DOI:10.2214/AJR.06.1224
AJR 2007; 188:1675-1681
© American Roentgen Ray Society
Non-Ischemic Causes of Delayed Myocardial Hyperenhancement on MRI
Ruth P. Lim1,
Monvadi B. Srichai and
Vivian S. Lee
1 All authors: Department of Radiology – MRI, New York University Medical
Center, 530 First Ave., New York, NY 10016.
Received September 15, 2006;
accepted after revision December 29, 2006.
Address correspondence to R. P. Lim.
Abstract
OBJECTIVE. Delayed contrast-enhanced cardiac MRI has been used to
evaluate myocardial viability in ischemic heart disease (IHD). However, it can
also be used in the assessment of non-ischemic cardiac diseases.
CONCLUSION. We illustrate a number of non-ischemic cardiac
conditions and describe how they can be differentiated from IHD.
Keywords: cardiac imaging • cardiovascular imaging • heart disease • MRI • MR technique
Introduction
Delayed hyperenhancement on contrast-enhanced cardiac MRI, with spatial
resolution and image contrast superior to scintigraphy and superior anatomic
coverage and unlimited multiplanar capability compared with echocardiography,
correlates well with clinical measures of myocardial infarction
[1] and is predictive of
myocardial viability before revascularization in ischemic heart disease (IHD)
[2].
Many non-ischemic cardiac diseases can cause delayed hyperenhancement. In
this article, we review the appearances and significance of delayed
hyperenhancement in the clinical management of these conditions.
Gadolinium Chelate Pharmacokinetics
Delayed hyperenhancement reflects irreversibly injured myocardium or
replacement fibrosis. Commonly used gadolinium chelates are extracellular
contrast agents that normally equilibrate rapidly between the vascular space
and interstitium. Disruption of cell membranes and edema that occur in acutely
infarcted myocardium increase accessibility of gadolinium to free water
protons. In addition, changes in coronary artery flow rates and in capillary
density and permeability lead to slower wash-in and washout of gadolinium in
chronically injured myocardium, thereby contributing to delayed
hyperenhancement [3].
Delayed Enhancement Sequences
Inversion-recovery gradient-echo sequences, either spoiled gradient-echo or
steady-state free precession sequences, are used to assess for the presence of
delayed hyperenhancement, whereb y an appropriate inversion time is used to
null unscarred myocardium and enhance the conspicuity of abnormal tissue. In
magnitude-reconstructed inversion-recovery sequences, which depict absolute
values of magnetization, it is important to set the inversion time using an
inversion time–mapping sequence to identify when normal myocardium is
lowest in signal because selection of an incorrect inversion time can lead to
inverted image contrast and incorrect identification of normal and abnormal
myocardium. Alternatively, a phase-sensitive reconstruction of the
inversion-recovery sequence—which does not require exact identification
of the optimal inversion time because it depicts the full range of
negative-to-positive values of magnetization—can be used in which
infarcted or injured myocytes will always be higher in signal intensity than
normal myocardium [4].
Ischemic Patterns of Delayed Hyperenhancement
In IHD, infarction always involves the subendocardium, which is most
vulnerable to ischemia because of its distance from the epicardial coronary
arteries, and delayed hyperenhancement due to ischemia corresponds to coronary
artery territories (Fig. 1).
Non-ischemic causes should be suspected if the subendocardium is spared or if
involvement does not conform to a vascular territory.
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Fig. 1 —75-year-old man with known coronary artery disease.
Short-axis true fast imaging with steady-state precession phase-sensitive
inversion-recovery image shows two hyperenhancing near-transmural infarct
areas involving left ventricular basal anterior and anteroseptal segments
(arrow) and basal inferolateral segment (arrowhead). These
areas correspond to 100% occluded proximal left anterior descending artery and
diffuse disease of both left circumflex artery and right coronary artery at
coronary angiography (not shown).
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Non-Ischemic Causes of Delayed Hyperenhancement
Cardiomyopathies
Delayed hyperenhancement is present in a range of cardiomyopathies and may
be predictive of inducible ventricular tachycardia in many forms of
nonischemic cardiomyopathy
[5].
