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Clinical Significance of Myocardial Magnetic Resonance Abnormalities in Patients With Sarcoidosis*: A 1-Year Follow-up Study FREE TO VIEW

Olivier Vignaux, MD; Robin Dhote, MD; Denis Duboc, MD, PhD; Philippe Blanche, MD; Daniel Dusser, MD; Simon Weber, MD; Paul Legmann, MD
Author and Funding Information

*From the Departments of Radiology (Drs. Vignaux and Legmann), Medicine (Drs. Dhote and Blanche), Pneumology (Dr. Duboc), and Cardiology (Drs. Dusser and Weber), Université René Descartes, Paris, France.

Correspondence to: Olivier Vignaux, MD, Université René Descartes, Hôpital Cochin, 27 rue du Fg Saint Jacques, 75679 Paris Cedex 14, France; e-mail: olivier.vignaux@cch.ap-hop-paris.fr



Chest. 2002;122(6):1895-1901. doi:10.1378/chest.122.6.1895
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Purpose: To assess the follow-up of patients with sarcoidosis and myocardial MRI abnormalities.

Materials and methods: Twelve patients with histologically proven sarcoidosis and highly suspected cardiac involvement underwent initial and 12-month follow-up cardiac assessment including cardiac MRI (T2-weighted, functional gradient echo, and T1-weighted gadolinium-diethylenetriamine penta-acetic acid-enhanced sequences). MRI abnormalities and clinical and MRI progression were scored by two observers.

Results: Six patients receiving corticosteroid therapy (including three patients with clinical cardiac involvement) were scored as having cleared or improved at MRI follow-up, while others were seen to have worsened or remained stable. The stability, improvement, or clearing of MRI findings were correlated with clinically stable, improved or cleared sarcoidosis, while a worsening at MRI follow-up was correlated with a worsening of sarcoidosis and, in one patient, was predictive of clinical cardiac involvement.

Conclusion: Cardiac MRI is a useful noninvasive method for the early diagnosis and follow-up of cardiac sarcoidosis.

Figures in this Article

Cardiac involvement is symptomatic in only 5% of patients with sarcoidosis,12 although it is evident in the myocardium at autopsy in 20 to 50%.23 Most patients with subclinical, myocardial, histologic lesions will remain asymptomatic, but sudden death due to ventricular tachyarrhythmia or conduction block accounts for 30 to 65% of fatalities.45 The early initiation of corticosteroid therapy in patients with cardiac sarcoidosis improves left ventricular function and prevent malignant arrhythmia.6 Noninvasive imaging methods such as echocardiography and thallium scan, which might allow the identification of patients at risk requiring corticosteroids, suffer from low sensitivity or specificity, while an endomyocardial biopsy finding may be negative because of the patchy distribution of lesions.

Experience in applying MRI to the diagnosis of sarcoidal heart disease has been limited to a few case reports.712 Shimata et al13 recently emphasized the usefulness of gadolinium-diethylenetriamine penta-acetic acid (DTPA)-enhanced MRI in a series of eight patients with histologically proven cardiac sarcoidosis. The aim of the present study was to prospectively assess the clinical and MRI follow-up of 12 patients with active sarcoidosis and initial cardiac MRI abnormalities, so as to clarify the significance of myocardial MRI abnormalities and investigate the role of cardiac MRI in the management of patients with sarcoidosis.

Study Population

Between October 1999 and September 2000, 20 patients with histologically proven, active sarcoidosis were referred for cardiac assessment. A diagnosis of sarcoidosis was confirmed if the clinical presentation and chest radiographic findings were supported by histologic evidence of noncaseous epithelioid granulomas by bronchial or salivary gland biopsy, and once the possibility of infection, environmental factors or medical treatment causing the granuloma had been eliminated. Other data collected included gender, age at the diagnosis of sarcoidosis, duration, chest radiography, and extrathoracic sarcoidosis based on clinical, biological, radiologic, and histologic findings. Radiologic chest stage by high-resolution CT (HRCT), angiotensin-converting enzyme concentrations, and treatment were recorded. Cardiac evaluation included a physical examination, surface ECG and 24-h Holter monitoring, echocardiography, 201Tl myocardial scintigraphy, and cardiac MRI; coronary angiography was also performed in patients with suspected coronary artery disease or those > 40 years old.

