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AJR 2005; 185:110-115
© American Roentgen Ray Society

Clinical Observations

Effectiveness of Delayed Enhanced MRI for Identification of Cardiac Sarcoidosis: Comparison with Radionuclide Imaging

Eiji Tadamura1, Masaki Yamamuro1, Shigeto Kubo1, Shotaro Kanao1, Tsuneo Saga1, Masaki Harada2, Muneo Ohba3, Ryohei Hosokawa3, Takeshi Kimura3, Toru Kita3 and Kaori Togashi1

1 Department of Nuclear Medicine and Diagnostic Imaging, Kyoto University Graduate School of Medicine, 54 Shogoinkawahara, Sakyo-ku, Kyoto 606-8507, Japan.
2 Department of Endocrinology, Kyoto University Graduate School of Medicine, Kyoto, Japan.
3 Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Received August 18, 2004; accepted after revision September 29, 2004.

 
Address correspondence to E. Tadamura (et{at}kuhp.kyoto-u.ac.jp).


Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to evaluate the usefulness of delayed enhanced MRI for detecting cardiac sarcoidosis and to clarify the relationship between the findings of MRI and those of radionuclide imaging.

CONCLUSION. Delayed enhanced MRI is considered a useful method for the early identification of cardiac sarcoidosis. Delayed hyperenhancement is frequently associated with a reduction of regional wall motion and thallium-201 perfusion defects.


Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Sarcoidosis is a multisystemic disease of unknown cause that is characterized by the formation of non-caseating granulomas [1]. Cardiac sarcoidosis is one of the most important factors determining prognosis [2-4]. Echocardiography, ECG, and radionuclide imaging are commonly used for the diagnosis of cardiac involvement. However, the diagnosis of cardiac involvement is still difficult. It is accurately diagnosed before death in only 29% of patients with fatal cardiac sarcoidosis [5]. Early initiation of corticosteroid therapy in patients with cardiac sarcoidosis improves left ventricular function and prevents malignant arrhythmia [6].

Delayed enhanced MRI was introduced a few years ago to identify myocardial infarctions [7]. This new technique has been shown to detect new or previous myocardial infarction with detail and high spatial resolution [7-10]. This approach also has been used for tissue characterization of various heart diseases [11-15]. However, to our knowledge, no study investigating the usefulness of delayed enhanced MRI for detection of myocardial involvement of sarcoidosis has been published, except for one case report [16]. The purpose of this study was to evaluate the effectiveness of delayed enhanced MRI for detecting cardiac involvement of sarcoidosis and to clarify the relationship between the findings of MRI and those of conventional radionuclide imaging.


Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects
We studied 10 consecutive patients with cardiac sarcoidosis diagnosed either histologically or clinically according to the following criteria: For the histologic diagnosis group, cardiac sarcoidosis was diagnosed when histologic analysis of operative or endomyocardial biopsy specimens showed epithelioid granuloma without caseating granuloma. For the clinical diagnosis group, consisting of patients with a histologic diagnosis of extracardiac sarcoidosis, cardiac sarcoidosis was diagnosed when complete atrioventricular block, ventricular tachycardia, or emergence of right bundle branch block or premature ventricular contraction (> grade 2 in Lown's classification) was observed. These criteria were modeled on Japanese Ministry of Health and Welfare guidelines for diagnosing cardiac sarcoidosis [17-19]. All patients underwent MRI and scintigraphy using thallium-201 (201Tl) and gallium-67 (67Ga). Coronary angiography was performed on patients with suspected coronary artery disease to exclude coronary artery disease. The protocol was approved by the local institutional ethics committee. Informed consent was obtained from each patient.

MRI
MRI was performed using a 1.5-T whole-body scanner (Symphony, Siemens) with multiple surface coils connected to phased-array receivers. Breathhold cine MRI was performed using segmented true fast imaging with steady-state precession [20, 21]. The typical imaging parameters were as follows: TR/TE, 3.6/1.8; a 60° flip angle; 13 lines per segment; a 256 x 200 matrix; and a 340 x 320 mm field of view. The temporal resolution was approximately 50 msec. Cine MR images were obtained in the contiguous short-axis planes covering the whole left ventricle [21, 22] and the vertical and horizontal long-axis planes. Fifteen minutes after injection of a 0.15 µmol/kg dose of gadodiamide contrast agent (Omniscan, Nycomed Amersham), delayed enhanced MR images were acquired in the same views as for cine images, using an inversion recovery segmented gradient-echo sequence [7-15]. The typical imaging parameters were as follows: TR/TE, 8.6/3.9; a 25° flip angle, 25 lines per segment, a 256 x 200 matrix, and a 340 x 320 mm field of view. Inversion time (220-360 msec) was optimized for each measurement. In-plane image resolution was typically 1.3 x 1.6 mm. Slice thickness was 8 mm and slice gap was 2 mm.



