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DOI:10.2214/AJR.06.0161
AJR 2007; 188:W423-W427
© American Roentgen Ray Society

Clinical Observations

Marked Lipomatous Infiltration of the Right Ventricle: MRI Findings in Relation to Arrhythmogenic Right Ventricular Dysplasia

Robson Macedo1, Kalpana Prakasa1, Crystal Tichnell1, Frank Marcus2, Hugh Calkins1, João A. C. Lima1,3 and David A. Bluemke1,3

1 Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, MRI Bldg., Rm. 143, 600 N Wolf St., Baltimore, MD, 21287.
2 Division of Cardiology, Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD.
3 Division of Cardiology, Department of Medicine, University of Arizona, Phoenix, AZ.

Received January 30, 2006; accepted after revision May 16, 2006.

 
Address correspondence to D. A. Bluemke (dbluemke{at}jhmi.edu).

WEB This is a Web exclusive article.


Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to describe the structure and function of the heart in the presence of marked lipomatous infiltration of the right ventricular wall in 13 patients referred for second opinions about fatty infiltration of the right ventricular wall and suspected arrhythmogenic right ventricular dysplasia.

CONCLUSION. Lipomatous infiltration with right ventricular thickness ≥ 6 mm on MRI but without regional or global functional abnormalities of the right ventricle appears to be distinct from fatty right ventricle associated with arrhythmogenic right ventricular dysplasia. The finding of right ventricular fat must be interpreted cautiously to avoid the pharmacologic and defibrillator intervention associated with management of arrhythmogenic right ventricular dysplasia.

Keywords: cardiac imaging • heart • MRI • right ventricle


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Fatty replacement of the myocardium is a peculiar condition that has been reported to occur primarily in the right side of the heart. Fontaine et al. [1] reported that fat is normally well demarcated from underlying muscle in the right ventricular (RV) free wall and around epicardial coronary vessels but is not present in the left ventricle in healthy persons. Fat, however, can be interspersed with RV myocardial fibers without accompanying fibrosis or signs of inflammation [1, 2].

Arrhythmogenic RV dysplasia (ARVD) is a condition in which the RV free wall is partially or almost entirely replaced by fatty or fibrofatty tissue. Residual myocardium with degenerative changes is interspersed among adipocytes and fibrous tissue, providing a substrate for life-threatening ventricular arrhythmia, which can result in sudden death [3]. ARVD is clinically characterized by ECG abnormalities of conduction, repolarization, and depolarization; ventricular arrhythmia; family history of sudden cardiac death; and structural and functional abnormalities of the right ventricle [4-6]. Fatty infiltration of the RV can occur without fibrosis, but its relation to ARVD is not understood.

The use of MRI in the diagnosis of ARVD is well established [7-9], but reliance on fat signal intensity in the MRI diagnosis of ARVD has met only variable success [7, 10, 11]. The purpose of this study was to report MRI findings on patients with fatty replacement of the right ventricle whose conditions did not meet the criteria for ARVD established by the World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of Cardiomyopathies [4].


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patient Population
All patients were retrospectively selected from the Johns Hopkins Hospital database of referrals for ARVD. Patients were originally referred because they had nonsustained ventricular tachycardia. They were evaluated by a senior clinical electrophysiologist experienced in evaluating ARVD. The evaluation included the relevant medical history, including history of arrhythmia or sudden death in the family. From the records entered into the database for the years 2003 through 2005, we selected cases in which T1-weighted MR images showed high signal intensity corresponding to fat in the RV wall and in which task force criteria for ARVD [5] were not met owing to normal physical examination findings and normal findings on resting and exercise ECG, signal-averaged ECG, echocardiography, or electrophysiologic studies. For the purposes of this study, MRI findings were excluded from consideration for evaluation of task force criteria. A total of 13 cases that matched the criteria were selected. The findings for patients meeting the selection criteria were compared with those for 20 healthy subjects (10 men and 10 women) free of clinical cardiovascular disease. Institutional review board approval was obtained.

MRI Protocol
All MRI data were obtained with 1.5-T systems (10 Signa Cvi, GE Healthcare; one Avanto, Siemens Medical Solutions; one Intera, Philips Medical Systems). The protocols included breath-hold retrospective ECG-gated 2D black blood images of the heart for the diagnosis of RV wall signal abnormality and for determination of RV wall thickness. The images were acquired in the transaxial or short-axis plane or both planes with double inversion recovery turbo fast spin-echo, spin-echo T1-weighted, or proton density-weighted technique with 5- to 8-mm slice thickness and 2- to 4-mm interslice gap. Fat-suppressed images were obtained to confirm the presence of fat in the RV wall by use of either chemical shift fat suppression or inversion recovery technique. Breath-hold retrospective ECG-gated 2D bright blood cine images with 6- to 8-mm slice thickness and 2- to 4-mm interslice gap were obtained in the transaxial and short axis planes with steady-state free precession technique (true fast imaging with steady-state free precession on the Avanto from Siemens Medical Solutions system, fast imaging with steady-state acquisition on the Signa Cvi from GE Healthcare systems, and balanced fast-field echo on the Intera from Philips Medical Systems). Surface coils were used for signal reception in all cases.