Inclusion criteria were patients with highly suspected cardiac involvement based on perfusion defects that regressed after nicardipine therapy on the thallium scan. Exclusion criteria were cardiac MRI findings not consistent with myocardial involvement (n = 3) or presence of other cardiac conditions, as evidenced by clinical, echocardiographic, or angiographic data (ischemia, n = 2; valve disease, n = 1; hypertension, n = 2). Twelve patients were included (3 male, 9 female; mean ± SD age, 38.2 ± 7.3 years), and they underwent a follow-up MRI examination at 12 months, using the same protocol as the initial MRI procedure.

The data collected during the 12-month follow-up assessment included physical examination, the visceral distribution of sarcoidosis, surface ECG and 24-h Holter monitoring, echocardiography, chest HRCT staging, angiotensin-converting enzyme concentrations, and treatment. The study was approved by the Institutional Review Board, and informed consent was obtained from all subjects.

Clinical Progression Score

At the 12-month follow-up assessment, two clinicians (R.D., P.B.) reached a consensus as to the clinical score for disease activity: cleared was defined as a return to normal of chest HRCT findings and angiotensin-converting enzyme concentrations, and a complete clearing of extrathoracic involvement; improvement was defined as a downgrading of the chest HRCT stage, a reduction in angiotensin-converting enzyme concentrations, and a reduction in visceral involvement; worsening was defined as an increase in at least one of these parameters, and stability was defined no changes from the initial evaluation.

MRI Protocol

MRI was performed using a 1.5-T imager (Echospeed; GE Medical Systems; Milwaukee, WI) with a cardiac-dedicated, phased-array coil. Three ECG electrodes were placed dorsally on the patient’s skin close to the position of the heart, and ECG triggering was initiated by standard software. After the patient had been positioned headfirst and supine in the center of the magnet, three-plane gradient-echo scout images were acquired. All morphologic acquisitions were gated in the diastole to minimize artifacts due to cardiac motion.

Multislice axial, long-axis, and short-axis images were acquired with the T2-weighted breath-hold, black blood, single-shot, fast spin-echo sequence, as previously described.14 Because data at the center of the k space may define image contrast, the center of the k space was sampled later in the echo train so that T2-weighting would be increased. The following parameters were applied: repetition time, 2 R-R to ∝; echo time, 26 ms; inversion time, − 600 ms; refocusing flip angle, 170°; echo train length, 40; matrix, 128 × 256 after half-Fourier processing; rectangular 250 × 125-mm field of view; section thickness, 5 mm; intersection gap, 0 mm; mean imaging time, 21 s (range, 17 to 26 s); one signal acquired.

A conventional axial ECG-triggered T1-weighted spin-echo sequence was also performed with fat suppression after an IV bolus of 0.1 mmol/kg gadolinium-DTPA: repetition time/echo time, 680 to 960/30 ms; matrix, 192 × 256 (phase encoding × frequency encoding); rectangular field of view with a maximum dimension of 380 to 440 mm; four signals acquired. Imaging times ranged from 7 min and 34 s, to 9 min and 18 s (mean, 8 min and 21 s).

The functional investigation was carried out using segmented k-space gradient-echo (FASTCARD; GE Medical Systems) magnetic resonance, multislice, double-angulated, long-axis (four-chamber views) and short-axis sequences with the following parameters: repetition time dependent on the heart beat interval/minimum echo time; flip angle, 20°; matrix, 128 × 256; rectangular field of view with a maximum dimension of 380 to 440 mm; slice thickness, 10 mm; eight views per segment; mean imaging time, 17 s (range, 13 to 21 s); one slice per breath-hold.

The total time required for the investigation was 45 min. The same protocol was applied during the 12-month MRI follow-up assessment.