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  		Fig. 1A —52-year-old woman with clinically diagnosed cardiac sarcoidosis. Basal short-axis delayed enhanced MR image depicts delayed enhancement on right ventricular side of septal region (arrows).

 



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  		Fig. 1B —52-year-old woman with clinically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show no abnormal wall motion.

 



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  		Fig. 1C —52-year-old woman with clinically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show no abnormal wall motion.

 



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  		Fig. 1D —52-year-old woman with clinically diagnosed cardiac sarcoidosis. Basal short-axis 201Tl SPECT image shows no abnormal perfusion defect. No abnormal 67Ga uptake in heart was observed on 67Ga scintigrams.

 
Scintigraphic Examinations
201Tl scintigraphy—201Tl (74 MBq) was administered IV under resting conditions. SPECT images were acquired 15 min after injection using a dual-head gamma camera (Millennium, GE Healthcare) equipped with a general-purpose collimator (30 projections over 180°, 30 sec per projection). Two 30% energy windows were used, one centered on the 70-keV peak and one on the 167-keV peak [22, 23].



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  		Fig. 2A —69-year-old man with clinically diagnosed cardiac sarcoidosis. Basal short-axis delayed enhanced MR image reveals strong transmural hyperenhancement in septal, anterior, and inferior regions (arrows).

 



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  		Fig. 2B —69-year-old man with clinically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show wall motion abnormalities in these segments (arrows, C).

 



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  		Fig. 2C —69-year-old man with clinically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show wall motion abnormalities in these segments (arrows, C).

 



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  		Fig. 2D —69-year-old man with clinically diagnosed cardiac sarcoidosis. Basal short-axis 201Tl SPECT image shows perfusion defects in septal, anterior, and inferior regions (arrows), where severe extent of transmural enhancement is seen on delayed enhanced MR images. No abnormal cardiac 67Ga uptake was detected on 67Ga scintigrams.

 
67Ga scintigraphy—Forty-eight hours after injection of 111 MBq of 67Ga, scintigraphic planar images were acquired using the dual-head gamma camera with medium-energy parallel collimators. Acquisition was performed using three photopeaks (93, 184, and 296 keV) with a 20% window. Thoracic 67Ga SPECT acquisition included three photopeaks, 32 projections over a 360° rotation, and 35 sec per step.

Image Analysis
Left ventricular function was assessed using cine MR images with the aid of commercially available software (Argus, Siemens Medical Solutions) followed by manual corrections of the left ventricular border [21]. Regional analysis of MR images and radionuclide images was performed using the 17-segment model [24]. The average segmental transmural extent of enhancement on delayed enhanced MR images was graded visually by two masked observers using the following scale: 0, no enhancement; 1, 1-25% enhancement; 2, 26-50% enhancement; 3, 51-75% enhancement; and 4, 76-100% enhancement [9]. Segmental wall motion was visually scored as 0, normal; 1, moderate hypokinesis; 2, severe hypokinesis; 3, akinesis; and 4, dyskinesis [9] by two masked investigators. The 201Tl perfusion defect was visually scored by two masked experienced nuclear cardiologists on the basis of severity of reduction in 201Tl activity as 0, normal; 1, mild; 2, moderate; and 3, severe [24]. Two experienced nuclear radiologists visually interpreted 67Ga accumulation while unaware of other results. Consensus was then reached for each visual analysis.

Statistical Analysis
Data are expressed as mean ± SD. Frequency analysis was performed with the Fisher exact test. The mean wall motion score and 201Tl defect score in each hyperenhancement grade were compared using the Mann-Whitney U test. A p value of less than 0.05 was considered significant.


Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Table 1 summarizes the patients' profiles and the results of MRI and radionuclide imaging.


