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Abstract
Cardiovascular magnetic resonance (CMR) has taken on an increasingly important role in the diagnostic evaluation
and pre-procedural planning for patients with congenital heart disease. This article provides guidelines for the
performance of CMR in children and adults with congenital heart disease. The first portion addresses preparation
for the examination and safety issues, the second describes the primary techniques used in an examination, and
the third provides disease-specific protocols. Variations in practice are highlighted and expert consensus
recommendations are provided. Indications and appropriate use criteria for CMR examination are not specifically
addressed.
Keywords: Cardiovascular magnetic resonance, Congenital heart disease, Heart defects, Imaging protocols,
Magnetic resonance imaging
* Correspondence: fratz@dhm.mhn.de;
andrew.powell@cardio.chboston.org
1 Department of Pediatric Cardiology and Congenital Heart
Disease,
Deutsches Herzzentrum München (German Heart Center Munich) of the
Technical University Munich, Munich, Germany
8 ’s Hospital, and the Department
Department of Cardiology, Boston Children of
Pediatrics, Harvard Medical School, Boston, MA, USA
Full list of author information is available at the end of the article
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 2 of 31http://jcmr-online.com/content/15/1/51
study. Prior to bringing the patient into the scanner room, the physician and technologists should review the patient’s
history and safety screening form to identify implanted devices which may be hazardous in the CMR environment or
produce image artifact. For patients who may have undergone a cardiac procedure and have an
© 2013 Fratz et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution,
and reproduction in any medium, provided the original work is properly cited.
incomplete or unreliable history, a chest radiograph a feeding [11,12]. The baby is undressed, prepared with
should be obtained to assist screening. A detailed ECG-leads and an oxygen saturation probe, and fed. As
discussion on CMR safety and device interactions can be soon as the infant starts falling asleep, it is swaddled or
found elsewhere [8-10]. wrapped in an immobilizer, provided noise protection,
Following safety screening, physiological monitoring and placed on the scanner table. With this “feed, swaddle,
devices and hearing protection (for both awake and and sleep” technique, scanning times of 30–60 minutes
sedated patients) are put in place. Young children can be achieved. However, this approach does not allow
dissipate body heat faster than adults; thus, patient suspension of respiration to reduce motion artifact. As the
temperature should be monitored and blankets applied as study can be compromised by early awakening, the
needed to minimize heat loss. A high-quality imaging protocol should be tailored strictly to the highest
electrocardiogram (ECG) signal is essential for optimum priority clinical questions.
data quality in cardiac-gated sequences. The adequacy of Alternatively, deep sedation can be achieved with a
the signal should be checked not only at the onset when variety of medications (e.g., pentobarbital, propofol,
the patient is outside the scanner bore, but also once fentanyl, midazolam, and inhalational agents). Meticulous
inside it and during actual scanning. In patients with care must be taken to maintain spontaneous breathing
dextrocardia, ECG leads are best placed on the right chest. under the supervision of an experienced anesthesiology
The imaging coil should be chosen to maximize the team. The principal drawbacks of this approach are an
signal-to-noise ratio over the body region to be examined. unprotected airway and reliance on spontaneous
Because CHD often involves abnormalities of the thoracic respiratory effort with the associated risks of aspiration,
vasculature, the coil will usually need to be large enough airway obstruction, and hypoventilation. A laryngeal
to cover the entire thorax and upper abdomen rather than mask airway may be used in conjunction with deep
just the heart. In smaller patients, pediatric thoracic coils sedation to decrease the risk of aspiration. From an image
or coils designed for an adultsized head, shoulder, or knee quality standpoint, respiratory motion artifact may reduce
may be suitable. Adequate coil coverage and placement sharpness. However, images acquired from sedated,
should be confirmed early in the examination by freely-breathing patients are often still of diagnostic
reviewing the localizing images. quality as the breathing pattern tends to be particularly
consistent and thus quite amenable to commonly available
Sedation respiratory motion compensation techniques.
Patients undergoing CMR must remain still in the scanner Because of these safety and image quality concerns, some
for up to 60 minutes to minimize motion artifact during institutions prefer to perform sedation using general
image acquisition and allow planning of successive anesthesia with mechanical ventilation and endotracheal
imaging sequences. Young children (typically less than intubation. This approach consistently achieves adequate
age 6 to 8 years) and cognitively impaired older patients sedation, protects the airway, and offers control of
typically require some form of sedation. Multiple factors ventilation. Respiratory motion artifact can be eliminated
should be taken into account when deciding whether a by suspending ventilation for brief periods (15–60
patient should have an examination with sedation seconds) in conjunction with neuromuscular blockade.
including the length of the anticipated examination Compared to deep sedation, general anesthesia tends to
protocol, developmental maturity, the patient’s experience require more specialized personnel and greater equipment
with prior procedures, the parents’ opinion of their child’s resources (e.g., a magnetic resonance (MR) compatible
capability to cooperate with the examination, the risks of anesthesia machine). Both the deep sedation and general
sedation, and the benefits of the diagnostic information. anesthesia strategies for CMR have been shown to have a
Strategies for sedation and anesthesia during CMR vary good safety profile in this fragile patient population [13-
and often depend on institutional preference and 18]. MR compatible equipment should be used to monitor
availability of resources such as pediatric the heart rate, transcutaneous oxygen saturation, blood
anesthesiologists with experience in CHD. Sedation in pressure, expired carbon dioxide, and body temperature.
