).

 


Figure 2
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  		Fig. 1B —Blood flow in ascending aorta. Box plot diagrams show peak velocity (A) and absolute blood flow (B).

 
Phase-contrast flow measurements were perpendicular to the ascending aorta, pulmonary trunk, and left and right pulmonary arteries. All measurements were obtained during deep inspiration (inspiratory breath-hold) and expiration (expiratory breath-hold at the level of end tidal exhalation) and smooth respiration (quiet breathing; no breath-hold). Sequence parameters for breath-hold acquisition were as follows: 2D fast low-angle shot; TR/TE, 37/3.2; slice thickness, 6 mm; segmentation factor, 5; receiver bandwidth, 698 Hz/pixel; number of acquisitions, 1; flip angle, 40°. For no-breath-hold acquisition the following parameters were used: 2D fast low-angle shot; 25/3.2; slice thickness, 6 mm; segmentation factor, 3; receiver bandwidth, 698 Hz/pixel; number of acquisitions, 3; flip angle, 40°. In all cases a matrix of 115 x 256 was used, resulting in spatial resolution of 2.1 x 1.3 x 6 mm. Both sequences were through-plane flow measurements with a Maxwell correction for flow and were prospectively gated by the scanner integrated optical decoupled ECG gating unit. The temporal resolution for breath-hold measurements was 37 milliseconds and for no-breath-hold acquisition was 25 milliseconds. No interpolation of time frames was done. A six-channel surface coil was used for signal detection.

For positioning the flow measurements perpendicular to the vessels, three to five true fast imaging with steady-state free precession localizers images were acquired in inspiratory breath-hold and expiratory breath-hold. For no-breath-hold acquisition, a mean slice orientation between the two extremes was chosen. For evaluation of flow measurements, the software Flow Quantification (part of Argus, version VA50C [Siemens Medical Solutions]) was used. Each vessel was outlined manually by an experienced observer. The following hemodynamic parameters were assessed and compared: peak velocity in centimeters per second, average blood flow in liters per minute, velocity gradient, and acceleration time in milliseconds.

Unless specified, data are presented as mean ± SD. For statistical analysis, Wilcoxon's signed-ranked test (SPSS for Windows, version 11.5) was used. A p value < 0.05 was considered statistically significant. For this type of data, nonparametric statistical analysis is preferred over the usual t test because the number of data in each case is not large enough to ensure reliability of the t test.


Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Acquisition times for inspiratory and expiratory breath-hold measurements were 20-25 seconds, depending on the subject's heart rate. The mean R-R interval during acquisition of the phase-contrast MR images in the pulmonary trunk was 931.5 ± 11.5 milliseconds; in the ascending aorta, 925.8 ± 9.8 milliseconds; in the right pulmonary artery, 925.6 ± 24.0 milliseconds; and in the left pulmonary artery, 916.1 ± 21.6 milliseconds.

The peak velocity in the ascending aorta during inspiratory breath-hold was 115.1 cm/s. During expiratory breath-hold it was 121.9 cm/s, and during no breath-hold it was 113.0 cm/s (Fig. 1A). Measurements between expiratory breath-hold and no breath-hold were significantly different (p = 0.001). The absolute blood flow in the ascending aorta was significantly different during expiratory breath-hold (6.2 L/min; p < 0.001) and no breath-hold (6.3 L/min; p < 0.001) compared with inspiratory breath-hold (5.3 L/min) (Fig. 1B). The velocity gradient was significantly different between inspiratory breath-hold (0.9) and expiratory breath-hold (1.2; p < 0.03) and not different for no breath-hold (1.0, p =0.4). A significant difference was found between expiratory breath-hold and no breath-hold (p = 0.01). The acceleration time in the ascending aorta was not statistically different for inspiratory breath-hold (119 milliseconds), expiratory breath-hold (110 milliseconds), or no breath-hold (116 milliseconds).

Peak velocity in the pulmonary trunk was significantly higher during expiration (86.6 cm/s) than during inspiration (74.3 cm/s; p < 0.001) and smooth respiration (83.0 cm/s; p = 0.01) (Fig. 2A). A significant difference also was found for inspiratory breath-hold and no breath-hold (p < 0.001). Absolute blood flow during inspiration (4.8 L/min) was significantly lower than during expiration (6.1 L/min; p < 0.001) and smooth respiration (6.4 L/min; p < 0.001) (Fig. 2B). A significant difference was seen between expiration and smooth respiration (p = 0.02).


Figure 3
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  		Fig. 2A —Blood flow in pulmonary trunk. Box plot diagrams show peak velocity (A) and absolute blood flow (B).

 

Figure 4
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  		Fig. 2B —Blood flow in pulmonary trunk. Box plot diagrams show peak velocity (A) and absolute blood flow (B).

