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DOI:10.2214/AJR.07.3022
AJR 2008; 190:1358-1361
© American Roentgen Ray Society


Original Research

Assessment of Global Right Ventricular Function on 64-MDCT Compared with MRI

Cédric Plumhans1, Georg Mühlenbruch1, Annuar Rapaee2, Kui-Hian Sim2, Tobias Seyfarth3, Rolf W. Günther1 and Andreas H. Mahnken1

1 Department of Diagnostic Radiology, RWTH Aachen University Hospital, Pauwelsstraβe 30, D 52057 Aachen, Germany.
2 Department of Cardiology, Sarawak General Hospital, Sarawak, Malaysia.
3 Siemens Medical Solutions, Erlangen, Germany.

Received August 14, 2007; accepted after revision October 19, 2007.

 
Address correspondence to C. Plumhans (plumhans{at}rad.rwth-aachen.de).


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The aim of this study was to compare ECG-gated 64-MDCT with MRI for the assessment of global right ventricular (RV) function from coronary CT angiography data.

SUBJECTS AND METHODS. Thirty-eight patients (25 men, 13 women; mean age ± SD, 55.0 ± 8.8 years) with suspected coronary artery disease underwent contrast-enhanced 64-MDCT (64 x 0.6 mm, 120 kV, 770 mAseff) and 1.5-T MRI (balanced fast-field echo; TR/TE, 3.3/1.6; flip angle, 60°; 50 phases). Double oblique short-axis MDCT and MR images were used for further analysis. End-diastolic volume (EDV), end-systolic volume (ESV), stroke volume (SV), and ejection fraction (EF) were computed from manually drawn endocardial contours of the right ventricle. For statistical analysis, repeated-measures analysis of variance and Pearson's correlation coefficients were calculated. Bland-Altman plots were computed.

RESULTS. In general, RV volumes calculated from 64-MDCT agreed well with those calculated from MRI. The mean EF (± SD) calculated from MDCT and MRI was 51.0% ± 7.8% and 51.4% ± 7.3%, respectively. An excellent correlation was observed for EDV (r = 0.99), ESV (r = 0.98), SV (r = 0.98), and EF (r = 0.97). Bland-Altman plots showed no systematic variation between MDCT and MRI data. No statistically significant differences (p ≤ 0.05) between the techniques were found.

CONCLUSION. Although contrast injection is optimized for visualization of the coronary arteries, retrospectively ECG-gated 64-MDCT permits reliable assessment of global RV function.

Keywords: cardiac imaging • heart disease • MDCT • MRI • right ventricular function


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
To date, cardiac MDCT with retrospective ECG gating is an established method for the detection of coronary artery stenosis and evaluation of aortocoronary bypass grafts [14]. Multiple studies have shown that left ventricular volumes can reliably be assessed from short-axis reformations of MDCT angiography data sets [59]. For certain clinical conditions, such as pulmonary hypertension, cardiomyopathy, acute or chronic pulmonary embolism, cardiac insufficiency, and myocardial infarction, assessment of right ventricular (RV) function is clinically relevant [10, 11]. The results of previous 16-MDCT studies have shown that assessment of RV function from short-axis reformations of coronary CT angiography data sets is feasible and reliable [1215]. According to the results of a study by Raman et al. [16], retrospectively ECG-gated coronary MDCT with the possibility of image reconstruction at any phase of the cardiac cycle and in any desirable orientation might be beneficial especially for assessment of the right ventricle given its complex shape. In this respect, cardiac MDCT might even be superior to 2D imaging techniques such as echocardiography or radionuclide ventriculography. However, the limited temporal resolution and considerable breath-hold periods of MDCT are important limitations for the assessment of global and regional ventricular function. Therefore, other noninvasive methods, such as echo cardiography or MRI, with a temporal resolution as low as 50 milliseconds, must be considered as the standards of reference [1719].

Potential advantages of 64-MDCT in cardiac function imaging compared with 16-MDCT are better temporal resolution, shorter breath-hold period, different contrast enhancement, and lack of β-blockers. In consideration of these advantages, our study differs from a previous similar study with 16-MDCT.

The aim of this study was to compare the assessment of global RV function using contrast-enhanced ECG-gated cardiac 64-MDCT with 1.5-T cine MRI.


Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
In this prospective study, 38 consecutive patients (13 women, 25 men) with a mean age (± SD) of 55.0 ± 8.8 years underwent cardiac 64-MDCT for suspected coronary artery disease. On the same day as MDCT, cine MRI was performed for assessment of cardiac function on a 1.5-T scanner. The study was approved by the local institutional review board. Written informed consent was obtained from each patient.

Patients with a resting heart rate above 70 beats per minute (bpm) received a β-blocker (50–100 mg of metoprolol) orally (n = 4) to minimize motion artifacts in MDCT coronary angiography. The CT examinations were per formed on a 64-MDCT scanner (Somatom Sensa tion 64 Cardiac, Siemens Medical Solutions). A standard ized scanning pro tocol with a collimation of 64 x 0.6 mm, gantry rotation time of 330 milliseconds, and table feed of 3.8 mm per ro tation, resulting in a pitch of 0.2, was used. A tube voltage of 120 kV with an effective tube current–time product of 770 mAseff was applied. No ECG-dependent tube current modulation was applied. Temporal resolution ranged between 83 and 165 milliseconds depending on each individual patient's heart rate. Radiation exposure doses were calculated (CT Expo version 1.5, Micrsoft Excel) [20].

For contrast enhancement, a nonionic contrast agent with an iodine concentration of 370 mg I/mL (iopromide [Ultravist 370, Bayer HealthCare]) was administered via an 18-gauge venous access placed in an antecubital vein. For optimized contrast timing, the test-bolus technique was used: 10 mL of contrast medium was injected at a flow rate of 5 mL/s followed by a 50-mL saline chaser injected at the same flow rate. The time between contrast injection and maximum enhancement in the ascending aorta was used as the scanning delay for optimal contrast in the coronary arteries. The total volume of contrast medium used was calculated as the scanning time multiplied by the flow rate of 5 mL/s plus an additional 8 mL, resulting in a mean total contrast volume of 75 ± 2 mL.

From the CT raw data, a stack of images was calculated every 5% of the cardiac cycle (0–95%). Double oblique short-axis reformations of the center on the right ventricle were computed on an external workstation (Leonardo, Siemens Medical Solutions). The slice thickness of the short-axis reformations was 5 mm without an interslice gap. For further data analysis, a dedicated software tool (Argus, Siemens) was used. End-systole was defined as the cardiac phase with the smallest RV volume, whereas end-diastole was defined as the cardiac phase with the largest RV volume (Fig. 1A, 1B, 1C, 1D). Endocardial contours were drawn manually using end-systolic and end-diastolic images. Slices from the apex to the tricuspid valve were included in the analysis, according to standard conventions defined by Pennell [21]. The RV outflow to the pulmonary valve was included in the RV volume. Papillary muscles were considered to be part of the RV cavity. For drawing endocardial contours, the window settings were individually adapted according to the half-contour principle.


Figure 1
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Fig. 1A 54-year-old man who underwent retrospectively ECG-gated 64-MDCT for exclusion of coronary artery disease. Short-axis reformation images of 64-MDCT data during end-diastole (A) and end-systole (B) correlate well with MR images (C and D).

 

Figure 2
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Fig. 1B 54-year-old man who underwent retrospectively ECG-gated 64-MDCT for exclusion of coronary artery disease. Short-axis reformation images of 64-MDCT data during end-diastole (A) and end-systole (B) correlate well with MR images (C and D).

 

Figure 3
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Fig. 1C 54-year-old man who underwent retrospectively ECG-gated 64-MDCT for exclusion of coronary artery disease. Short-axis reformation images of 64-MDCT data during end-diastole (A) and end-systole (B) correlate well with MR images (C and D).

 

Figure 4
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Fig. 1D 54-year-old man who underwent retrospectively ECG-gated 64-MDCT for exclusion of coronary artery disease. Short-axis reformation images of 64-MDCT data during end-diastole (A) and end-systole (B) correlate well with MR images (C and D).

 

End-diastolic volume (EDV), end-systolic volume (ESV), stroke volume (SV), and ejection fraction (EF) were calculated using Simpson's method.

MRI was performed on a 1.5-T whole-body scanner (Gyroscan Intera, Philips Medical Systems) using a 5-channel cardiac coil. For ECG synchronization, prospective triggering was applied, and during breath-holding, 50 phases for one cardiac cycle were acquired at each slice position. A balanced fast-field echo sequence used the following imaging parameters: TR/TE, 3.3/1.6; flip angle, 60°; and slice thickness, 5.0 mm without an interslice gap. The measured voxel size was 1.83 x 1.70 x 5.00 mm with a reconstructed voxel size of 1.48 x 1.48 x 5.0 mm. Short-axis MR images were analyzed in the same manner as 64-MDCT images using the same software.