infants younger than approximately six months can be An appropriately equipped resuscitation cart and
achieved by allowing them to fall into a natural sleep after emergency management plan for the MR environment
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 3 of 31http://jcmr-online.com/content/15/1/51
should be in place. To maximize patient safety and relaxation time (T1) at 3 T, typically lead to improved
examination quality, it is recommended that different clinical performance of coronary angiography,
healthcare providers be responsible for supervising the contrastenhanced angiography, myocardial tagging, and
imaging and sedation/anesthesia aspects of the study, and myocardial perfusion imaging sequences. However, MR
that both communicate closely with each other. imaging at 3 T has inherently stronger off-resonance
artifacts (B0-field inhomogeneity) and dielectric shading
Gadolinium-based contrast agents artifacts (B1-field inhomogeneity). These factors translate
Gadolinium-based intravenous MR contrast agents to significant dark band artifacts and loss of tissue
(GBCA) are commonly administered in CHD patients of contrast on steady-state free precession (SSFP) pulse
all ages for angiography and the assessment of myocardial sequences and signal loss on spin echo pulse sequences
perfusion and viability. These agents are often used “off- that are unpredictable [26]. Strategies to reduce some of
label” in children as several of them are not approved by these artifacts are currently under evaluation [27]. It is
regulatory agencies, such as the United States Food and also worth noting that implanted metallic devices (e.g.,
Drug Administration or the European Medicines Agency, sternal wires, stents, septal occluders, and vascular
for pediatric-age patients. The incidence of adverse events occlusion coils) are commonly encountered in CHD
related to GBCA in both adults and children is very low patients referred for CMR [28]. Device-related signal loss
[14,19-21]. The vast majority of these reactions are mild artifact from T2* effects is typically more pronounced at
and include coldness, warmth, or pain at the injection site; higher field strengths. Moreover, CMR compatibility
nausea; vomiting; headache; paresthesias; dizziness; and information for devices is more commonly available at the
itching. Severe, life-threatening anaphylactoid or 1.5 T than the 3 T field strength.
nonallergic anaphylactic reactions are quite rare (0.001%
to 0.01%) [22]. There is no evidence indicating Common CMR techniques (modules) in CHD
nephrotoxicity at approved dosages. This section focuses only on established CMR techniques
GBCA administration to patients with acute renal failure which are in routine use throughout the CMR community
or severe chronic kidney disease is associated with the and are available from all scanner manufacturers. The
development of nephrogenic systemic fibrosis (NSF), a authors readily acknowledge that newer applications such
rare and serious condition that involves fibrosis of as 3D phase-contrast flow measurement, real-time and 3D
primarily the skin and subcutaneous tissue but may also cine imaging, and blood pool contrast agents can be useful
involve the lungs, esophagus, heart, and skeletal muscles. when performing CMR in CHD patients.
Patients with an estimated glomerular filtration rate <30
ml/min/1.73 m2 are considered at highest risk. Thus, all Spin echo
patients who are candidates for GBCA administration Spin echo pulse sequences are typically used in CMR to
should be screened for renal dysfunction, and, if generate images in which flowing blood appears dark and
identified, the most recent institutional or national more stationary tissues appear as varying shades of gray
guidelines regarding GBCA use should be consulted or white (Figure 1). The most common variants of this
[22,23]. There are only a small number of reported cases technique are fast (turbo) spin echo (commercial names:
of NSF in children (fewer than 20 as of 2010), the TSE, Siemens; FSE, General Electric; TSE, Philips) and
youngest of which was 8 years of age [24,25], and all had single-shot fast (turbo) spin echo (commercial names:
significant renal dysfunction [22]. No NSF cases have HASTE, Siemens; SSFSE, General Electric; SSTSE,
been reported in preterm or term neonates despite their Philips). Both versions usually employ ECGtriggering to
immature kidney function and estimated glomerular compensate for cardiac motion and preparation pulses to
filtration rates which may be < 30 ml/min/1.73 m 2 [25]. suppress signal from blood and improve image contrast.
Accordingly, caution and a careful assessment of benefits Respiratory motion can be addressed by breath-holding,
and risk but not prohibition are advised when acquiring multiple signal averages, triggering from
administering GBCA to neonates and infants [22,23]. respiratory bellows, or respiratory-navigator gating. By
utilizing half-Fourier k-space filling, the single-shot
Scanner field strength technique acquires all the data to make an image in one
Most CMR is performed on 1.5 T or 3 T scanners. In heartbeat and is thus very time efficient. The fast spin
general, 3 T yields a higher signal-to-noise ratio, and echo technique collects data for one image
therefore allows for better spatial resolution, which is
particularly desirable in younger, smaller patients. This
stronger signal and the inherently longer longitudinal
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Gradient echo cine imaging can be performed using a vasculature in a short scan time, typically less than 30
standard spoiled gradient echo pulse sequence or the seconds (Figure 3). As CHD
subsequently developed SSFP sequence (commercial
names: TrueFISP, Siemens; FIESTA, General Electric;
Infant/small c
balanced-FFE, Philips). SSFP imaging is faster and
provides superior contrast between blood and In-plane resolution (mm) 1.2-2.0
myocardium compared to standard gradient echo imaging
and is thus more commonly used. The SSFP sequence is Slice thickness (mm) 4-6
also relatively less sensitive to flow disturbances caused
Inter slice gap (mm) 0-2
ECG gating
Figure 2 Stainless steel coil artifact.17-year-old patient with dextrocardia, double-outlet right ventricle, and pulmonary stenosis who has
undergone a Rastelli operation and catheter implantation of a single stainless steel vascular coil to occlude a small left superior vena cava
draining to the left atrium. ECG-gated steady-state free precession sequence in a coronal planeA)( and axial plane (B) demonstrating a region of
signal loss in the upper left chest (arrow) resulting from the coil. The area of signal loss is several times larger than the coil and obscures a
portion of the left pulmonary artery. C( ) shows an ECG-triggered fast spin echo sequence with a double inversion preparation pulse acquired in
diastole with a similar orientation as in B( ) With this sequence, the extent of signal loss artifact is reduced, and the left pulmonary artery is more
clearly visualized.