Hypertrophic cardiomyopathy (HCM)—A cause of lethal
arrhythmias in young adults, HCM is caused by genetic mutations of cardiac
sarcomeric proteins that result in asymmetric hypertrophy of the left
ventricular wall. Autosomal dominant transmission is most common
[6]. Delayed hyperenhancement
has been reported in a high percentage of HCM patients
[7], is predominantly patchy
rather than confluent, and is mainly localized to the interventricular septum
at sites of attachment of the right ventricle to the left ventricle (Fig.
2A,
2B). It is thought to correlate
histopathologically with plexiform fibrosis in HCM.
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Fig. 2A —42-year-old man with known hypertrophic cardiomyopathy.
Short-axis inversion-recovery turbo FLASH image obtained using 3.0-T scanner
10 minutes after gadolinium administration shows patchy subendocardial septal
enhancement at mid ventricular level (arrow).
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Fig. 2B —42-year-old man with known hypertrophic cardiomyopathy.
Three-chamber contrast-enhanced inversion-recovery turbo FLASH image again
shows delayed mid anteroseptal hyperenhancement (arrowhead).
Asymmetric septal hypertrophy (arrow) is better seen on this view
than on A.
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Non-ischemic dilated cardiomyopathy— Dilated cardiomyopathy
is the most common type of cardiomyopathy. It may be idiopathic or secondary
to a range of causes: toxic substances, such as alcohol or chemotherapeutic
agents; myocarditis; pregnancy; or familial in 25–35% of cases,
including Duchenne or Becker muscular dystrophies
[6]. Ischemic cardiomyopathy is
an indirect cause of myocardial dysfunction and is therefore not included.
Morphologically, all cardiac chambers are enlarged, with variable ventricular
mural thickness.
Delayed hyperenhancement is a variable finding that has been described as
having two distinct patterns: patchy with longitudinal mid wall enhancement
that spares the subendocardium and subepicardium or subendocardial or
transmural enhancement that is indistinguishable from IHD, with the latter
possibly representing sequelae of recanalized coronary artery disease
incorrectly classified as non-ischemic dilated cardiomyopathy
[8]
(Fig. 3).
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Fig. 3 —45-year-old man with non-ischemic dilated cardiomyopathy.
Two-chamber segmented turbo FLASH image obtained 10 minutes after contrast
administration shows anterior wall linear hyperenhancement sparing
subendocardium and subepicardium (arrow).
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Arrhythmogenic right ventricular cardiomyopathy (ARVC)—ARVC
is associated with ventricular tachycardia and sudden death. Delayed
hyperenhancement may be seen in regions of fibrofatty infiltration of the
right ventricular wall, particularly the outflow tract and anterobasal region
(Fig. 4A,
4B). Although ARVC cannot be
diagnosed on the basis of MRI alone, right ventricular dilation and
dysfunction with microaneurysms are highly suggestive features.
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Fig. 4A —37-year-old man with arrhythmogenic right ventricular
cardiomyopathy presenting with syncope and T-wave inversion in precordial
leads. (Courtesy of David Bluemke, John Hopkins University School of Medicine,
Baltimore, MD) Delayed contrast-enhanced short-axis image shows enhancement of
right ventricular free wall (arrow) and involvement of left ventricle
(arrowhead).
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Fig. 4B —37-year-old man with arrhythmogenic right ventricular
cardiomyopathy presenting with syncope and T-wave inversion in precordial
leads. (Courtesy of David Bluemke, John Hopkins University School of Medicine,
Baltimore, MD) Axial dark-blood T1-weighted image obtained before contrast
administration shows high signal consistent with fat within right ventricular
free wall (arrow) and left ventricular lateral wall
(arrowhead).
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Restrictive cardiomyopathies—Restrictive cardiomyopathy can
be idiopathic or secondary to radiation fibrosis, amyloidosis, sarcoidosis, or
inborn errors of metabolism
[6]. Gross morphology is
generally similar regardless of the cause, with normal-sized ventricles;
patchy or diffuse interstitial fibrosis; and, commonly, biatrial
enlargement.
Appearances of cardiac sarcoid depend on the stage of disease. Acutely,
there may be T2 hyperintensity and delayed hyperenhancement secondary to edema
and inflammation that preferentially affect the mid wall rather than
subendocardium. Focal areas of thickening may mimic HCM. Sarcoid granulomas,
if present, may show delayed hyperenhancement and T2 hyperintensity, sometimes
with central T2 hypointensity from hyaline fibrosis. Sarcoid favors the basal
septum or left ventricular wall, with papillary or right ventricular
involvement rarely seen (Fig.