MDCT and MR images were evaluated independently by two radiologists with 8 and 2 years' experience in cardiac radiology, respec tively. The two observers were blinded to the results of the other technique.

Continuous data are given as means ± SD. For data analysis, repeated-measures analysis of variance was performed. Pearson's correlation coefficient was calculated. Statistical analysis was performed using JMP software (version 6, SAS Institute). Agreement in global RV function parameters was determined with Bland-Altman plots (MedCalc, version 8.2.1.0, MedCalc Software) [22]. A p value of ≤ 0.05 was considered statistically significant.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
All MDCT and MR examinations were completed without complications, and all were of diagnostic quality. The mean heart rate during MDCT and MRI, respectively, was 64 ± 1.7 and 63 ± 1.5 bpm for men and 67 ± 2.4 and 64 ± 2.6 bpm for women. Calculated radiation exposure was 11.3 ± 1.0 mSv for men and 16.9 ± 1.1 mSv for women.

On MDCT and MRI, respectively, the mean EDV was 78.3 ± 17.7 vs 77.9 ± 17.7 mL; mean ESV, 38.3 ± 10.1 vs 37.7 ± 9.8 mL; mean SV, 40.0 ± 11.2 vs 40.0 ± 11.0 mL; and mean EF, 51.0% ± 7.8% vs 51.4% ± 7.3%. These results showed an excellent correlation; analysis of variance did not reveal statistically significant differences between the imaging techniques (Table 1).


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TABLE 1: Parameters of Right Ventricular Function as Determined by MDCT and MR Imaging

 

Bland-Altman plots showed no systematic variation between MDCT and MR data (Fig. 2A, 2B, 2C, 2D).


Figure 5
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Fig. 2A Bland-Altman plots. Plots for end-diastolic volume (EDV) (A), end-systolic volume (ESV) (B), stroke volume (SV) (C), and ejection fraction (EF) (D) show good agreement between 64-MDCT and MRI. There is no systematic variation.

 

Figure 6
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Fig. 2B Bland-Altman plots. Plots for end-diastolic volume (EDV) (A), end-systolic volume (ESV) (B), stroke volume (SV) (C), and ejection fraction (EF) (D) show good agreement between 64-MDCT and MRI. There is no systematic variation.

 

Figure 7
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Fig. 2C Bland-Altman plots. Plots for end-diastolic volume (EDV) (A), end-systolic volume (ESV) (B), stroke volume (SV) (C), and ejection fraction (EF) (D) show good agreement between 64-MDCT and MRI. There is no systematic variation.

 

Figure 8
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Fig. 2D Bland-Altman plots. Plots for end-diastolic volume (EDV) (A), end-systolic volume (ESV) (B), stroke volume (SV) (C), and ejection fraction (EF) (D) show good agreement between 64-MDCT and MRI. There is no systematic variation.

 

Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
The results of our study illustrate that cardiac 64-MDCT permits the reliable assessment of RV function when compared with MRI. In several clinical conditions, such as pulmonary hypertension, pulmonary embolism, and myocardial infarction, assessment of RV function predicts outcome. According to the results of a study by Larose et al. [23], RV dysfunction late after myocardial infarction is an important predictor of mortality after myocardial infarction. Thus, assessment of RV function in addition to CT coronary angiography during the same session adds relevant value to cardiac CT. In our study, we found that coronary MDCT angiography using a 64-MDCT scanner, with its high spatial and temporal resolution, in addition allows functional analysis of the right ventricle. When compared with echocardiography, cross-sectional imaging techniques such as MRI or MDCT are advantageous because they do not rely on geometric assumptions and therefore can provide more accurate RV volumes than echocardiography.