by stenotic or regurgitant jets. However, it is also more Table 2 Cine steady-state free precession
prone to image artifact when there are inhomogeneities in is frequently associated with abnormalities of the chest
the magnetic field (B0) caused by suboptimal scanner vasculature, this technique is often employed in both pre-
shimming or implanted ferromagnetic devices. Thus, the and post-operative CMR imaging protocols. Studies
standard gradient echo technique may be preferred for demonstrating its utility and accuracy in patients with
visualization of flow jets or imaging near implanted CHD have been published for examination of the aorta
devices such as stents and mechanical valves. and its branches, pulmonary arteries, pulmonary veins,
When imaging smaller structures in younger patients, the systemic veins, aortopulmonary and venousvenous
spatial resolution should be increased appropriately (Table collateral vessels, systemic-to-pulmonary artery shunts,
2). Changes to accomplish this (e.g., increased matrix conduits, and vascular grafts [29-34]. The 3D datasets
size, smaller field of view, thinner slice thickness), generated by MRA are well-suited to volume rendered
however, will prolong the echo time (TE). Once the TE displays which can enhance understanding of complex
becomes > 2 ms and the TR > 4 ms, the quality of SSFP spatial relationships and are more comprehensible to non-
imaging often deteriorates. One can increase the matrix CMR specialists (Figure 3). Nevertheless, it is essential
size only in the phase encode direction to improve that the source data be carefully reviewed by the reporting
resolution without prolonging the TE, but this is done at physician as anatomic information may be omitted or
the expense of increased acquisition time. Thus, a careful distorted by the volume rendering algorithm.
balance must be struck between spatial resolution, When possible, MRA should be performed with breath-
acquisition time, and image quality. Alternatively, some holding to minimize artifact from respiratory motion [35].
centers prefer to use high-resolution standard gradient In smaller patients, one should ensure that spatial
echo imaging with free-breathing and multiple signal resolution, both in-plane and partition thickness, is
averages. sufficient. A contrast agent dose of 0.1-0.2 mmol/kg is
typically used. The time delay between the start of
Contrast-enhanced magnetic resonance angiography Magnetic contrast injection and data acquisition will influence
resonance angiography (MRA) using an intravenously which portions of the vasculature will be depicted. This
administered GBCA can produce a high-resolution, high- interval can be determined by a MR fluoroscopic method
contrast three-dimensional (3D) dataset of the entire chest that allows real-time visualization of the arrival of the
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 6 of 31http://jcmr-online.com/content/15/1/51
contrast bolus to the targeted region, by a preceding Another disadvantage is that the use of GBCA incurs
timing run with a smaller dose of contrast, or by some risk of adverse reactions (see above).
automatic bolus detection. Because the effect of the ECG and respiratory navigator-gated 3D SSFP
contrast agent In its typical implementation, the ECG and respiratory
navigator-gated 3D SSFP technique delivers a 3D
anatomic dataset with an isotropic voxel size of
approximately 1.2-2.0 mm without the use of a contrast
agent (Table 3). Its utility and validation have been
reported in patients with CHD [40-42]. Using ECG
triggering, the data acquisition is confined to one or two
portions of the cardiac cycle thereby minimizing blurring
from cardiac motion. Intracardiac anatomy and coronary
arteries can thus be more clearly visualized than with
contrastenhanced MRA. The 3D SSFP sequence is
performed with free-breathing. Respiratory motion is
compensated for by gating data acquisition to expiration
Figure 3 Contrast-enhanced magnetic resonance angiography.
with the use of a navigator beam tracking the motion of
9-year-old patient with partially anomalous pulmonary venous return
of the left upper pulmonary vein (arrow) to the leftward aspect of the diaphragm. This approach allows for improvement in
the left innominate vein. Contrast-enhanced magnetic resonance spatial resolution including isotropic voxel size because
angiogram shown in a coronal plane using a sub-volume maximal scan time is not limited to the duration of a single breath-
intensity projection (A) and volume rendering (B). hold. The isotropic property of the anatomic data permits
arbitrary reformatting in any desired imaging plane during
review without the loss of resolution (Figure 4).
persists even during recirculation, two or three sequential
The 3D SSFP sequence has four principal disadvantages.
MRA data acquisitions are useful to ensure visualization
First, its acquisition time is relatively long, usually
of all the vasculature. More recently, imaging acceleration
approximately 7–10 min, during which the patient must
techniques have been applied to shorten the acquisition
be absolutely still. Younger children may have difficulty
time to 2–5 seconds thereby permitting multiple 3D
with this level of cooperation. Second, the sequence is
volume sets to be acquired as the contrast agent passes
very susceptible to artifacts caused by turbulent flow and
through the circulation producing a “time-resolved” MRA
magnetic field inhomogeneity such as that caused by
[36-39]. A smaller contrast dose (0.05-0.1 mmol/kg) is presence of stents or other ferromagnetic implants.
often used. This time-resolved approach has several Therefore, vessels with stenosis or regurgitation, and
potential advantages: 1) observing the passage of contrast structures around stents can sometimes be misinterpreted.
may have diagnostic benefits, 2) timing of the acquisition Third, the data is confined to one or two portions of the
is less critical because multiple volume sets are obtained cardiac cycle thereby precluding the evaluation of cardiac
as the contrast passes through the circulation, and 3) it and vessel motion. Finally, as with other ECG-gated
may have less sensitivity to respiratory motion artifact. techniques, image quality will suffer when the patient has
The principal disadvantage with this technique is that the an irregular heart rhythm. In such cases, generating stacks
decrease in acquisition time is usually achieved in part of thin SSFP localizer type images in the cardinal planes
from a reduction in spatial resolution which may hinder
during a breath-hold or free-breathing with 2–3 signal
diagnostic accuracy, particularly in smaller patients. In
averages may be a useful alternative.
addition, the undersampling of k-space used to accelerate
A version of 3D SSFP is generally the technique of choice
the acquisition may result in image artifact.
for coronary artery imaging in patients with CHD (Figure
Both the standard and time-resolved contrast MRA 5) [43-46]. For this purpose in particular, data acquisition
techniques do not utilize ECG-gating; therefore, motion must be confined to the rest period of the cardiac cycle
over the cardiac cycle causes blurring, particularly of the (i.e., that with the least motion) to minimize blurring of
aortic root, coronary arteries, and intracardiac structures. these small, fast moving structures.