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  		TABLE 1 : Patient Profiles and Results of MRI and Scintigraphy

 

Frequency of Abnormality
Among 10 subjects, five exhibited abnormal delayed enhancement without an abnormality in wall motion or abnormalities shown by radionuclide imaging (Figs. 1A, 1B, 1C, and 1D). One subject exhibited abnormal delayed enhancement and a 201Tl perfusion defect without regional wall motion abnormalities or abnormal cardiac 67Ga uptake. Two subjects exhibited abnormal delayed enhancement, 201Tl perfusion defects, and regional wall motion abnormalities without cardiac 67Ga accumulation (Figs. 2A, 2B, 2C, and 2D). Two subjects showed abnormal delayed enhancement, thallium perfusion defects, regional wall motion abnormalities, and abnormal cardiac 67Ga uptake (Figs. 3A, 3B, 3C, 3D, and 3E). Thus, delayed enhancement was observed in every patient with cardiac sarcoidosis (100%). Wall motion abnormalities were observed in four of 10 patients (40%). 201Tl perfusion defects were noted in five subjects (50%). Two patients exhibited abnormal 67Ga accumulation in the heart (20%). Abnormal delayed enhancement was more frequently observed than were 201Tl perfusion defects (p < 0.05) or abnormal 67Ga accumulation in the heart (p < 0.001).



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  		Fig. 3A —65-year-old woman with histologically diagnosed cardiac sarcoidosis. Basal short-axis delayed enhanced MR image reveals strong transmural enhancement in septal and inferior regions (arrows). Abnormal hyperenhancement is also observed in right ventricular wall (arrowheads).

 


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  		Fig. 3B —65-year-old woman with histologically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show wall motion abnormalities in inferior segments (arrows, C).

 


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  		Fig. 3C —65-year-old woman with histologically diagnosed cardiac sarcoidosis. Cine MR images obtained at end diastole (B) and end systole (C) for basal short-axis slice show wall motion abnormalities in inferior segments (arrows, C).

 


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  		Fig. 3D —65-year-old woman with histologically diagnosed cardiac sarcoidosis. Basal short-axis 201Tl SPECT image shows perfusion defects in septal and inferior regions (arrows).

 


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  		Fig. 3E —65-year-old woman with histologically diagnosed cardiac sarcoidosis. Basal short-axis 67Ga SPECT image shows abnormal accumulation of 67Ga mainly in inferior and septal regions (arrows), corresponding to areas with significant transmural hyperenhancement and 201Tl perfusion defects.

 

Location of Abnormal Enhancement
Among the 170 myocardial segments, abnormal delayed enhancement was observed in 48. Figure 4 shows the number of regional segments with abnormal delayed enhancement in the 10 patients. In nine (90%) of the 10 patients, hyperenhancement occurred in the basal septal wall, especially on the right ventricular side (Figs. 1A, 2A, and 3A). The subendocardium of the left ventricle was not involved in seven patients (Fig. 1A).



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  		Fig. 4 —Number of segments with abnormal delayed enhancement among 17 myocardial segments in 10 patients. Abnormal delayed enhancement was frequently observed in basal septal region.

 
Wall Motion Abnormality, 201Tl Perfusion Defects, and 67Ga Accumulation Versus Delayed Enhancement
The transmural extent of enhancement on contrast-enhanced MR images correlated significantly with regional 201Tl uptake (Fig. 5) and with regional wall motion (Fig. 6). 201Tl perfusion abnormalities and wall motion abnormalities corresponded to the area showing significant transmural enhancement (Figs. 2A, 2B, 2C, 2D, 3A, 3B, 3C, 3D, and 3E). However, 201Tl perfusion defects or wall motion abnormalities were undetectable in some segments with mild-to-moderate transmural enhancement (Figs. 1A, 1B, 1C, and 1D). When observed in the heart, abnormal 67Ga accumulation was seen in the segments with severe transmural enhancement and with 201Tl perfusion defects (Figs. 3A, 3B, 3C, 3D, and 3E). On the other hand, delayed enhancement was also observed in regions showing 201Tl perfusion defects without significant 67Ga uptake (Figs. 2A, 2B, 2C, and 2D).



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  		Fig. 5 —Bar graph shows relationship between transmural extent of delayed gadolinium enhancement and 201Tl perfusion defects. Significant differences were observed in mean percentage of 201Tl perfusion defect score between segments of grades 0 and 1, grades 1 and 2, grades 2 and 3, and grades 3 and 4.

 


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  		Fig. 6 —Bar graph indicates relationship between transmural extent of delayed gadolinium enhancement and regional wall motion. Significant differences were noted in mean percentage of wall motion score between segments of grades 0 and 1, grades 1 and 2, grades 2 and 3, and grades 3 and 4.

