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Published online before print February 28, 2003, 10.1148/radiol.2271011415
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(Radiology 2003;227:283-288.)
© RSNA, 2003

Technical Developments

Coronary MR Angiography: True FISP Imaging Improved by Prolonging Breath Holds with Preoxygenation in Healthy Volunteers1

Richard M. McCarthy, MD, Steven M. Shea, MS, Vibhas S. Deshpande, MS, Jordin D. Green, MS, F. Scott Pereles, MD, James C. Carr, MD, J. Paul Finn, MD and Debiao Li, PhD

1 From the Departments of Radiology (R.M.M., S.M.S., V.S.D., J.D.G., F.S.P., J.C.C., J.P.F., D.L.) and Biomedical Engineering (S.M.S., V.S.D., J.D.G., D.L.), Northwestern University Medical School, Suite 700, 448 E Ontario St, Chicago, IL 60611. Received August 22, 2001; revision requested October 11; final revision received August 6, 2002; accepted August 20. Supported in part by grant HL 38698 from the National Institutes of Health and by Siemens Medical Solutions, Erlangen, Germany. Address correspondence to D.L. (e-mail: d-li2@northwestern.edu).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 Results
 DISCUSSION
 REFERENCES
 
In 15 healthy volunteers undergoing coronary magnetic resonance (MR) angiography, the breath-hold duration with and without preoxygenation was measured. The effect of preoxygenation on coronary artery imaging was also evaluated. A three-dimensional magnetization-prepared true fast imaging with steady-state precession sequence was employed for coronary MR angiography. All subjects showed an increase in comfortable breath-hold duration with preoxygenation. This extra imaging time allowed coronary artery imaging with increased spatial resolution.

© RSNA, 2003

Index terms: Coronary vessels, MR, 54.12142, 54.121416 • Magnetic resonance (MR), pulse sequences, 54.12142, 54.121416 • Magnetic resonance (MR), rapid imaging, 54.12142, 54.121416 • Magnetic resonance (MR), vascular studies, 54.12142, 54.121416


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 Results
 DISCUSSION
 REFERENCES
 
There are two main approaches to eliminating respiratory motion in coronary artery magnetic resonance (MR) angiography. One involves the use of a navigator echo technique in which the subject breathes freely during image acquisition, and respiratory motion is compensated for by monitoring diaphragmatic motion with or without section correction (1–4). The second approach is to perform imaging during suspended respiration—a breath-hold approach (5,6).

True fast imaging with steady-state precession (FISP) (7) is an MR imaging sequence that recently has gained wide acceptance in cardiovascular imaging (8–10). The combination of electrocardiographically triggered, magnetization-prepared, segmented three-dimensional (3D) true FISP imaging and a breath-hold volume-targeted approach (6) has recently been described for coronary MR angiography (11). This technique produces images with inherently high signal-to-noise ratio (SNR). However, the spatial resolution of the images acquired with 3D breath-hold true FISP is still limited by the duration of the breath hold. It has been shown previously that breathing oxygen before a breath hold prolongs the duration of voluntary apnea (12–14). Preoxygenation has recently been shown to prolong breath holds and improve electron-beam tomography of coronary artery bypass grafts (15). The purpose of our study was to investigate whether preoxygenation would increase breath-hold duration during coronary MR angiography and whether this increased imaging time could be used to increase spatial resolution while maintaining acceptable image SNR with 3D true FISP.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
Results
 DISCUSSION
 REFERENCES
 
Fifteen healthy volunteers with no known cardiac or respiratory disease were enrolled in the study. The study protocol was approved by our institutional review board. Each subject gave written informed consent and was checked for contraindications to MR imaging. Three of the original 15 subjects subsequently were excluded from future analysis: one because of unexpected claustrophobia, one because of an inability to tolerate the flow of oxygen, and one because of a technical problem with the oxygen apparatus. The 12 subjects who satisfactorily completed the study included nine men and three women (mean age, 31.6 years; range, 23–49 years).

Oxygen was administered via nasal cannula connected with plastic tubing to a cylinder of standard medical oxygen outside the imaging room. For the postoxygen images, oxygen was administered at a rate of 4 L/min for 2 minutes before the commencement of imaging. Because hyperventilation has been reported to be associated with coronary artery spasm, the subjects were instructed not to hyperventilate and were asked to breathe in through the nose and out through the mouth at a normal rate during oxygen administration (15,16). They were then instructed to hold their breath at maximum inspiration.