Table 3 ECG and respiratory navigator-gated 3D steady-state free precession
Infant/small child Large child/adult
The rest period of the heart is chosen by reviewing a high evaluation of the right ventricle or single ventricle. It is a
temporal resolution cine image of the heart (≥50 images key component of the CMR functional evaluation in
per cardiac cycle), usually a 4-chamber view, and patients with CHD.
identifying the appropriate trigger delay and acquisition
(shot) duration. Younger patients will typically have faster
heart rates and thus require a shorter acquisition duration.
Moreover, at higher heart rates (> 90-100 bpm) the
optimal rest period may be in end-systole. If a patient has
difficulty being still during the scan and the primary
diagnostic goal is to visualize the proximal
Ventriculography
CMR ventriculography generates cine images of the
ventricles that enable calculation of ventricular volume,
mass, and ejection fraction as well as evaluation of
regional wall motion. It is a specialized application of
gradient echo cine imaging described above. CMR is
widely considered the clinical reference standard for
ventriculography. It is particularly useful in situations
where echocardiography has significant limitations such
as in patients with poor acoustic windows and the
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Figure 8 Tracing ventricular borders.Diagram demonstrating the drawing of left and right ventricular endocardial contours in end-diastole.
Images may be acquired in a ventricular short-axis orientation A( and B) or in an axial orientation(C and D). There is practice variation regarding
whether to trace the papillary muscles and right ventricular trabeculations to exclude them fromA( and C) versus include them in (B and D) the
blood pool.
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 12 of 31http://jcmr-online.com/content/15/1/51
be allocated. In patients with ventricular conduction A PC CMR pulse sequence produces two sets of cine
delay, which is relatively common in CHD, the images: magnitude images that provide anatomic
endsystolic and end-diastolic frames (i.e., time point in information and phase images in which the velocity
the cardiac cycle) may not be the same for the right and information is encoded. On the phase images, the signal
left ventricles and should thus be selected independently amplitude (brightness) of each voxel is proportional to
to yield the minimum and maximum volumes mean flow velocity within that voxel. Maximum velocity
respectively. There is practice variation regarding whether in one direction is displayed as the brightest white,
to trace the papillary muscles and right ventricular maximum velocity in the opposite direction as the darkest
trabeculations in order to exclude them from blood pool black, and zero velocity as mid-grey. Using specialized
and count them toward ventricular mass (Figure 8) [58- software, regions of interest around a vessel are defined,
61]. Tracing these structures will yield smaller ventricular and the flow rate is automatically calculated from the
volumes, with little change in stroke volume but a higher product of the mean velocity and the cross-sectional area.
ejection fraction. Though theoretically more accurate, this Blood flow measurements are an important element of the
approach is time consuming in the absence of a reliable CMR examination of CHD patients and have variety of
automated system and may reduce measurement applications. Examples include measurement of cardiac
reproducibility. output [74,75], pulmonary-to-systemic flow ratio (Q p/Qs)
Normative data on ventricular parameters by CMR are [76-81], differential lung perfusion [82-85], valvular
available for both adults and older children regurgitation [55,86-94], aortopulmonary collateral flow
[50,52,53,62,63]; there is still a need for robust data in [95-97], and pressure gradient [98-101].
patients younger than 8 years. Given the practice For PC CMR flow measurements, the use of retrospective
variations in the methods of acquiring and analyzing the rather than prospective ECG-gating is preferred so that the
ventriculography image data noted above, it is entire diastolic portion of the cardiac cycle is evaluated
recommended that a center’s approach to these issues (Table 4). The quality of the ECG-gating should be
correspond to that used in the normative dataset that has carefully monitored, particularly during acquisitions
been selected as the center’s reference values. Although lasting several minutes. If the heart rate changes
indexing ventricular volumes to body surface area is a significantly or there are frequent invalid triggers, the
common practice, this does not fully account for changes sequence should be stopped and repeated. Measurements
in body size from infancy to adulthood as the volumes do can be performed with free-breathing and multiple signal
not vary linearly with body surface area averages (2–4) or by shortening the scan time so that it
[52,64,65]. Thus, a given indexed volume (e.g., end- can comfortably be performed within a breath-hold. The
diastolic volume of 80 ml/m2) may be normal for an adult reduced scan time is usually achieved by reductions in
but above normal for an infant. temporal and spatial resolution, as well as faster gradient
One of the strengths of CMR ventriculography is that switching–all of which may increase measurement error.
studies have demonstrated very good reproducibility in Moreover, physiological changes can occur with breath-
children and adults with CHD [58,66-69]. To achieve this holding that alter the measurements [102-104] and may
level of quality and reliability, centers should maintain a confound clinical interpretation. For these reasons, the
rigorous and consistent approach to imaging and analysis. authors recommend free-breathing acquisitions. The scan
Furthermore, to optimize interstudy reproducibility in time of these measurements may be reduced with the use
patients followed longitudinally, the ventricular borders of parallel imaging [80,105,106].
demarcated in the analysis software should be saved so Table 4 Velocity-encoded phase-contrast cine for quantitative flow measuremen
that they can be compared side-by-side with those from Infant/small child
subsequent studies.
In-plane resolution (mm) 1.0-1.3
Blood velocity and flow measurement Slice thickness (mm) 5
Velocity-encoded phase-contrast (PC) cine CMR is the Number of signal averages
primary technique used to measure blood flow velocity
and volume. A detailed description can be found Reconstructed phases per R-R interval
elsewhere [70-73]. In brief, PC CMR is based on the
principle that the signal from hydrogen nuclei (such as Velocity encoding (cm/s) Artery
those in blood) flowing through specially designed Cardiac/respiratory motion Ret
magnetic field gradients accumulates a predictable and Accurate PC CMR measurements require sufficient
measurable phase shift that is proportional to its velocity. spatial resolution to avoid significant partial volume
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effects. Specifically, there should be more than 3 pixels vessel’s or valve’s orientation using two orthogonal
across the diameter or more than 8 pixels in the planning views in order to minimize partial volume
crosssection of the vessel or cardiac valve of interest effects (Figure 10), and the velocity encoding direction
[107,108]. Proper attention to prescribing an appropriate should be set to the through-plane direction. The vessel of
temporal resolution is also essential because under- interest should be as close to the scanner’s isocenter as
sampling will smooth a pulsatile flow curve and cause possible to maximize gradient fidelity (Figure 11). This is
inaccuracies. For PC CMR, true temporal resolution (as accomplished by prescribing the plane so that the center
opposed to interpolated temporal resolution) equals of the image is at the same level as the vessel in the
2•TR•lines per segment (lines per segment is also called superoinferior direction. The scanner will then slide the
views per segment or TFE factor). It is recommended that patient table so that the center of the imaging plane and
a minimum of 20 noninterpolated images be acquired over thus the vessel is close to the scanner’s isocenter.