 

Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
MRI and radionuclide imaging showed a variety of patterns of abnormalities in patients with cardiac sarcoidosis. Among the various findings in MRI and radionuclide imaging, delayed enhanced MRI was considered the most sensitive marker of cardiac involvement of sarcoidosis.

Endomyocardial biopsy may be essential for establishing the diagnosis of cardiac sarcoidosis. However, myocardial biopsies are invasive and, because they are performed blindly and myocardial involvement is not homogeneous, may be insensitive. Echocardiography can detect features such as wall thinning, abnormalities in left ventricular regional wall motion, and pericardial effusion in advanced cardiac sarcoidosis [25-28]. However, early diagnosis of cardiac involvement is difficult on echocardiography. Radionuclide imaging, although it can be helpful for the diagnosis [29-31], does not provide adequate spatial resolution. Indeed, half the cases of cardiac sarcoidosis did not show 201Tl perfusion defects in the current study. MRI has been used to detect cardiac involvement of sarcoidosis [17, 32]. However, those studies used the standard T1-weighted contrast-enhanced spin-echo sequence in which images are acquired without breath-holding. This conventional sequence needs a relatively long acquisition time, which frequently produces respiration motion artifacts [33]. In addition, the contrast between normal and diseased myocardium is not always sufficient [33]. Therefore, we have used a new technique [7-16, 33] for the identification of cardiac involvement of sarcoidosis.

In the current study, delayed enhancement was not always associated with 201Tl perfusion defects or with abnormal 67Ga accumulation. This imperfect association may be caused partly by the poor spatial resolution of radionuclide imaging. However, the transmural extent of hyperenhancement on delayed enhanced MR images correlated significantly with regional 201Tl uptake (Fig. 5). 201Tl perfusion defects were seen in the segments with significant transmural delayed enhancement (Figs. 2A, 2B, 2C, 2D, 3A, 3B, 3C, 3D, and 3E). Decreased 201Tl uptake of the myocardium in patients with cardiac sarcoidosis is known to represent fibrogranulomatous replacement of the myocardium [1, 31]. 67Ga scintigraphy has been used to diagnose and evaluate disease activity. In particular, 67Ga accumulation is interpreted as evidence of active inflammatory disease [31]. When abnormal 67Ga accumulation was detected in the heart, the segments with 67Ga uptake corresponded to the areas with considerable transmural delayed enhancement and with 201Tl perfusion defects (Figs. 3A, 3B, 3C, 3D, and 3E). In addition, the transmural extent of hyperenhancement on delayed enhanced MR images significantly correlated with regional wall motion as shown in Figure 6. These findings suggest that the area with delayed enhancement represents myocardium that has been replaced by the fibrogranulomatous tissue of sarcoidosis, resulting in decreased wall motion. On the other hand, regions with 201Tl perfusion defects and no significant 67Ga uptake also showed delayed enhancement (Figs. 2A, 2B, 2C, and 2D), suggesting that it does not reflect disease activity, although poor spatial resolution might be responsible for undetectable 67Ga uptake.

As shown in Figure 4, delayed enhancement was frequently observed in the basal septal region. This finding is consistent with the findings of previous pathologic and morphologic studies [3, 19, 34, 35] indicating that cardiac involvement of sarcoidosis is common in the basal septal region. The subendocardium of the left ventricle was not involved in seven patients (Figs. 1A, 1B, 1C, and 1D), unlike the patients with coronary artery disease. Delayed enhancement on the right ventricular side of the basal septal wall might be specific for cardiac involvement in patients with sarcoidosis, because hyperenhancement in this location is uncommon in other cardiac diseases [8, 9, 11, 12, 14]. In addition, this bundle and the right bundle branch are located around this position, possibly accounting for the fact that atrioventricular block or right bundle branch block is frequently observed in cardiac sarcoidosis.

The major limitation of our study was that cardiac sarcoidosis was proven histologically in only one patient. To confirm our results, further studies should be performed on a large population of patients with histologically proven cardiac sarcoidosis.

In conclusion, delayed enhanced MRI is considered useful for the early identification of cardiac involvement of sarcoidosis. Delayed enhancement is frequently associated with a reduction of regional wall motion and thallium perfusion defects.


References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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J.-P. Smedema and E. Tadamura
Previous Studies on Delayed Enhanced MRI for the Detection of Cardiac Sarcoidosis
Am. J. Roentgenol., February 1, 2006; 186(2): 578 - 579.
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