Analysis of MRIs

All initial and follow-up MRIs were interpreted by two experienced cardiovascular radiologists (O.V., P.L.), who reached a consensus unaware of the clinical findings. Scores ranging from − 1 to + 1 were assigned to six different myocardial areas (right ventricle, septal wall, and anterior, lateral, inferior and posterior walls) for morphologic T2-weighted and gadolinium-DTPA–enhanced spin-echo images, on the basis of a qualitative evaluation of signal intensity: 0 = normal (medium homogeneous signal intensity of the myocardial wall); + 1 = increased (hyperintense area with signal intensity higher than normal myocardial wall); − 1 = decreased (hypointense area with signal intensity lower than normal myocardial wall). Myocardial wall thickness was evaluated on axial, left ventricular long-axis and short-axis images; scores ranging from − 1 to + 1 were assigned to the same myocardial areas: 0 = normal (3 to 10 mm), + 1 = increased (> 10 mm); − 1 = decreased (< 3 mm). Functional gradient-echo images were analyzed using specific software (MASS; Medis; Lieden, the Netherlands). Regional wall motion was semiquantitatively assessed by cine-loop simulation in both the true long and short left ventricular axes, and the two observers assigned scores ranging from 0 to + 1 after reaching a consensus (0 = normokinetic, + 1 = hypokinetic, akinetic or dyskinetic) for the six myocardial areas: right ventricle, septal wall, and anterior, lateral, inferior and posterior walls. A total score, obtained by adding together the scores obtained for each myocardial area in terms of signal intensity, myocardial thickness, and contractility, was then calculated for each patient.

MRI abnormalities of myocardial signal intensity and thickness were grouped to produce three different patterns: (1) pattern A, the pure nodular type, with an increased nodular intramyocardial signal on both T2-weighted and gadolinium-DTPA–enhanced T1-weighted images (with or without a central portion of decreased signal intensity); pattern B, focal increased intramyocardial signal on gadolinium-DTPA–enhanced T1-weighted images (whatever the signal on the T2-weighted sequence), with or without myocardial thickening; and pattern C, focal increased intramyocardial signal on T2-weighted images without gadolinium uptake and/or focal or diffuse myocardial thinning.

MRI Progression Score

Twelve-month follow-up MRI images were interpreted by the same observers using the scoring method applied to the six myocardial areas (right ventricle, septal wall, and anterior, lateral, inferior and posterior walls) in terms of signal intensity, myocardial thickness, and contractility. The total score (addition of the scores obtained for each myocardial area) was then calculated for each patient and compared with the initial score, and outcome was graded as follows: cleared, if a complete regression of the initial MRI abnormalities was noted (12-month total score of zero); improvement, if the increased signal intensity on the T2-weighted sequence had regressed, and/or the increased signal intensity on the contrast- enhanced sequence had regressed, and/or increased myocardial thickness and/or initial contraction abnormalities had regressed (12-month total score lower than the initial score); stability, if the initial MRI abnormalities had remained unchanged (same 12-month total score as initial total score); and worsening, if there was an increase in the score over the initial MRI abnormalities (increased 12-month total score compared to the initial score). Using this scoring method, myocardial thinning (= − 1) at the 12-month follow-up assessment was considered as suggestive of scarring, and scored as an improvement.

Clinical Data at Inclusion

The clinical findings concerning the 12 patients included in the study are summarized in Table 1 . Eight patients had intrathoracic disease and the involvement of other organs. Two patients (patients 4 and 5) exhibited isolated intrathoracic involvement. One patient presented with Löfgren syndrome (patient 10), and one patient with myositis and intrathoracic involvement (patient 11). Sarcoidosis had been diagnosed only 1 year previously in seven patients, while disease duration ranged from 5 to 23 years in the other five patients.

Three patients exhibited clinical cardiac involvement: syncope with atrioventricular block (n = 1), dyspnea with dilated cardiomyopathy on echocardiography (n = 1), and acute cardiac failure following surgery (n = 1). In two of these patients, sarcoidosis was multivisceral, while only intrathoracic involvement was present in the third patient.

MRI at Inclusion

The results of the initial MRI examination are described in Table 2 . The three patients with clinical cardiac involvement exhibited pattern B images. MRI revealed a septal nodule (pattern A) in two patients. Other patients without clinical cardiac involvement had pattern B in six patients and pattern C in one patient. Contraction abnormalities (hypokinesis) were recorded in one patient with clinical cardiac involvement and three patients without clinical cardiac involvement (pattern B, n = 3; pattern C, n = 1); their localization was correlated with the topography of the intramyocardial increased signal on T2-weighted images and/or gadolinium-DTPA–enhanced T1-weighted images.