the cardiac cycle (R-R interval/(2•TR•lines per segment) Placement of the imaging plane in regions of turbulent
≥ 20). At the higher heart rates typically seen in younger flow should be avoided as such flow can lead to signal
children, this will require that the number of lines per loss and inaccuracies. Similarly, positioning of the
segment be decreased to maintain adequate temporal imaging plane away from ferromagnetic implanted
resolution. Finally, with PC CMR measurements, the devices is recommended as these disrupt the magnetic
operator must set the velocity range (v enc) prior to running field gradients.
the pulse sequence; velocities which exceed this range There is some uncertainty and practice variation regarding
will alias and be misrepresented (Figure 9). It is the optimal location for semilunar valve flow
recommended that the venc be set to approximately 25%
above the expected maximum velocity so as to optimize
the dynamic range. When blood velocity is increased,
such as in the setting of valve or vessel stenosis, the
operator’s choice of venc may be guided by information
from recent echocardiography. If aliasing occurs, the
measurement should be repeated using a higher v enc or the
data may be rescaled with cautious use of post-processing
software.
Careful positioning of the PC CMR imaging plane is
essential for accurate velocity and flow measurements. It
should be aligned strictly perpendicular to the blood
Figure 9 Effect of aliasing on phase-contrast cine CMR (PC CMR) flow measurements.Sixteen-year-old patient with surgically repaired
tetralogy of Fallot and mild pulmonary valve stenosis. PC CMR was performed in the main pulmonary artery with the velocity rangeenc (v) set
incorrectly at 200 cm/sec (top row) and then with the evnc set correctly at 300 cm/sec (bottom row). Magnitude (A, D) and phase images (B, E)
in systole, and the resulting flow curves C,( F) generated from analyzing the region of interest (yellow contour) are shown. Because the peak
velocity is 260 cm/sec, aliasing B
( ) and flow underestimation (C) are seen with a venc of 200 cm/sec but not with a venc of 300 cm/sec (E and F).
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 14 of 31http://jcmr-online.com/content/15/1/51
on the principle that administration of a coronary artery build an image as is the case for standard cine CMR. A
vasodilator (e.g., adenosine, dipyridamole, and minimum 3 short-axis slices should be prescribed to
regadenoson) will cause a greater increase in the perfusion ensure coverage of all but the apical left ventricular
of myocardium supplied by normal coronary arteries than segment. Additional short-axis or long-axis slices may
myocardium supplied by stenotic coronary arteries. also be useful. At the slower heart rates typically found in
Perfusion is assessed by administering an intravenous adult patients, the cardiac cycle length is long enough to
dose of a GBCA and then rapidly imaging the ventricles allow acquisition of 3–5 slice locations during each beat
at multiple locations to visualize the enhancement pattern (Figure 13). The slice locations are timed to different
during the first transit of the contrast bolus through the phases of the cardiac cycle but each location is acquired
myocardium. The appearance of contrast will be repeatedly at the same phase. At the higher heart rates
attenuated, both in amplitude and rate, in regions of (and shorter cardiac cycle lengths) seen in younger
compromised coronary blood flow. Typically, a perfusion patients, fewer locations can be acquired in one beat.
scan is run both at rest and with vasodilator infusion in Thus, it may be advantageous to spread the imaging
order to distinguish fixed perfusion defects (e.g., infarct) period for the slices over two heartbeats so that a
from inducible ones. As adenosine is the most commonly sufficient number of locations can be acquired–each
used vasodilator medication, the subsequent discussion location every other beat. Spatial resolution should also be
will focus on this agent. increased in smaller patients.
Vasodilator perfusion CMR has been shown to have Detailed instructions on how to perform an adenosine
similar or superior sensitivity and specificity to nuclear perfusion CMR protocol have previously been published
cardiology techniques for detecting significant coronary [143-145]; the basic steps follow here. Prior to
artery stenosis in adult patients [130-133]. Moreover, the undergoing adenosine perfusion CMR, the patient should
results of perfusion CMR have been shown to have be screened for contraindication to adenosine
prognostic value in adults with coronary heart disease administration including second or third degree heart
[134,135]. Reports of adenosine perfusion CMR for the block, sinus node dysfunction, severe asthma or
assessment of coronary artery disease in children and obstructive pulmonary disease, and pregnancy. Caffeine,
adults with CHD have been limited to small studies [136- aminophyline, and nitrate intake should be avoided on the
140]. It is increasingly being used to assess patients with day of the examination as these agents interfere with the
chest pain, anomalous origins of the coronary arteries, and action of adenosine. A specific consent procedure should
after surgeries which involve coronary artery be undertaken to inform the patient/guardian of potential
reimplantation (e.g., the arterial switch or Ross side effects and complications such as dyspnea, flushing,
operations). However, it is important to note that headache, light-headedness, blurred vision, nausea,
adenosine mainly induces myocardial blood flow bronchospasm, heart block, and hypotension. It is
inhomogeneities by vasodilatation and steal effects that do preferable to have two intravenous lines in separate veins
not necessarily represent the pathophysiology of coronary —one for adenosine and one for contrast agent
artery problems found in CHD patients. Furthermore, it is administration—in order to avoid a bolus dose of
unclear whether exercise induced ischemia caused, for adenosine with contrast administration. Monitoring
example, by an anomalous coronary artery coursing equipment should include a continuous ECG recording
between the arterial roots can be detected by adenosine and blood pressure cuff placed on the arm not being used
perfusion CMR. In some settings it may, therefore, be for the adenosine infusion. Equipment and qualified
preferable to use other “stress” agents such as dobutamine personnel for resuscitation must be available.