For each subject, the maximum comfortable breath-hold time with room air and after oxygenation was determined by acquiring real-time timing images of the diaphragm during breath holds and visually inspecting the position of the diaphragm for obvious motion during dynamic display of the images. The heart rate of the subject was noted at 10-second intervals during the timing series. Coronary MR angiograms were then planned with parameters adjusted to take advantage of the time available for both room-air and postoxygen breath holds. The acquisition time of the coronary MR angiograms was designed to last for approximately 80% of the maximum breath-hold duration for both room-air and postoxygen images in order to allow for any variability in the breath-hold times. To limit the total imaging time per subject, we decided to concentrate on imaging the left main and left anterior descending coronary arteries, although the right coronary artery was also imaged in some subjects. Participants were also asked to grade the subjective difficulty of the breath hold with room-air and with oxygen by using the following scale: 1, very difficult; 2, difficult; 3, easy; or 4, very easy.

The MR imaging examinations were performed with a 1.5-T whole-body imager (Magnetom Sonata; Siemens Medical Solutions, Erlangen, Germany) with a high-performance gradient subsystem (maximum gradient strength, 40 mT/m; maximum gradient slew rate, 200 mT/m/sec). The breath-hold timing images were acquired in a coronal plane with two-dimensional true FISP (TrueFISP; Siemens Medical Solutions). Imaging parameters were as follows: 3.9/2.0 (repetition time msec/echo time msec); flip angle, 50°; field of view, 400 x 400 mm2; data acquisition matrix size, 128 x 256 (phase encoding by frequency encoding); readout bandwidth, 465 Hz/pixel; section thickness, 6 mm; and temporal resolution of images, approximately 500 msec.

An electrocardiographically triggered, magnetization-prepared, segmented 3D true FISP sequence with fat saturation was used to image the coronary arteries (11). One or more overlapping 3D true FISP localizer images were first acquired in a transverse plane at the level of the left main coronary artery. The parameters for the images were as follows: 2.7/1.0; flip angle, 70°; field of view, 255 x 300 mm2; data acquisition matrix size, 90 x 256; number of lines acquired per heartbeat, 45; and readout bandwidth, 980 Hz/pixel. Asymmetric sampling was employed to reduce repetition time, with the echo center occurring at the 48th point in a 256-point readout period. A total of 12 partitions (interpolated to 24) were acquired with a slab thickness of 60 mm. The breath-hold time was 24 cardiac cycles.

With the localizer images, a three-point tool was used to prescribe a 3D volume for coronary artery imaging, which had the following constant parameters: 3.4/1.3; flip angle, 70°; and readout bandwidth, 650 Hz/pixel. The remaining parameters varied considerably among the subjects because the parameters were adjusted to take full advantage of the available breath-hold time to improve resolution and volume coverage. The number of lines collected per heartbeat varied depending on the heart rate. However, for the same subject, the number of lines per cardiac cycle and the spatial coverage in the section-select direction remained the same for pre- and postoxygen images.

The image voxel size and SNR were compared between room-air and oxygen breath holds. For SNR assessment, the blood signal was measured in a region of interest manually drawn on the console of the imager by one of the authors (R.M.M.) within the left main coronary artery or the first 3 cm of the left anterior descending or right coronary artery. The regions of interest ranged from 4 to 6 mm2. The room-air and postoxygen images were analyzed side by side on the satellite console of the imaging system, and the same region of interest was used for each image pair in the same volunteer by using the copy-and-paste function. As shown by Henkelman (17), the mean signal intensity in the background of a magnitude image is 1.25 times the standard deviation of noise in a uniform region within the body. Therefore, the standard deviation of the noise was estimated as the mean signal of the background air divided by a factor of 1.25.