Clinical Data at 12-Month Follow-up

All three patients with cardiac sarcoidosis diagnosed clinically at the first assessment were treated with corticosteroid therapy. Two of these patients exhibited a regression of cardiac involvement (patients 1 and 2), and one patient showed an improvement in cardiac insufficiency (patient 4).

At 12 months, 3 patients without clinical cardiac involvement treated with high-dose corticosteroids were scored as either cleared or improved. One patient receiving a low-dose regimen of corticosteroids (10 mg/d) between the first and second MRI examinations was scored as stable (patient 9).

As for the five patients who did not receive any corticosteroid therapy, two patients were scored as stable and three patients were scored as worsening. In one of the patients not receiving corticosteroids and scored as worsening (patient 3; Fig 1 ), cardiac involvement was clinically diagnosed at the follow-up examination (appearance of a new right bundle- branch block). At the initial evaluation 12 months previously, ECG and Holter ECG findings had been normal.

12-Month MRI Follow-up

The results of the 12-month MRI follow-up examination are shown in Table 3 . All six patients treated with high-dose corticosteroids were scored as cleared or improved at the 12-month MRI follow-up assessment (including three patients with clinical cardiac involvement). The patient receiving a low-dose regimen of corticosteroids (10 mg/d) between the first and second MRI examinations was scored as stable. Patients not receiving any corticosteroids were scored as worsening in three patients and stable in two patients.

A regression of contraction abnormalities was recorded in three patients (pattern B, n = 2; pattern C, n = 1), while the emergence of focal hypokinesis was observed in four other patients (pattern B, n = 3; pattern C, n = 1). The regression or emergence of focal hypokinesis was recorded in two patients, and scored as stable (patients 9 and 10).

Correlation of Clinical and MRI Findings at the 12-Month Follow-up Assessment

A clearing of cardiac MRI findings at the 12-month follow-up assessment was correlated with a clearing of sarcoidosis in two patients (ie, all extracardiac sarcoidosis cleared in concert with clearing cardiac sarcoidosis), while an improvement in MRI findings was correlated with a clinical improvement in two patients (Table 4 ). In one patient, an improvement at the MRI follow-up (MRI feature qualified as scarring) was correlated with a clearing of sarcoidosis.

A worsening in findings at the MRI follow-up (n = 3) was always correlated with a worsening of sarcoidosis (n = 3), while stability (n = 3) was correlated with stable sarcoidosis (n = 3). As for the patient with Löfgren syndrome (patient 10), both MRI and clinical features had remained stable without treatment. A worsening of MRI findings in one untreated patient was associated with the emergence of right bundle branch block at follow-up. All patients with worsening sarcoidosis were treated with corticosteroids after the 12-month follow-up assessment.

The pathologic features of cardiac sarcoidosis include patchy infiltration of the myocardium with three successive histologic stages: edema, granulomatous infiltration, and fibrosis leading to postinflammatory scarring.2 MRI provides high-resolution information for both morphology and function, rendering MRI an effective method for the assessment of myocardial diseases. The ability of MRI to diagnose sarcoidal heart disease has been emphasized in several case reports,712 allowing early identification of patients requiring careful study and treatment. The diagnostic success of biopsy in cardiac sarcoidosis is low, and the accurate localization of sarcoidal lesions by MRI could guide endomyocardial biopsy. Sarcoidal infiltrates are visible on MRIs as zones of increased intramyocardial signal intensity; these are more pronounced on T2-weighted images because of the edema associated with inflammation and granulomatous lesions, and are enhanced on gadolinium-DTPA–enhanced MRIs.1113 Increases in the thickness of the interventricular septum or part of the left ventricular wall have also been recorded, suggesting that cardiac sarcoidosis may mimic, or even present as, hypertrophic cardiomyopathy.15 In the nodular type of sarcoidosis, MRI may visualize a central portion with low signal intensity on both T1- and T2-weighted images, representing hyaline fibrotic tissue, and a peripheral area yielding high signal intensity on T2-weighted images, representing the edema associated with granulomatous inflammation.10