Analysis of RV function was feasible using the reported contrast injection protocol and the same contrast bolus as that used for coronary MDCT angiography. In this particular setting, the use of a contrast injection protocol optimized for enhancement of the coronary arteries did not greatly hamper evaluation of global RV function. Nevertheless, improvements in RV contrast enhancement may ease delineation of the RV endocardial border. The latter may be achieved using biphasic contrast injection protocols with or without a delay between both contrast injections or by mixing 10–30% of contrast material in the saline chaser bolus. Thus, gated cardiac scanning can be optimized for analysis of RV function by using bi- or multiphasic contrast injection [24] or by adding contrast medium to the saline chaser so that a certain amount of contrast enhancement in the right ventricle during scanning could be reached without altering of coronary enhancement. In our study, we opted for a single-phase contrast medium injection to make the viability of the study uniform.

Compared with the studies by Koch et al. [12] and Raman et al. [13] in which a mean contrast volume of 100 mL was injected to assess RV function, in this study a mean total contrast volume of 75 ± 2 mL was sufficient to obtain excellent RV function measurements. Reducing the total volume of contrast injected for cardiac MDCT is particularly suitable for patients with clinical diagnoses such as renal insufficiency.

Otherwise, cardiac MDCT can be optimized for visualization of the truncus pulmonalis, especially for analysis of RV function in patients with pulmonary hypertension or pulmonary embolism. In doing so, we increase the risk of beam hardening in the right ventricle, which causes the endocardial contours of the right ventricle to become less identifiable.

In accordance with the results of other studies [23], our results showed that assessment of RV function using MDCT led to a slight overestimation of the mean EDV and ESV. The limited temporal resolution of MDCT compared with MRI is considered the main reason for this phenomenon [12]. In some patients, discrimination of the heart apex from the diaphragm was hampered by low contrast. Low contrast may result in in-accurate contours being drawn, with subsequent overestimation of the RV volumes. Nevertheless, the average deviation from the reference standard is within clinically acceptable ranges. For clinical purposes, these differences can be neglected.

A major shortcoming of this study is the need to administer β-blockers in some patients with elevated heart rates (> 70 bpm). The negative inotropic and chronotropic effects of β-blockers may limit the significance of results by interfering with the true RV volumes. However, because MRI was performed immediately after 64-MDCT, the effect of the β-blockers likely continued during the MR examination. The mean time delay between MDCT and MRI was 54 ± 17 minutes. This assumption is supported by the comparable heart rates during both examinations. Another general limitation of MDCT is radiation and contrast material exposure. Consequently, there is no indication to perform cardiac MDCT solely to assess cardiac function because radiation-free and contrast material–free imaging techniques, such as MRI and echocardiography, are readily available.

In conclusion, retrospectively ECG-gated 64-MDCT of the heart provides reliable RV function measurements when compared with MRI. Cardiac 64-MDCT shows excellent correlation with MRI for EDV, ESV, SV, and EF measurements. RV function measurements with the aid of 64-MDCT offer precious information in patients with pulmonary embolism, patients with pulmonary hypertension, or patients being evaluated after myocardial infarction, in addition to those who have undergone a triple-rule-out examination.

The intrinsic drawbacks of CT, such as radiation exposure and the need for iodinated contrast material, limit the application of MDCT solely for assessing cardiac function. However, in patients with suspected RV dysfunction who undergo coronary CT angiography, assessment of RV function will improve the diagnostic significance of cardiac MDCT.