[141] or another imaging modality in conjunction with Table 5 T1-weighted vasodilator perfusion
exercise stress. saturation-recovery acquisition first followed
Vasodilator perfusion CMR has been performed using a gradient echo for first pass by the rest acquisition
variety of pulse sequences; a detailed review can be found myocardial perfusion with at least 15 minutes
elsewhere [142]. In brief, strong T1 contrast is provided between
Infant/small child the two so as to
by a preparation pulse such as inversion recovery or minimize contamination
saturation recovery (Table 5). This is followed by fast In-plane resolution (mm) of the rest images by
imaging using a gradient echo, gradient echo-planar, or Slice thickness (mm) residual contrast given
SSFP acquisition. Parallel imaging techniques are widely Image acquisition timing 1 R-R during
or 2 R-R the vasodilator
used as a means for accelerating image acquisition. These The consensus group infusion. An adenosine
sequences create images of the heart in one heartbeat authors recommend dose of 0.14 mg/kg/min is
rather than acquiring data from multiple cardiac cycles to performance of the typically used though the
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 17 of 31http://jcmr-online.com/content/15/1/51
adequacy and safety of infusion is discontinued. (LGE) images [147]. In a true subendocardial
this dose has not been Adenosine should be the absence of LGE, perfusion defect, this dark
thoroughly established in terminated earlier if the homogeneous rim artifact typically lasts
the pediatric age group. patient develops persistent enhancement in all for only a few heartbeats
After the adenosine has or symptomatic heart locations at rest and with and then fades away. The
been infusing for 3 block, significant the vasodilator indicates dark rim artifact is more
minutes, a GBCA (0.05- hypotension, or severe no inducible ischemia. A commonly seen with high
0.1 mmol/ kg) is rapidly respiratory difficulty. An region with transmural heart rates, a more
injected followed by a intravenous dose of LGE and perfusion concentrated contrast
saline flush. In adultsize aminophylline can be used defects at rest and with bolus, and the use of a
patients, rates of 5 ml/s to rapidly counteract the the vasodilator, a balanced SSFP rather than
with 25 ml of flush are effects of adenosine. The socalled “fixed defect”, a gradient echo based
recommended. In same contrast infusion is also interpreted as the perfusion sequences.
children, a minimum rate protocol and pulse absence of inducible
of 3 ml/s through an sequence parameters as ischemia. A region that Late gadolinium
appropriate size used in the adenosine has a perfusion defect enhancement
intravenous line and 10 perfusion segment should with vasodilator but is LGE, also known as
ml flush is suggested. be used later for the rest normal at rest and has no myocardial delayed
The perfusion imaging perfusion imaging. LGE is diagnostic of enhancement, is a
sequence is started Though quantitative ischemia. Perfusion technique that detects
Figure 13 Schematic diagram illustrating data acquisition timing in a first-pass perfusion sequence. Each rectangle represents data
acquisition to form one complete image and the numbers inside them correspond to different slice locations. At a heart rate of 60 bpm A),( the
cardiac cycle length is long enough to allow acquisition of 4 slice locations during each beat. The slice locations are timed to different phases of
the cardiac cycle, but each location is acquired repeatedly at the same phase in subsequent cycles. At a heart rate of 120 bpm B),( the cardiac
cycle length is shorter so only two slice locations can be acquired over each beat; the other 2 locations are acquired the following beat. Note
that the temporal resolution (images per unit time) is the same inA and B.
simultaneously with the analysis of perfusion defects should be focal regions of
contrast agent infusion, imaging [146] is possible reported as either full myocardial fibrosis and
and its scanning duration using commercially thickness or partial infarction. It is based on
should be set to acquire available image analysis thickness (sub- the observation that
approximately 60 software, this process endocardial) with the GBCA have slower
heartbeats. In order to remains time-consuming affected region of the left washout and an increased
minimize respiratory to perform and is subject ventricle described using volume of distribution in
motion artifact, breathing to technical challenges. the standard 17-segment fibrotic and necrotic
should be suspended as Visual analysis by an American Heart myocardium. Thus, such
long as possible during experienced reader is Association model [148]. areas appear brighter than
the image acquisition. If usually sufficient for On some perfusion scans normal myocardium on
breath-holding is not routine clinical practice. there may be a rim of LGE images. Validation
possible, the patient Interpretation is also reduced signal intensity studies have correlated the
should be instructed to guided by review of the in the subendocardium, finding of LGE with the
breathe shallowly. Once cine images of ventricular which can mimic a presence and extent of
the imaging is function and late hypoperfused area myocardial fibrosis
completed, the adenosine gadolinium enhancement [145,149]. Compared to detected by histology in
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 18 of 31http://jcmr-online.com/content/15/1/51
resolution for the thin- Slice thickness (mm) increased and that of usually improved contrast
walled RV [172]. Thus Views per segment abnormal myocardium against the bright
high spatial resolution is decreased (or even enhanced regions.
Number of signal averages
required to properly nulled) leading to gross
Image acquisition timing 3 R-R or 4 R-R
assess for LGE on thin- misinterpretation. If the
Trigger delay Diastole
walled ventricles. TI orissystole
set too long, the Disease-specific protocols
Performing the LGE scanner’s no-trigger relative contrast between This section provides
technique in children interval and double the normal and abnormal suggested disease-specific
requires modifications to data acquisition interval. myocardium will be CMR protocols using the
address smaller-sized In addition, the data reduced and sensitivity modules reviewed above.