Figure 1
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  		Fig. 1A —30-year-old man in normal health. Axial proton density-weighted fast spin-echo MR image without fat saturation shows intermediate signal intensity of normal right ventricular wall (arrows) in relation to high signal intensity of adjacent fat.

 


Figure 2
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  		Fig. 1B —30-year-old man in normal health. Axial proton density-weighted fast spin-echo MR image with fat saturation shows normal right ventricular wall with well-defined epicardial border (arrows).

 
Image Evaluation
On T1-weighted and proton density-weighted black blood MR images, normal myocardium has intermediate signal intensity similar to that of skeletal muscle, and fat has high signal intensity. There is often a clear line of demarcation between the intermediate signal intensity of RV myocardium and the high signal intensity of epicardial fat (Fig. 1A, 1B). High signal intensity replacing the intermediate RV signal intensity indicates infiltration of epicardial fat into the RV wall [10]. The presence of fat was confirmed with chemically selective MR pulses based on the resonance frequency of lipid. RV fat was described as present or absent in the RV outflow tract, basal free wall, middle free wall, apical free wall, and inferior wall. Images were independently evaluated by two blinded reviewers. The reviewers were allowed to adjust window width and level on the workstation (Efilm 2.0, Merge) to optimize visualization of the right ventricle. In cases of reviewer discrepancy, a third reviewer provided the final adjudication for descriptive purposes.

RV free wall thickness, volume, and function were measured with MASS software (version 6.1, Medis) with manual contouring. RV free wall thickness was determined on ECG-gated black blood axial images of the myocardium acquired during diastole. RV wall thickness was measured from epicardium to endocardium, excluding the RV epicardial fat. Fat external to the pericardium also was excluded. RV volume was determined by manually contouring the endocardium on each slice, summing the slices, and multiplying by slice thickness (Simpson rule) and interslice gap. The moderator band was included as part of the RV volume. RV global and regional end-diastolic volume and ejection fraction were calculated by use of a summation-of-disks method (Simpson rule) with integration over image slices containing the right ventricle.

Global and regional peak filling rate (a measure of diastolic function [12]) and peak ejection rate were determined as previously described [13, 14]. RV and left ventricular wall motion was subjectively evaluated as normal, hypokinetic, akinetic, or dyskinetic for basal, middle cavity, and apical slices.

Statistical Analysis
All statistical analyses were performed with Stata 8.0 software (Stata). Continuous data were expressed as mean ± SD. Proportions for RV wall signal abnormality were analyzed for the RV outflow tract, basal, middle, apical, and inferior regions. The mean values and SD in the patient and control groups were obtained for RV end-diastolic diameter, RV wall thickness, RV global and regional end-diastolic volumes, RV global and regional ejection fractions, and RV global and regional peak ejection and peak filling rates. The Wilcoxon's rank sum (Mann-Whitney) test was used for comparing two unmatched samples (patient group and control group). Interobserver variability for the diagnosis of intramyocardial fat in the RV wall was analyzed with the kappa statistic.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Patient Population
The patient group included four men and nine women. The mean age of the patients selected was 56 years. The mean age of the women was 58.7 years and that of the men was 49.7 years. The body mass index (BMI, derived by dividing weight in kilograms by height squared in meters) of the patient group as a whole was 27.9 ± 5.34. The BMI of the women was 25.6 ± 3.2 and that of the men was 31.5 ± 8.9.

Intramyocardial Fat
Fat signal intensity was visualized in the RV outflow tract of 10, basal free ventricular wall of 12, middle free ventricular wall of 11, apical free ventricular wall of 11, and inferior ventricular wall of eight patients. The most commonly affected RV region in women was the basal wall, which was affected in all nine women. The RV outflow tract and basal walls were equally affected in the four men. Seven patients had RV free wall transmural infiltration and replacement extending from the epicardial to the endocardial surface. There was good correlation between observers for the diagnosis of intramyocardial fat in the wall of the RV outflow tract ({kappa} =1.0, p < 0.01), basal wall ({kappa} =1.0, p < 0.01), middle wall ({kappa} =1.0, p < 0.01), apical wall ({kappa} =0.8, p < 0.01), and inferior wall ({kappa} =1.0, p < 0.01).

RV Morphologic Parameters
There was no difference between the RV end-diastolic diameter of the patient group and that of the control group (Table 1). Fat infiltration of the RV wall was associated with increased RV wall thickness in all 13 patients compared with the healthy subjects. The thickness of the RV anterior wall ranged from 6 to 13 mm (mean, 9 ± 2.5 mm) in the patient group and from 2 to 5 mm in the control group (mean, 4.1 ± 1.1) (p < 0.001) (Table 1). No RV aneurysms were identified in the patient group.


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  		TABLE 1: Right Ventricular Morphologic and Functional Measurements

 

RV Function and Volume Parameters
There were no differences between the global and regional RV ejection fractions and global and regional RV end-diastolic volumes of the patient group and those of the control group (p > 0.05 for all parameters) [15] (Table 1), and there were no differences between the global and regional RV peak ejection rates and peak filling rates (p > 0.05 for all parameters) (Table 1). No left ventricular or RV wall motion abnormalities were identified in the patient group, including in the area of the right ventricle in which MRI showed high signal intensity correlating with fat tissue.