References
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Ohnesorge B, Flohr T, Becker C, et al. Cardiac imaging by means of electrocardiographically gated multisection spiral CT: initial experience. Radiology 2000;217 : 564–571[Abstract/Free Full Text]
  2. Mollet NR, Cademartiri F, van Mieghem CA, et al. High-resolution spiral computed tomography coronary angiography in patients referred for diagnostic conventional coronary angiography. Circulation 2005;112 :2318 –2323[Abstract/Free Full Text]
  3. Mühlenbruch G, Mahnken AH, Das M, et al. Evaluation of aortocoronary bypass stents with cardiac MDCT compared with conventional catheter angiography. AJR 2007;188 : 361–369[Abstract/Free Full Text]
  4. Nikolaou K, Rist C, Wintersperger BJ, et al. Clinical value of MDCT in the diagnosis of coronary artery disease in patients with a low pretest likelihood of significant disease. AJR2006; 186:1659 –1668[Abstract/Free Full Text]
  5. Juergens KU, Fischbach R. Left ventricular function studied with MDCT. Eur Radiol 2006;16 : 342–357[CrossRef][Medline]
  6. Mahnken AH, Koos R, Spuentrup E, et al. Sixteen-slice spiral CT versus MR imaging for assessment of left ventricular function in acute myocardial infarction. Eur Radiol 2005;15 : 714–720[CrossRef][Medline]
  7. Juergens KU, Grude M, Fallenberg EM, et al. Using ECG-gated multidetector CT to evaluate global left ventricular function in patients with coronary artery disease. AJR 2002;179 :1545 –1550[Abstract/Free Full Text]
  8. Dewey M, Muller M, Eddicks S, et al. Evaluation of global and regional left ventricular function with 16-slice computed tomography, biplane cine-ventriculography, and two-dimensional transthoracic echocardiography: comparison with mag netic resonance imaging. J Am Coll Cardiol 2006; 48:2034 –2044[Abstract/Free Full Text]
  9. Mahnken AH, Katoh M, Bruners P, et al. Acute myocardial infarction: assessment of left ventricular function with 16-detector row spiral CT versus MR imaging—study in pigs. Radiology2005; 236:112 –117[Abstract/Free Full Text]
  10. Oldershaw P. Assessment of right ventricular function and its role in clinical practice. Br Heart J 1992;68 : 12–15[Free Full Text]
  11. Coche E, Vlassenbroek A, Roelants V, et al. Evaluation of biventricular ejection fraction with ECG-gated 16-slice CT: preliminary findings in acute pulmonary embolism in comparison with radionuclide ventriculography. Eur Radiol 2005;15 :1432 –1440[CrossRef][Medline]
  12. Koch K, Oellig F, Oberholzer K, et al. Assessment of right ventricular function by 16-detector-row CT: comparison with magnetic resonance imaging. Eur Radiol 2005;15 : 312–318[CrossRef][Medline]
  13. Raman SV, Shah M, McCarthy B, et al. Multidetector row cardiac computed tomography accurately quantifies right and left ventricular size and function compared with cardiac magnetic resonance. Am Heart J 2006; 151:736 –744[CrossRef][Medline]
  14. Dogan H, Kroft LJ, Huisman MV, et al. Right ventricular function in patients with acute pulmonary embolism: analysis with electrocardiography-synchronized multi-detector row CT. Radiology 2007;242 : 78–84[CrossRef][Medline]
  15. Dogan H, Kroft LJ, Bax JJ, et al. MDCT assessment of right ventricular function. AJR 2006;186 [6 suppl 2]:S366 –S370[Abstract/Free Full Text]
  16. Raman SV, Shah M, McCarthy B, Garcia A, Ferketich AK. Multi-detector row cardiac computed tomography accurately quantifies right and left ventricular size and function compared with cardiac magnetic resonance. Am Heart J 2006;151 : 736–744[CrossRef][Medline]
  17. Miller S, Simonetti OP, Carr J, et al. MR imaging of the heart with cine true fast imaging with steady-state precession: influence of spatial and temporal resolution on left ventricular functional parameters. Radiology 2002;223 : 263–269[Abstract/Free Full Text]
  18. Rerkpattanapipat O, Mazur W, Link KM, et al. Assessment of cardiac function with MR imaging. Magn Reson Imaging Clin N Am2003; 11:67 –80[CrossRef][Medline]
  19. Bellenger NG, Burgess MI, Ray SG, et al. Comparison of left ventricular ejection fraction and volumes in heart failure by echocardiography, radionuclide ventriculography and cardiovascular magnetic resonance: are they interchangeable? Eur Heart J2000; 21:1387 –1396[Abstract/Free Full Text]
  20. Stamm G, Nagel HD. CT Expo: a novel program for dose evaluation in CT [in German]. Rofo 2002;174 :1570 –1576[Medline]
  21. Pennell DJ. Ventricular volume and mass by CMR. J Cardiovasc Magn Reson 2002;4 : 507–513[CrossRef][Medline]
  22. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurements. Lancet1986; 1:307 –310[CrossRef][Medline]
  23. Larose E, Ganz P, Reynolds G, et al. Right ventricular dysfunction assessed by cardiovascular magnetic resonance imaging predicts poor prognosis late after myocardial infarction. J Am Coll Cardiol2007; 49:855 –862[Abstract/Free Full Text]
  24. Numburi DU, Chatzimavroudis GP, Stillman AE, et al. Patient-specific contrast injection protocols for cardiovascular multidetector row computed tomography. J Comput Assist Tomogr2007; 31:281 –289[CrossRef][Medline]

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