ventricles and faster acquisition (shot) duration diminished. For conciseness, the
heart rates (Table 6). In should be decreased by Ghosting artifacts can ventriculography and LGE
order to ensure adequate reducing the views per result from regions that modules are listed once in
spatial resolution, voxel segment (turbo factor) to have a long T1 such as detail at the beginning and
size should be 1.0-1.5 minimize blurring from pericardial fluid or then simply referred to in
mm in-plane with a faster cardiac motion at cerebrospinal fluid [174]. the disease-specific
thickness of 5 mm. The the higher heart rate. Artifact from protocols. Similarly, the
resulting decreased Although image analysis cerebrospinal fluid can abbreviations used in the
signal-to-noise ratio can software can be used to be removed by protocols are listed below
Figure 16 Schematic diagram illustrating data acquisition timing in a late gadolinium enhancement sequence. Each rectangle represents
data acquisition timed to coincide with the cardiac rest period and during which a user-defined number ofk-space lines are filled. Multiple data
acquisitions and thus cardiac cycles are required to fillk-space and produce an image. At a heart rate of 80 bpm(A), data acquisition occurs
every second cardiac cycle in order to allow sufficient time for recovery of longitudinal signal. At a heart rate of 120 bpmB),( the cardiac cycle
length is shorter so the sequence is modified to acquire data every third cycle in order to maintain the same time for the recovery of
longitudinal signal. In addition, the data acquisition duration is shortened to compensate for the briefer cardiac rest period associated with a
faster heart rate.
be compensated for by objectively quantify the Finally, subendocardial, for easy reference. PC
performing two signal extent of enhanced papillary muscle, and CMR acquisitions are with
averages, albeit at the myocardium [173], right ventricular wall throughplane velocity
expense of a longer qualitative visual enhancement may be Ventriculography
acquisition time. At interpretation is typically inconspicuous when
module (see
higher heart rates (>100 performed in clinical adjacent to a relatively
bpm), in order to allow practice. The involved bright blood pool. ventriculography
time for adequate cardiac segments can be Interpreting the LGE section above for
longitudinal signal reported according to the images side-by-side with
recovery between 17-segment left the cine images details) Standard
successive
Table inversion
6 T1-weighted ventricular model [148] addresses this pitfall as imaging
inversion-recovery gradient and a 9-segment right these will provide
echo for late gadolinium ventricular model [155]. information regarding 1. Cine CMR: left
enhancement In addition, it is helpful to wall thickness and ventricular 2-
note the extent of the wall
Infant/small child papillary muscle position chamber and
thickness that is involved [174]. Moreover, 3chamber views,
In-plane resolution (mm) and the pattern of performing LGE imaging
enhancement (e.g., later after contrast agent
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 20 of 31http://jcmr-online.com/content/15/1/51
section
above for
details)
Standard
imaging
1. LGE imaging in
left ventricular 2-
chamber and
3chamber views,
right ventricular 1. Cine CMR: long-
3-chamber view, axis aortic arch
4-chamber view plane (Figure 1)
2. LGE imaging 2. Ventriculography
with a stack of module
contiguous slices
tocompletely
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 21 of 31http://jcmr-online.com/content/15/1/51
n a r anoblique sagittal
plane
d l d perpendicular to
the atrial septum
u to completely
encompass the
m d i atrial septum
(Figure 17)
e 3. Ventriculography
m
module
a f
a 4. PC CMR: AAo,
MPA
t e
g Additional case-
r c specific/comprehensive
i imaging
i t
1. PC CMR: 1–3
n
contiguous slices
a
g positioned parallel
to the atrial septal
l S
1. Cine CMR: stack plane to obtain an
t of contiguous en face view of
thin slices in a the defect (Figure
s a 4chamber plane 17), and with
to completely through-plane
e
n encompass the velocity encoding
atrial septum 2. PC CMR: stack of
p contiguous thin
d 2. Cine CMR: stack
of contiguous slices in a
t
a thin slices in 4chamber plane
Figure 17 Secundum atrial septal defect (ASD) imaging protocol. A.Axial steady-state free precession (SSFP) image in a 10-year-old with a
large secundum ASD (white arrow).B. The axial SSFP image is used to plan a stack of oblique sagittal SSFP images to visualize the ASD and the
superior and inferior defect margins. C. The axial and oblique sagittal images are used together to plan a stack of phase-contrast (PC) cine images
to visualize the ASD flowen face. This provides insight into the oval shape of the defect and may demonstrate additional ASDs.
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 23 of 31http://jcmr-online.com/content/15/1/51
and/or in an mid-abdomen s c
oblique sagittal tothe top of the
plane aortic arch t
perpendicular to 2. Cine CMR:
the atrial septum v
oblique plane to
to completely image the
e S
encompass the anomalousvein(s)
atrial septum, in long-axis n t
and with in-plane 3. Ventriculography
velocity module o a
encoding in the 4. CE-MRA or 3D
direction of atrial SSFP to image the s
n
septal defect thoracicvasculatur
flow e (Figure 3) u
d
3. CE-MRA or 3D 5. PC CMR: AAo,
SSFP to image MPA, branch PAs s
a
the Additional case-
thoracicvasculatu specific/comprehensive r
re imaging s
Key reporting d
1. PC CMR:
elements: number anomalous vein e
and location of the Key reporting elements:
p
defects, defect rim number, location, i
measurements, and drainage of the t
ventricular pulmonary veins; m
a
parameters, Qp/Qs ventricular
a
parameters; Qp/Qs, l
Partially anomalous
branch pulmonary g
pulmonary venous
artery flow
connection, before or distribution i
d
Figure 18 Sinus venosus septal defect imaging protocol. A.Axial steady-state free precession (SSFP) cine image in a 22-year-old with a large
sinus venosus septal defect (white arrow).B. The axial SSFP image is used to plan a stack of oblique sagittal SSFP cine images to visualize the
defect in an orthogonal view and assess its superoinferior dimension.
after repair Standard Si e n
imaging n f g
1. Cine CMR: axial
stack from the u e
Fratz et al. Journal of Cardiovascular Magnetic Resonance 2013, 15:51 Page 24 of 31http://jcmr-online.com/content/15/1/51
Figure 19 Ebstein anomaly imaging protocol. A.Right ventricular 3-chamber view (RV 3C) steady-state free precession cine image in a 22-year
-old with Ebstein anomaly. In this example, the functional tricuspid valve plane is displaced and inflow is directed into the right ventricular
outflow tract (white arrow). B. The RV 3C image is used to plan a stack of cine images to visualize the displaced tricuspid valve orifice
en face for
anatomic assessment or flow quantification.
defect, drainage of 4. PC CMR: AAo, operation
3. Ventriculograph Left ventricle; IVC: Inferior vena authors thank Emily Harris for S, Stern H. Routine clinical
cava; MPA: Main pulmonary her assistance with the cardiovascular magnetic
y module resonance in paediatric and adult
artery; MR: Magnetic resonance; preparation of the figures.