Our results are consistent with previously described MRI abnormalities. The MRI findings could be grouped by three different patterns. This preliminary study shows that such cardiac MRI features were correlated with clinical outcome. The stability, improvement or clearing of MRI findings were paralleled by clinically stable, improved, or cleared extracardiac sarcoidosis. Worsening MRI at follow-up was correlated with active sarcoidosis and was seen to be predictive of clinical cardiac involvement in one patient at follow-up, even though this patient had been asymptomatic at the initial examination.

An early initiation of corticosteroid therapy is recommended in patients with cardiac sarcoidosis.16 Our study shows that all patients receiving corticosteroids scored as cleared or improved at MRI follow-up, while patients without corticosteroids were scored as worsened or stable. A worsening of subclinical cardiac MRI abnormalities at follow-up suggests that corticosteroids should be considered in the particular group of multiple-organ sarcoidosis without an extracardiac indication for treatment. Early initiation of corticosteroid therapy has been reported to prevent malignant arrhythmia.6 Additional studies are required to confirm these preliminary findings.

An experimental study in a rodent myocarditis model has reported that an accumulation of gadolinium- DTPA in myocarditis and ongoing replacement fibrosis at both the active inflammatory and healing stages but not in scar tissue.17 Corticosteroid therapy may be required in patients with positive gadolinium-DTPA–enhanced MRIs (patterns A and B), while an increased signal on T2-weighted images may be observed both at the active inflammatory stage and in scar tissue. It should be noted that a pattern C at the initial MRI examination was correlated with clinical clearing or improvement at MRI follow-up, suggesting that this pattern may be related to scar tissue with a fibrotic component.

Endomyocardial biopsy was not performed during our study, with a view to correlating MRI patterns and histologic stages, and this is a potential limitation that is important to consider. However, all MRI abnormalities that we described have been previously reported with histologic correlation in most cases.713 In our study, the diagnosis of cardiac sarcoidosis was strongly suspected in these patients with active multiple-organ sarcoidosis, positive thallium scan findings, other heart diseases excluded, and improvement after corticosteroid therapy at the follow-up when recorded. Furthermore, the diagnostic success rate of endomyocardial biopsy is low because of the patchy distribution of lesions18; from an ethical point of view, invasive endomyocardial biopsy could not be recommended in patients without any clinical cardiac involvement.

In conclusion, this preliminary study demonstrates that cardiac MRI follow-up findings are well correlated with clinical follow-up findings. We believe that cardiac MRI should be used more widely to investigate and follow up patients with ongoing sarcoidosis, to enable the early detection of cardiac involvement, the initial manifestation of which may be sudden death in as many as 60% of these patients. A worsening of cardiac MRI findings at follow-up may suggest the need to initiate corticosteroid therapy if this has not already been done. Further studies are required to confirm the clinical significance of cardiac MRI abnormalities, so that the role of this noninvasive imaging method can be clarified regarding the management of such patients.

Abbreviations: DTPA = diethylenetriamine penta-acetic acid; HRCT = high-resolution CT

Table Graphic Jump Location
Table 1. Demographics, Clinical Data, and Cardiac Involvement in 12 Patients With Sarcoidosis
* 

Cardiac involvement was clinically diagnosed at the follow-up examination.

Table Graphic Jump Location
Table 2. Results of the Initial MRI Examination
Figure Jump LinkFigure 1. Multiple-organ sarcoidosis in a 44-year-old man without initial clinical cardiac involvement. Left ventricular, T2-weighted, long-axis black-blood, single-shot, fast spin-echo sequence. Top: initial MRI examination (left ventricular external slice) showing subtle focal increase in signal intensity in the lateral wall. Bottom: 12-month MRI follow-up (left ventricular internal slice close to the septal wall) showing progression of the increased signal to the apicoseptal and inferior wall. Appearance of a right bundle-branch block diagnosed at the follow-up examination was associated with this worsening in MRI findings.Grahic Jump Location
Table Graphic Jump Location
Table 3. Results of the 12-Month Follow-up MRI Examination
Table Graphic Jump Location
Table 4. Correlation of Clinical and MRI Follow-up
Mayock, RL, Bertrand, P, Morrison, CE (1963) Manifestations of sarcoidosis.Am J Med35,67-89. [PubMed] [CrossRef]
 