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We used MRI in the evaluation of a group of patients with suspected ARVD with marked diffuse lipomatous infiltration of the right ventricle, which has not to our knowledge been previously described. These patients were unique in that the marked fatty infiltration of the right ventricle caused the ventricular wall to appear thickened (Figs. 2A, 2B and 3A, 3B, 3C). Despite RV fat infiltration, on cine MR images, global and regional wall motion in the patient group was not distinguishable from that in a group of healthy volunteers. At careful clinical evaluation by an experienced electrophysiologist, none of these patients had findings that met ARVD task force criteria, which were assessed independently of MRI findings.


Figure 3
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  		Fig. 2A —45-year-old woman with history of nonsustained ventricular tachycardia. Axial proton density-weighted fast spin-echo MR image without fat saturation shows fat replacement of entire right ventricular (RV) wall (arrows), which appears thickened.

 

Figure 4
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  		Fig. 2B —45-year-old woman with history of nonsustained ventricular tachycardia. Axial proton density-weighted fast spin-echo MR image with fat saturation shows suppression of fatty component of RV wall. Thin portion of nonfatty RV wall (arrows) is evident.

 

Figure 5
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  		Fig. 3A —48-year-old woman with history of palpitations and nonsustained ventricular tachycardia. Axial T1-weighted fast spin-echo MR image without fat saturation shows fat replacement of entire right ventricular wall (arrows), which appears thickened.

 

Figure 6
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  		Fig. 3B —48-year-old woman with history of palpitations and nonsustained ventricular tachycardia. Bright blood four-chamber MR images of heart in diastole (B) and systole (C) show normal biventricular cardiac function.

 

Figure 7
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  		Fig. 3C —48-year-old woman with history of palpitations and nonsustained ventricular tachycardia. Bright blood four-chamber MR images of heart in diastole (B) and systole (C) show normal biventricular cardiac function.

 
Since the original MRI descriptions of ARVD [16-20], physicians have tended to equate fatty infiltration of the right ventricle detected with MRI to the diagnosis ARVD. Molinari et al. [21] found that myocardial adipose replacement can be a source of RV arrhythmia.

Fat detection with MRI was not part of the original ARVD task force criteria because the influence of MRI technology and specificity in diagnosis were not known [5]. In a study conducted with conventional spin-echo MRI, healthy subjects and patients with definite ARVD could not be differentiated on the basis of fatty infiltration of the right ventricle [7]. We used more sophisticated fast spin-echo pulse sequences to address the issue of RV fat. Abundant replacement of the RV free wall by fat was readily detected with MRI and was not associated with other morphologic or functional abnormalities of the right ventricle.

A definitive pathologic description for the patients in this study was not available because these patients did not qualify for RV biopsy on the basis of clinical or imaging findings. Patients in this series had abundant fat replacing the RV free wall with characteristic hypertrophy of the RV wall due to the presence of fat (Figs. 2A, 2B and 3A, 3B, 3C). There have been several histopathologic descriptions of RV fat, although none of them are entirely consistent with our observations. The fat dissociation syndrome proposed by Fontaine et al. [1] consists of diffuse fat interspersed with RV myocardial fibers but without fibrosis or inflammation. Fontaine et al. described this condition as common in more than one half of the 140 hearts they examined after necropsy. A second pattern of RV fat, described by Tansey et al. [22] as a normal variant, consists of minimal fat interspersed with normal myocytes in healthy elderly patients without cardiomyopathy. Burke et al. [2] reported fatty infiltration of the right ventricle in normal hearts, primarily in the anteroapical region, indicating that as much as 15% fat at the apex was of little clinical significance. In our study, however, fat was detected primarily at the base and middle wall of the right ventricle.

The cause of abundance of RV fat is unknown. One possibility is that it is associated with obesity. On average, the patient group was obese with a mean BMI of 28. This BMI is nearly equal to the mean BMI found in a population-based study in the United States [23, 24]. The BMI of the control group was not available. Further population-based studies are needed to define any association between fatty right ventricle and obesity. Other causes may include viral injury and genetic predisposition.

An important limitation of this study was the small number of subjects. We believe this small number may reflect the rarity of the condition; the true population prevalence is unknown. Our study subjects were referred to us by cardiologists because they had nonspecific symptoms, such as nonsustained ventricular tachycardia. Although these patients do not appear to be at the same risk of sudden death as ARVD patients, the long-term consequences of RV infiltration by fat needs further longitudinal evaluation. It has been suggested [22] that fatty infiltration without fibrosis and myocyte degeneration has low arrhythmogenic potential.

Lipomatous infiltration of the right ventricle without global or regional functional abnormalities appears to be a distinct MRI-defined disorder that should be differentiated from ARVD. Thus strict adoption of the World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of Cardiomyopathies criteria for ARVD is needed to avoid unnecessary pharmacologic and implantable cardioverter-defibrillator intervention in patients with isolated fatty infiltration of the right ventricle.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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