5A,
5B). Delayed hyperenhancement
and myocardial thickening may resolve after a patient undergoes corticosteroid
therapy, although T2 hyperintensity usually persists. In more advanced cases,
fibrosis occurs, with patchy or diffuse wall thinning and persistent delayed
hyperenhancement [9].
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Fig. 5A —58-year-old man with sarcoidosis presenting with ventricular
tachycardia. Three-chamber turbo FLASH single-shot phase-sensitive
inversion-recovery image at 10 minutes after contrast injection shows delayed
hyperenhancement in mid wall involving basal inferolateral segment
(arrow).
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Fig. 5B —58-year-old man with sarcoidosis presenting with ventricular
tachycardia. Three-chamber unenhanced dark-blood turbo spin-echo T2-weighted
image shows slightly more distal T2 hyperintensity in mid inferolateral wall
(arrow) that indicates inflammation.
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In amyloidosis, cardiac involvement may be ventricular in the systemic form
or atrial in the primary form
[6]. Mural thickening and
delayed hyperenhancement in affected regions, which may be global and
subendocardial, are presumably secondary to increased extracellular space
caused by amyloid deposition
[10]
(Fig. 6).
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Fig. 6 —76-year-old man with systemic amyloidosis. Two-chamber
delayed contrast-enhanced image shows diffuse linear enhancement of left
ventricle (arrow). (Courtesy of Rajiv Agarwal, Cleveland Clinic
Foundation, Cleveland, OH)
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Hypereosinophilic syndrome (and eosinophilic leukemia if a specific
cytogenetic abnormality is present) is a multisystemic condition. Cardiac
involvement (Loeffler's endomyocarditis) is common and associated with a poor
clinical outcome. Eosinophil infiltration causes myocardial damage in three
stages: acute necrotic; thrombotic–necrotic, with a risk of distal
emboli; and late fibrotic, with mural thickening due to thrombus and scar
organization with progressive obliteration of the affected cavity. Although
there is often subendocardial involvement similar to IHD, biventricular and
biatrial involvement with sparing of the outflow tracts is distinctive (Fig.
7A,
7B,
7C,
7D).
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Fig. 7A —63-year-old woman with eosinophilic leukemia and
thrombotic–necrotic stage of Loeffler's endomyocarditis. Short-axis true
fast imaging with steady-state precession (FISP) phase-sensitive
inversion-recovery (PSIR) image at 10 minutes after contrast administration
shows confluent subendocardial hyperenhancement of all apical segments
involving less than 50% of wall thickness (arrowheads).
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Fig. 7B —63-year-old woman with eosinophilic leukemia and
thrombotic–necrotic stage of Loeffler's endomyocarditis. Four-chamber
true FISP PSIR image shows extent of subendocardial involvement, extending
proximally to involve mid inferoseptal (white arrowhead) and basal
and mid anterolateral segments (black arrowheads). There is
hyperenhancement of apical right ventricular free wall (arrow).
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Fig. 7C —63-year-old woman with eosinophilic leukemia and
thrombotic–necrotic stage of Loeffler's endomyocarditis. Four-chamber
dark-blood T2 fast spin-echo image shows corresponding T2 hyperintensity
(thick arrow) where delayed hyperenhancement is present in B
and ancillary findings of apical left lower lobe consolidation (thin
arrow) and pericardial effusion (arrowheads).
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Fig. 7D —63-year-old woman with eosinophilic leukemia and
thrombotic–necrotic stage of Loeffler's endomyocarditis. Three-chamber
true FISP PSIR image shows 1-cm nonenhancing focus overlying basal
inferolateral endocardium (arrow), which is consistent with small
left ventricular thrombus.
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Trauma and Postablation
Delayed hyperenhancement in the setting of trauma may indicate permanent
myocyte death from blunt trauma or myocardial infarction secondary to coronary
artery injury. The mechanism of injury and appearance of the delayed
hyperenhancement can help to distinguish between them. The extent of
myocardial necrosis in radiofrequency ablation for arrhythmias can also be
monitored noninvasively with MRI because these lesions show early
hypoperfusion and delayed hyperenhancement (Fig.
8A,
8B).
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Fig. 8A —52-year-old woman presenting with recurrent tachyarrhythmia
after undergoing right ventricular outflow tract radiofrequency ablation.