The sharpness of the coronary artery boundary delineation was evaluated as a quantitative measure to compare the spatial resolution of room-air and postoxygen images according to a procedure previously described (18–20). One of the authors (D.L.) performed the analysis by using commercially available software (Scion Image; Scion, Frederick, Md). Original images of each pair of 3D data sets acquired with room-air and postoxygen breath holds were given to that author in random order. The image that best delineated the coronary artery was chosen from each data set and magnified three times by using bilinear interpolation. The average signal intensity profile was obtained along a user-defined line (width, three lines) perpendicular to the long axis of the vessel. The maximum and minimum values were first noted for the rising and falling sides of the profile. The 20% and 80% points between the maximum and minimum signals were calculated for each side of the profile. The distance (in millimeters) between the two points was then determined for both sides. The inverse of the averaged distance of the two sides was used as a measurement of coronary artery sharpness. The greater the sharpness score, the better the vessel boundary delineation.

All data collected were organized on a spreadsheet (Excel; Microsoft, Redmond, Wash). Statistical significance was assessed by using the Wilcoxon signed rank test, and P < .05 was regarded as significant.


   Results
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 Results
DISCUSSION
 REFERENCES
 
The breath-hold data are summarized in Table 1. The median room-air breath hold was 56 seconds (range, 21–173 seconds), the median postoxygen breath hold was 92 seconds (range, 33–241 seconds), and the median improvement was 39 seconds (range, 12–68 seconds). This difference was statistically significant (P = .003). Data on heart rate during breath holds were available for only eight of the 12 subjects. The average heart rate was 66.9 beats per minute ± 7.5 during a room-air breath hold and 64 beats per minute ± 5.1 during an oxygen breath hold. This difference was not found to be statistically significant, but with only eight volunteers in this group, the statistical power is limited.


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  		TABLE 1. Subject Demographic and Breath-hold Data

 
The subjective difficulty of room-air and oxygen breath holds is also summarized in Table 1. Oxygen breath holds were rated as significantly easier than room-air breath holds (P = .005). In 66% of the cases, the postoxygen breath holds were rated as easier compared with room-air breath holds. For the other 33%, the postoxygen and room-air breath holds were rated as equally difficult.

The results for the room-air and postoxygen coronary artery images are summarized in Table 2. The average voxel size decreased from 0.8 x 1.1 x 4.0 mm3 on the room-air images to 0.8 x 0.9 x 2.6 mm3 on the postoxygen images. This difference in voxel volume (3.4 mm3 ± 1.0 vs 1.9 mm3 ± 0.7) was statistically significant (P = .001). In addition, the voxel became more isotropic on postoxygen images. In six of the 14 vessels studied (43%), the reduction in voxel size with preoxygenation was due to improvement in through-plane resolution only, and in two vessels (14%), the reduction was due to improvement in in-plane resolution only. In the remaining six vessels (43%), the reduction in voxel size was due to improvement in both in-plane and through-plane resolution. The average SNR decreased from 15.9 ± 8.1 on the room-air images to 11.8 ± 5.0 on the postoxygen images (P = .001).


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  		TABLE 2. Comparison of Room-Air and Postoxygen Coronary Artery Images

 
The results of the analysis of coronary artery boundary sharpness are shown in Table 2. In 11 of the 14 arteries analyzed, the postoxygen images had higher sharpness scores than the corresponding room-air images; in the remaining three arteries, the sharpness scores were the same for room-air and postoxygen images. The average postoxygen vessel sharpness score was 1.2 mm-1 ± 0.3, compared with 0.9 mm-1 ± 0.2 for room air. This difference was statistically significant (P = .002).

Examples of the timing images are shown in Figure 1. Obvious motion of the diaphragm is observed between the two images. Four pairs of coronary artery images (before and after oxygen administration) are shown in Figures 2–5. Note the improved boundary delineation of the coronary arteries on postoxygen images because of the improved spatial resolution.



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  		Figure 1. Example images showing the positions of the diaphragm during a breath-hold period. The images were acquired with a two-dimensional true FISP sequence (3.9/2.0; flip angle, 50°) in a coronal plane. Left: Image from a breath-hold timing series shows the depressed position of the diaphragm (arrow) during suspended inspiration. Right: Another image from the same series at the end of suspended inspiration shows higher position of the diaphragm (arrow), indicating termination of suspended inspiration.