 
The velocity gradient in the pulmonary trunk was significantly lower during inspiration than during expiration (0.7; p = 0.002) and smooth respiration (0.6; p = 0.01). No difference was seen between expiration and smooth respiration (p = 0.08). The acceleration time in the pulmonary trunk showed no statistical difference between smooth respiration (153 milliseconds), expiration (145 milliseconds), and inspiration (151 milliseconds; p = 0.04).

The results for the right and left pulmonary arteries showed the same behavior as for the pulmonary trunk and are summarized in Tables 1, 2, 3. Table 4 shows the results of statistical analysis of all measurements. Absolute blood flow in the systemic and pulmonary arterial circulation was significantly different during inspiratory breath-hold (5.3 L/min vs 4.8 L/min; p < 0.001). No difference was seen in blood flow during expiratory breath-hold (6.2 L/min vs 6.1 L/min; p = 0.3) and no breath-hold (6.3 L/min vs 6.4 L/min; p = 0.3). The sum of absolute blood flow in the right and left pulmonary arteries compared with absolute blood flow in the pulmonary trunk showed excellent linear correlation in all maneuvers (r = 0.8-0.9), but the absolute values were significantly different for inspiratory breath-hold (p < 0.001) (Table 5).


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  		TABLE 1: Hemodynamic Parameters Measured During Inspiratory Breath-Hold

 

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  		TABLE 2: Hemodynamic Parameters Measured During Expiratory Breath-Hold

 

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  		TABLE 3: Hemodynamic Parameters Measured During No Breath-Hold (Smooth Respiration)

 

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  		TABLE 4: Statistical Analysis of Variables and Breathing Maneuvers

 

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  		TABLE 5: Absolute Blood Flow in Pulmonary Trunk and Sum of Absolute Blood Flow of Right and Left Pulmonary Arteries

 


Discussion
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
We found that in accordance with results of previous studies, hemodynamic parameters depended on breathing conditions during acquisition of images. The systemic circulation showed significant reduction of absolute blood flow during inspiratory breath-hold, whereas peak velocity did not change significantly. The pulmonary arterial circulation showed a significant difference between the different methods of acquisition. Peak velocity was highest in expiratory breath-hold with a significant difference between all maneuvers. However, the velocity gradient was significantly higher during expiratory breath-hold and no breath-hold than during inspiratory breath-hold. There was a significant difference in absolute blood flow in the systemic and pulmonary arterial system during inspiration, but there was no difference in expiration and no breath-hold. Although blood flow measurements in the pulmonary trunk, compared with the sum of flow in the right and left pulmonary arteries, showed good linear correlation, during inspiratory breath-hold the absolute numbers were significantly different.

MR flow measurements have become a reliable clinical tool for noninvasive assessment of blood flow. The range of applications covers large and small vessels down to the size of the coronary arteries. Even slow flow of CSF in small anatomic structures such as the foramen magnum can be assessed with high accuracy [7]. It also has been shown that the segmentation factor of the sequence used has no effect on the absolute numbers of the measurements [8]. Systemic and pulmonary arterial blood flow measurements usually are obtained in smooth respiration. Velocity measurements in the pulmonary trunk are used for assessment of pulmonary arterial pressure, for example, in pulmonary hypertension [9, 10]. MR phase-contrast flow measurements most often correlate either with short-axis cine MR measurements of the right and left ventricles [11] or with echocardiographic findings [12]. However, because cine MR short-axis acquisitions are performed during breath-hold, the flow measurements compared were also obtained in breath-hold. The standard procedure for assessment of hemodynamics is invasive right-heart catheterization, which is performed during smooth respiration.

Reduction of cardiac output at deep inspiration can be explained by decreased venous return to the heart. The most important effect of breath-hold on cardiac performance is the difference in intrathoracic pressure. Using impedance cardiography, Ferrigno et al. [13] measured cardiac output and intrathoracic pressure in six healthy volunteers and found a 24% decrease in cardiac index with breath-hold at large lung volumes produced by breath-hold as the result of increased intrathoracic pressure and decreased venous return. In another study [14], flow in the superior vena cava decreased 11% during inspiratory breath-hold compared with no breath-hold. These measurements were reproduced and expanded to the inferior vena cava [15]. During Valsalva maneuver, blood flow decreased 16% in the superior vena cava and 28% in the inferior vena cava compared with smooth breathing. The sequence used was a gradient echo velocity-encoded technique with an acquisition time of approximately 15 seconds. Together with the findings of the study in which volunteers were not asked specifically to perform a Valsalva maneuver, it can be assumed that this breath-hold pattern is produced automatically by patients. Young patients with the capability to inspire deeply are affected more than older patients with less deep inspiration. However, to our knowledge there have been no reports of evaluations of this possible age dependency.