Silverman, KJ, Hutchins, GM, Bulkley, BH Cardiac sarcoid: a clinicopathologic study of 84 unselected patients with systemic sarcoidosis.Circulation1978;58,1204-1211. [PubMed]
 
Roberts, WC, McAllister, HA, Ferrans, VJ Sarcoidosis of the heart.Am J Med1977;63,86-108. [PubMed]
 
Valantine, H, McKenna, WJ, Nihoyannopoulos, P Sarcoidosis: a pattern of clinical and morphological presentation.Br Heart J1987;57,256-263. [PubMed]
 
Abeler, V Sarcoidosis of the cardiac conducting system.Am Heart J1979;97,701-707. [PubMed]
 
Sharma, OP Cardiac and neurologic dysfunction in sarcoidosis.Clin Chest Med1997;18,813-825. [PubMed]
 
Riedy, K, Fisher, MR, Belic, N, et al MR imaging of myocardial sarcoidosis.AJR Am J Roentgenol1988;151,915-916. [PubMed]
 
Dupuis, JM, Victor, J, Furber, A, et al Value of magnetic resonance imaging in sarcoidosis:a proposof a case.Arch Mal Cœur Vaiss1994;87,105-110
 
Chandra, M, Silverman, ME, Oshinski, J, et al Diagnosis of cardiac sarcoidosis aided by MRI.Chest1996;110,562-565. [PubMed]
 
Matsuki, M, Matsuo, M MR findings of myocardial sarcoidosis.Clin Radiol2000;55,323-325. [PubMed]
 
Inoue, S, Shimada, T, Murakami, Y Clinical significance of gadolinium-DTPA-enhanced MRI for detection of myocardial lesions in a patient with sarcoidosis.Clin Radiol1999;54,70-72. [PubMed]
 
Schulz-Menger, J, Strohm, O, Dietz, R, et al Visualization of cardiac involvement in patients with systemic sarcoidosis applying contrast-enhanced magnetic resonance imaging.MAGMA2000;11,82-83. [PubMed]
 
Shimata, T, Shimada, K, Sakane, T, et al Diagnosis of cardiac sarcoidosis and evaluation of the effects of steroid therapy by gadolinium-DTPA-enhanced magnetic resonance imaging.Am J Med2001;110,520-527. [PubMed]
 
Vignaux, O, Augui, J, Coste, J, et al Comparison of optimized single-shot fast spin-echo with conventional spin-echo sequences for MR imaging of the heart: initial experience.Radiology2001;219,545-550. [PubMed]
 
Matsumori, A, Hara, M, Nagai, S, et al Hypertrophic cardiomyopathy as a manifestation of cardiac sarcoidosis.Jpn Circ J2000;64,679-683. [PubMed]
 
Yasaki, Y, Isobe, M, Hiroe, M, et al Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone.Am J Cardiol2001;88,1006-1010. [PubMed]
 
Aso, H, Takeda, K, Ito, T, et al Assessment of myocardial fibrosis in cardiomyopathic hamsters with gadolinium-DTPA enhanced magnetic resonance imaging.Invest Radiol1998;33,22-32. [PubMed]
 
Uemura, A, Morimoto, S, Hiramitsu, S, et al Histologic diagnostic rate of cardiac sarcoidosis: evaluation of endomyocardial biopsies.Am Heart J1999;138,299-302. [PubMed]
 

Figures

Figure Jump LinkFigure 1. Multiple-organ sarcoidosis in a 44-year-old man without initial clinical cardiac involvement. Left ventricular, T2-weighted, long-axis black-blood, single-shot, fast spin-echo sequence. Top: initial MRI examination (left ventricular external slice) showing subtle focal increase in signal intensity in the lateral wall. Bottom: 12-month MRI follow-up (left ventricular internal slice close to the septal wall) showing progression of the increased signal to the apicoseptal and inferior wall. Appearance of a right bundle-branch block diagnosed at the follow-up examination was associated with this worsening in MRI findings.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Demographics, Clinical Data, and Cardiac Involvement in 12 Patients With Sarcoidosis
* 

Cardiac involvement was clinically diagnosed at the follow-up examination.