Delayed contrast-enhanced turbo FLASH inversion-recovery horizontal long-axis
image shows hyperenhancement of right ventricular outflow tract close to
interventricular septum at site of prior ablation (arrow).
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Fig. 8B —52-year-old woman presenting with recurrent tachyarrhythmia
after undergoing right ventricular outflow tract radiofrequency ablation. Cine
true fast imaging with steady-state precession vertical long-axis image
through right ventricle shows focal outpouching (arrow) in systole,
which is consistent with dyskinesis at site of radiofrequency ablation.
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Myocarditis
Myocarditis can cause acute chest pain with ECG and cardiac enzyme changes
that may mimic IHD. With acute myocarditis, delayed hyperenhancement has been
described as more nodular and subepicardial, without respect for vascular
territories, with an often inferolateral and apical distribution
[11] (Fig.
9A,
9B). Changes of myocarditis
may be subtle and focal acutely, becoming more diffuse over the next 10 days.
Early perfusion imaging is usually normal in myocarditis unlike the focal
hypoenhancement that may occur with acute IHD.
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Fig. 9A —17-year-old boy with chest pain, inferior and lateral
ST-elevation ECG changes, and elevated troponin with normal findings on
coronary angiography. Four-chamber segmented turbo FLASH inversion-recovery
image obtained 10 minutes after contrast administration shows patchy foci of
hyperenhancement subepicardially involving mid and apical lateral left
ventricular wall (arrows).
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Fig. 9B —17-year-old boy with chest pain, inferior and lateral
ST-elevation ECG changes, and elevated troponin with normal findings on
coronary angiography. Short-axis view at mid level again shows subepicardial
nature of inferolateral wall hyperenhancement (arrow). Multiple
vascular territories and nonsubendocardial involvement are typical of
myocarditis.
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Masses
Masses are often readily distinguished from other causes of delayed
hyperenhancement, although diagnosis of specific tumors is more problematic.
Intramyocardial masses, however, can be difficult to distinguish from primary
myocardial disease, particularly if they show subtle changes in signal
characteristics from the surrounding myocardium, are sessile, or have poorly
defined margins (Fig. 10A,
10B,
10C). Metastatic tumors, most
commonly bronchogenic, breast, and esophageal carcinomas, are approximately 40
times more common than primary cardiac tumors. Heterogeneous delayed
hyperenhancement may be seen with metastases. An aggressive or infiltrative
appearance or pleural or pericardial involvement may also indicate malignancy
(Fig. 11A,
11B,
11C).
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Fig. 10A —18-year-old asymptomatic man with heart murmur at physical
examination and fibroma at surgery. Two-chamber phase-sensitive
inversion-recovery contrast-enhanced delayed phase image shows intensely
enhancing well-circumscribed mass involving mid to apical anterior left
ventricular wall (arrow) with small nonenhancing central focus.
Pericardial effusion is also present.
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Fig. 10B —18-year-old asymptomatic man with heart murmur at physical
examination and fibroma at surgery. Corresponding short-axis magnitude image
confirms intramyocardial location of mass with thin rim of circumferential
myocardium (arrowheads). There is left ventricular cavity
deformation.
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Fig. 10C —18-year-old asymptomatic man with heart murmur at physical
examination and fibroma at surgery. Unenhanced cine true fast imaging with
steady-state precession short-axis systolic image shows mass is isointense to
myocardium, a mimic for hypertrophic cardiomyopathy.
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Fig. 11B —67-year-old woman with history of metastatic renal cell
carcinoma. Tagged FLASH image shows noncontractile mass with no deformation of
grid tags within mass (arrow) compared with normal myocardium
(arrowheads).
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Fig. 11C —67-year-old woman with history of metastatic renal cell
carcinoma. Four-chamber segmented true fast imaging with steady-state
precession inversion-recovery image obtained 10 minutes after contrast
administration shows vivid hyperenhancement of mass (arrow), with
small focus of necrosis, and tiny right ventricular mural thrombus
(arrowhead).
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Primary tumors are most commonly benign. Up to 50% of primary benign tumors
may show delayed hyperenhancement, particularly myxomas, hemangiomas, and less
commonly fibromas. Primary malignancies are more likely to enhance vividly
and, as with metastases, may be infiltrative.
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Abstract
Introduction