In another study, flow in the pulmonary trunk was 4.5 L/min during inspiratory breath-hold [6]. This value is 7% less than the volume of 4.8 L/min measured in our study. This difference may be due to the effect found among volunteers in a study by Sakuma et al. [6] who inspired more deeply (larger inspiratory volume) than the volunteers in our study, further reducing venous return. Both studies showed a significant increase in pulmonary arterial and systemic blood flow during normal respiration. The difference between the two studies is only 2% (Sakuma et al., 6.5 L/min; our study, 6.4 L/min). This observation emphasizes that quantitative measurements of blood flow are most reproducible during normal respiration. The results of this study for no-breath-hold acquisition were very similar to those of Mousseaux et al. [16] (6.65 L/min for pulmonary arterial system and 6.37 L/min for the systemic circulation). The influence of breathing on left ventricular stroke volume, even during normal respiration, has been documented with real-time MR flow measurements [17]. However, no further data have been supplied, especially regarding the pulmonary circulation and peak velocity.

We found a significant difference in pulmonary arterial blood flow between expiratory breath-hold and no breath-hold, with a higher (5%) flow for no breath-hold. This finding may have been caused by a slight increase in intrathoracic pressure during expiratory breath-hold that reduces venous return.

The difference in blood flow in the systemic and pulmonary arterial systems was largest (0.5 L/min) in inspiratory breath-hold. Expiratory breath-hold (0.1 L/min) and no breath-hold (0.1 L/min) had a smaller difference. This finding may have been the result of more precise measurement. Another cause may have been physiologic bronchosystemic shunting. However, this was a new finding, and a tailored examination is needed.

As shown by Henk et al. [18], there is slightly more blood flow to the right lung (55% of total pulmonary blood flow) than to the left lung (45%). This observation was confirmed in our study. The blood flow distribution to the left and the right lungs remained constant during all acquisition conditions (Table 6). This finding may indicate that blood flow distribution is constant and stable if there is no underlying disease of the lung parenchyma. For evaluation of a shift of blood flow distribution in disease, data can be acquired regardless of the breathing maneuver.


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  		TABLE 6: Distribution of Average Blood Flow to the Right and Left Lungs

 

Peak velocity in the systemic circulation was in the range of 115-121 cm/s and showed statistical difference between expiratory breath-hold and no breath-hold. However, no-breath-hold acquisition exhibited the smallest SD. The data for the pulmonary circulation showed a slight but significant peak during expiration. The SD of the measurements was smallest in inspiration, and expiratory measurements showed the largest variation. To determine which measurement method is the most accurate, further investigations and correlation with invasive measurements are mandatory.

The velocity gradient in the systemic circulation was highest during expiration, and there was no significant difference between inspiration and smooth respiration. The SD was smallest, however, during smooth respiration, indicating that those measurements are most stable. A similar situation occurs for the pulmonary circulation. The velocity gradient of no-breath-hold acquisition ranges between the two others but with the smallest SD.

The acceleration time of the blood in the pulmonary and systemic systems during no-breath-hold acquisition with a temporal resolution of 24 milliseconds was described by Mousseaux et al. [16]. Those authors found an acceleration time of 134 milliseconds for the pulmonary system, which is in the range of the values found in this study (mean, 151 milliseconds). The ascending aorta, however, showed an acceleration time of 89 milliseconds in the study by Mousseaux et al., whereas we found a time of 116 milliseconds. We found a value of 110 milliseconds during expiration. Because of the temporal resolution of the sequences used, these values differ by only one time frame, although the absolute numbers are quite different. Although we did not find a statistically significant difference, the acceleration time was markedly increased during inspiration. Thus, we do not advise acquiring this parameter in inspiration for estimation of pressure in the pulmonary circulation.

Another clinical condition in which the results of this study can be used is CT angiography of the pulmonary vasculature or the aorta. It is a known problem that during inspiration in CT angiography the bolus of contrast medium is either delayed or spread out [15]. It may be possible to avoid this phenomenon by performing the studies during expiratory breath-hold.

A limitation of this study was that the results were based on data on a small number of volunteers. Furthermore, as shown by Laffon et al. [19], the absolute numbers are age-dependent. Thus, for each group of patients with any type of disease, an age- and body mass index-matched control group should be evaluated.

In conclusion, measurements during inspiratory breath-hold lead to significant reduction in all hemodynamic parameters in the pulmonary circulation. The systemic circulation was impaired the same way. The smallest variation of measurements was found during no-breath-hold acquisition, indicating that this method is rather robust and should be used as an MRI reference method. In addition, blood flow distribution to the left and right lungs was not influenced by breathing maneuvers.


Acknowledgments
 
We thank Susanne Yubai and Kathleen Knauer for their help in performing and evaluating the examinations. This work contains parts of the doctoral thesis of Gunnar Pfingsten.


References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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