4. CE-MRA or 3D MRA: Magnetic resonance congenital heart disease: patients,
SSFP to image angiography; NSF: Nephrogenic Author details protocols, questions asked and
systemic fibrosis; PAs: Pulmonary 1 Department of contributions made. J Cardiovasc
the Pediatric Cardiology Magn Reson. 2008; 10:46.
arteries; PC CMR: Velocity-
thoracicvasculatu encoded phase-contrast cine CMR; and Congenital Heart 4. Bailliard F, Hughes ML, Taylor AM.
re Qp/ Qs: Pulmonary-to-systemic Disease, Introduction to cardiac imaging in
Deutsches Herzzentrum infants and children: techniques,
5. PC CMR: AAo, flow ratio; RV: Right ventricle;
München (German Heart Center
RVOT: Right ventricular outflow potential, and role in the imaging
native MPA, Munich) of the work-up of various cardiac
tract; SA: Short-axis; SSFP: Steady-
branch state free precession; SVC:
Technical University Munich, malformations and other pediatric
Munich, Germany. 2Department heart conditions. Eur J Radiol.
PAs,SVC, IVC Superior vena cava; TE: Echo time;
of Diagnostic 2008; 68:191–98.
Additional case- TFE: Turbo field echo; TI: Inversion
Imaging, Children’s Hospital & 5. Marcotte F, Poirier N, Pressacco J,
time; TR: Repetition time; venc:
specific/comprehensiv Velocity encoding range. Research Center Oakland, Paquet E, Mercier LA, Dore A,
e imaging Oakland, California, USA.
3Department of Pediatric
Ibrahim R, Khairy P. Evaluation of
adult congenital heart disease by
1. Cine CMR: long- Competing interests Cardiology, Evelina Children’s cardiac magnetic resonance
The authors declare that they have Hospital/Guy’s and St. Thomas’ imaging. Congenit Heart Dis. 2009;
axis aortic arch no competing interests. Hospital NHS Foundation Trust; 4:216–30.
plane Division of Imaging Sciences & 6. Prakash A, Powell AJ, Geva T.
2. LGE module Authors’ contributions
Biomedical Engineering, King’s Multimodality noninvasive
College London, London, UK.
3. PC CMR: SF drafted and conceived of the 4The Herma
imaging for assessment of
congenital heart disease. Circ
tricuspid and review, designed the initial
Heart Center, Children’s Hospital Cardiovasc Imaging. 2010; 3:112–
structure of the manuscript,
mitral coordinated author
of Wisconsin, Medical College of 25.
Wisconsin, Milwaukee, WI, USA.
valves,pulmonar communication, and revised the 5Centre for Cardiovascular
7. Kilner PJ, Geva T, Kaemmerer H,
Trindade PT, Schwitter J, Webb
y veins authors’ contributions to produce Imaging, UCL Institute of GD. Recommendations for
the draft version of the
Key reporting Cardiovascular Science, & Great cardiovascular magnetic
manuscript; TC drafted the Ormond Street Hospital for resonance in adults with
elements: Fontan ventriculography section; GFG Children, London, congenital heart disease from the
drafted the contrast-enhanced
pathway, SVC, UK. 6Division of Cardiology, respective working groups of the
MRA and 3D SSFP sections; MMS University Children’s Hospital European Society of Cardiology.
IVC, branch PA, provided extensive editorial Zurich, Zurich, Eur Heart J. 2010; 31:794–805.
assistance; AMT drafted of the Switzerland. 7Department of
pulmonary vein, 8. Zikria JF, Machnicki S, Rhim E,
vasodilator perfusion section; Diagnostic Imaging and Division Bhatti T, Graham RE. MRI of
and aortic arch ERVB drafted the sedation section; of Cardiology, patients with cardiac pacemakers:
SJY drafted the blood velocity and Department of Paediatrics,
obstruction; Fontan flow measurement section; AJP Hospital for Sick Children,
a review of the medical literature.
AJR Am J Roentgenol. 2011;
baffle defects; drafted the LGE and patient University of Toronto, 196:390–401.
preparation sections, and revised Toronto, Ontario, Canada.
ventricular and synthesized all of the authors’ 8Department of Cardiology,
9. Levine GN, Gomes AS, Arai AE,
Bluemke DA, Flamm SD, Kanal E,
parameters; valve contributions to produce the final Boston Children’s Hospital, and Manning WJ, Martin ET, Smith JM,
version of the manuscript. All the Department of Pediatrics,
regurgitation; Harvard Medical School, Boston,
Wilke N, Shellock FS. Safety of
authors contributed substantially magnetic resonance imaging in
aortopulmonary to the design of the review, MA, USA. patients with cardiovascular
collaterals critically revised the manuscript devices: an American Heart
Received: 9 April 2013 Accepted:
for important intellectual content, Association scientific statement
Abbreviations 8 May 2013
and read and approved the final from the Committee on
2C: 2-chamber; 2D: 2- Published: 13 June 2013
manuscript. Diagnostic and Interventional
dimensional; 3C: 3-chamber; 4C: Cardiac Catheterization,
4-chamber; 3D: 3dimensional; References Council on
Acknowledgements
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The authors thank Mark A. Fogel,
Atrial septal defect; CEMRA: Evaluation of Cardiovascular Council on Cardiovascular
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cardiovascular magnetic resonance in children and adults with
congenital heart disease: SCMR expert consensus group on congenital
heart disease.Journal of Cardiovascular Magnetic Resonance2013 15:51.
we perform delayed
enhancement