 


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  		Figure 2. Paired room-air and postoxygen images of the left main and left anterior descending coronary arteries in healthy volunteer 5. Left: Room-air image, with voxel size of 2.44 mm3 and acquisition time of 47 seconds, shows the left main and left anterior descending (straight arrow) coronary arteries. Right: Postoxygen image, with voxel size of 0.98 mm3 and acquisition time of 102 seconds, shows improved definition of the distal left anterior descending coronary artery (curved arrow) on this higher-spatial-resolution image. Both images are maximum intensity projections of 3D true FISP data sets (3.4/1.3; flip angle, 70°) acquired in a coronal-to-transverse-to-sagittal orientation.

 


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  		Figure 3. Paired room-air and postoxygen images of the right coronary artery in healthy volunteer 5. Left: Room-air image, with voxel size of 4.08 mm3 and acquisition time of 44 seconds, shows the right coronary artery (arrow). Right: Postoxygen image, with voxel size of 2.10 mm3 and acquisition time of 95 seconds, shows improved definition of the right coronary artery on this higher-spatial-resolution image. Both images are maximum intensity projections of 3D true FISP data sets (3.4/1.3; flip angle, 70°) acquired in a coronal-to-transverse-to-sagittal orientation.

 


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  		Figure 4. Paired room-air and postoxygen images of the left main and left anterior descending coronary arteries in healthy volunteer 7. Left: Room-air image, with voxel size of 3.84 mm3 and acquisition time of 38 seconds, shows the left main and left anterior descending (straight arrow) coronary arteries. Right: Postoxygen image, with voxel size of 2.10 mm3 and acquisition time of 69 seconds, shows improved definition of the distal left anterior descending coronary artery (curved arrow) on this higher-spatial-resolution image. Both images are maximum intensity projections of 3D true FISP data sets (3.4/1.3; flip angle, 70°) acquired in a transverse-to-coronal-to-sagittal orientation.

 


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  		Figure 5. Paired room-air and postoxygen images of the right coronary artery in healthy volunteer 7. Left: Room-air image, with voxel size of 4.30 mm3 and acquisition time of 49 seconds, shows the right coronary artery (straight arrow). Right: Postoxygen image, with voxel size of 2.08 mm3 and acquisition time of 105 seconds, shows improved definition of the distal right coronary artery (curved arrow) on this higher-spatial-resolution image. Both images are maximum intensity projections of 3D true FISP data sets (3.4/1.3; flip angle, 70°) acquired in a sagittal-to-coronal-to-transverse orientation.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 Results
 DISCUSSION
REFERENCES
 
With the true FISP sequence for coronary artery imaging, SNR is substantially improved compared with steady-state incoherent imaging such as fast low-angle shot imaging (11). The spatial resolution of this breath-hold imaging technique is limited by the duration of voluntary apnea. One way to improve spatial resolution is to prolong the breath-hold time. In this study, we demonstrated that by increasing the inspired oxygen concentration, the duration of the breath hold was markedly increased. We were able to use the increased breath-hold time to produce images with substantially increased spatial resolution by reducing the voxel size. The increased spatial resolution was achieved while maintaining an acceptable SNR. Quantitative analysis revealed that the increased spatial resolution led to increased sharpness of the coronary artery boundary delineation on the postoxygen images. In addition, we found that the longer breath holds with oxygen were subjectively as easy as or easier than the shorter ones with room air.

Breathing oxygen has previously been shown to prolong voluntary apnea. Hyperventilation, combined with oxygen administration, has been shown to further prolong voluntary apnea compared with oxygen administration with a normal minute ventilation (14). However, hyperventilation has also been associated with coronary artery spasm; therefore, we did not employ it as a method of prolonging voluntary apnea in this study (15,16). In addition, previous investigators have employed continuous oxygen administration combined with hyperventilation to prolong voluntary apnea (12–14). Continuous oxygen administration, however, carries the risk of CO2 retention in patients with chronic obstructive lung disease (21,22). Clearly, this would not be an issue in a group of healthy volunteers but may well represent a problem in a patient population (23). Therefore, we decided that short-term administration of oxygen immediately before breath holding was preferable (15).

The mechanism of prolonged voluntary apnea after administration of oxygen is not fully understood. Most oxygen in the bloodstream is transported bound to hemoglobin. For healthy subjects breathing room air, hemoglobin is highly saturated, and additional oxygen increases this saturation only slightly. Therefore, it seems unlikely that increased oxygen transportation in the bloodstream is an important factor in the observed prolongation of voluntary apnea after oxygen administration. A more likely explanation is that oxygen administration increases the concentration of oxygen in the lung volume, which may allow for continued gas exchange during the period of apnea (14). Finally, there is the possibility of the placebo effect, which can be assessed only by giving a control group room air through the nasal cannula without the subjects’ knowledge.