Table Graphic Jump Location
Table 2. Results of the Initial MRI Examination
Table Graphic Jump Location
Table 3. Results of the 12-Month Follow-up MRI Examination
Table Graphic Jump Location
Table 4. Correlation of Clinical and MRI Follow-up

References

Mayock, RL, Bertrand, P, Morrison, CE (1963) Manifestations of sarcoidosis.Am J Med35,67-89. [PubMed] [CrossRef]
 
Silverman, KJ, Hutchins, GM, Bulkley, BH Cardiac sarcoid: a clinicopathologic study of 84 unselected patients with systemic sarcoidosis.Circulation1978;58,1204-1211. [PubMed]
 
Roberts, WC, McAllister, HA, Ferrans, VJ Sarcoidosis of the heart.Am J Med1977;63,86-108. [PubMed]
 
Valantine, H, McKenna, WJ, Nihoyannopoulos, P Sarcoidosis: a pattern of clinical and morphological presentation.Br Heart J1987;57,256-263. [PubMed]
 
Abeler, V Sarcoidosis of the cardiac conducting system.Am Heart J1979;97,701-707. [PubMed]
 
Sharma, OP Cardiac and neurologic dysfunction in sarcoidosis.Clin Chest Med1997;18,813-825. [PubMed]
 
Riedy, K, Fisher, MR, Belic, N, et al MR imaging of myocardial sarcoidosis.AJR Am J Roentgenol1988;151,915-916. [PubMed]
 
Dupuis, JM, Victor, J, Furber, A, et al Value of magnetic resonance imaging in sarcoidosis:a proposof a case.Arch Mal Cœur Vaiss1994;87,105-110
 
Chandra, M, Silverman, ME, Oshinski, J, et al Diagnosis of cardiac sarcoidosis aided by MRI.Chest1996;110,562-565. [PubMed]
 
Matsuki, M, Matsuo, M MR findings of myocardial sarcoidosis.Clin Radiol2000;55,323-325. [PubMed]
 
Inoue, S, Shimada, T, Murakami, Y Clinical significance of gadolinium-DTPA-enhanced MRI for detection of myocardial lesions in a patient with sarcoidosis.Clin Radiol1999;54,70-72. [PubMed]
 
Schulz-Menger, J, Strohm, O, Dietz, R, et al Visualization of cardiac involvement in patients with systemic sarcoidosis applying contrast-enhanced magnetic resonance imaging.MAGMA2000;11,82-83. [PubMed]
 
Shimata, T, Shimada, K, Sakane, T, et al Diagnosis of cardiac sarcoidosis and evaluation of the effects of steroid therapy by gadolinium-DTPA-enhanced magnetic resonance imaging.Am J Med2001;110,520-527. [PubMed]
 
Vignaux, O, Augui, J, Coste, J, et al Comparison of optimized single-shot fast spin-echo with conventional spin-echo sequences for MR imaging of the heart: initial experience.Radiology2001;219,545-550. [PubMed]
 
Matsumori, A, Hara, M, Nagai, S, et al Hypertrophic cardiomyopathy as a manifestation of cardiac sarcoidosis.Jpn Circ J2000;64,679-683. [PubMed]
 
Yasaki, Y, Isobe, M, Hiroe, M, et al Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone.Am J Cardiol2001;88,1006-1010. [PubMed]
 
Aso, H, Takeda, K, Ito, T, et al Assessment of myocardial fibrosis in cardiomyopathic hamsters with gadolinium-DTPA enhanced magnetic resonance imaging.Invest Radiol1998;33,22-32. [PubMed]
 
Uemura, A, Morimoto, S, Hiramitsu, S, et al Histologic diagnostic rate of cardiac sarcoidosis: evaluation of endomyocardial biopsies.Am Heart J1999;138,299-302. [PubMed]
 
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