We did not find significant changes in the heart rate between room-air and postoxygen breath holds in these healthy volunteers. Therefore, the same window of data acquisition per heartbeat was used for pre- and postoxygen images. However, the statistical power of the heart rate comparison between room-air and postoxygen breath holds was limited because of the small number of samples. A different acquisition window will be needed if the heart rate changes substantially between room-air and postoxygen breath holds.

It is possible to combine preoxygenation with contrast-enhanced fast low-angle shot imaging to improve 3D breath-hold coronary artery imaging. A complicating factor with contrast-enhanced imaging is that, with the same amount of contrast agent, the injection rate must be reduced if the breath-hold time is increased with preoxygenation. This will cause less blood T1 shortening and less blood signal enhancement.

The increase in spatial resolution on postoxygen images was due to voxel size reductions in the phase-encoding and partition-encoding directions, while the field of view and coverage remained the same. There was certain loss in SNR with postoxygen images because of the reduced voxel size. The SNR for postoxygen images was 74% of that for room-air images, which is comparable to the square root of the voxel size reduction for postoxygen images (75%), the theoretically predicted relationship. The ultimate question is whether this increase in spatial resolution leads to improved coronary artery delineation. On the basis of the work of Venkatesan and Haacke (24), once the SNR reaches a certain level (>4), the definition of the object depends more on spatial resolution than on SNR. Therefore, as long as SNR is more than 4, which was true for our postoxygen images, loss of SNR does not reduce the benefit of preoxygenation. However, if SNR decreases to less than 4, the benefit of increased spatial resolution with oxygen will be limited.

Other potential approaches to improving spatial resolution with 3D breath-hold coronary artery imaging include parallel imaging (25,26), partial Fourier reconstruction (27,28), and undersampled projection reconstruction (29). These methods can be used to potentially achieve higher spatial resolution without increasing breath-hold time. Nevertheless, the resulting SNR values of these images are expected to be less than those of images acquired with increased breath-hold times. Further investigations are necessary to compare these approaches.

The findings from this study have shown that preoxygenation is a practical and well-tolerated technique in healthy volunteers undergoing coronary MR angiography and can enhance the subject’s comfort and produce images with increased spatial resolution and improved vessel wall delineation. It is likely that many patients who are suspected of having coronary artery disease will also have respiratory disease and therefore have shorter breath-hold times than those achieved by healthy volunteers. However, Marks et al (13) showed that oxygen administration allowed patients with chronic pulmonary disease to more than double their average maximum breath-hold duration. We believe that with preoxygenation, patients with coronary artery disease will also increase their breath-hold duration. Further study is needed to clarify how much improvement will occur in these patients.


   ACKNOWLEDGMENTS
 
The authors thank Tom C. Krejcie, MD, of the Department of Anesthesiology, Northwestern University Medical School, Chicago, Ill, for helpful discussions regarding the use of oxygen to prolong voluntary apnea in healthy subjects.


   FOOTNOTES
 
Abbreviations: FISP = fast imaging with steady-state precession, SNR = signal-to-noise ratio, 3D = three-dimensional

Author contributions: Guarantors of integrity of entire study, R.M.M., D.L.; study concepts and design, R.M.M., D.L., J.P.F.; literature research, R.M.M., D.L.; clinical studies, R.M.M., D.L., S.M.S., V.S.D.; experimental studies, R.M.M., D.L., S.M.S., V.S.D., J.D.G.; data acquisition, R.M.M., D.L.; data analysis/interpretation, R.M.M., D.L., V.S.D., S.M.S., J.D.G., F.S.P., J.C.C.; statistical analysis, R.M.M., D.L.; manuscript preparation, R.M.M., D.L., S.M.S., V.S.D., J.D.G.; manuscript definition of intellectual content, R.M.M., D.L., J.P.F.; manuscript editing, R.M.M., D.L.; manuscript revision/review, F.S.P., R.M.M., D.L., J.P.F., J.C.C.; manuscript final version approval, all authors.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 Results
 DISCUSSION
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RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE