Group Title: Journal of Cardiovascular Magnetic Resonance 2008, 10:33
Title: Strain-encoding cardiovascular magnetic resonance for assessment of right-ventricular regional function
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Title: Strain-encoding cardiovascular magnetic resonance for assessment of right-ventricular regional function
Series Title: Journal of Cardiovascular Magnetic Resonance 2008, 10:33
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Creator: Youssef A
Ibrahim ESH
Korosoglou G
Abraham MR
Weiss RG
Osman NF
Publication Date: 39633
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Volume ID: VID00001
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: Open Access: http://www.biomedcentral.com/info/about/openaccess/

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Journal of Cardiovascular Magnetic 0

Resonance BioMed Centra


Research


Strain-encoding cardiovascular magnetic resonance for assessment
of right-ventricular regional function
Amr Youssef*1,2, El-Sayed H Ibrahim3, Grigorios Korosoglou4,5, M
Roselle Abraham', Robert G Weiss1,4 and Nael F Osman4,6


Address: 'Department of Medicine, Division of Cardiology, Johns Hopkins University, Baltimore, MD, USA, 2Cardiology department, Ain Shams
University, Cairo, Egypt, Department of Radiology, University of Florida, Jacksonville, FL, USA, 4Russell H. Morgan Department of Radiology and
Radiological Science, Johns Hopkins University, Baltimore, MD, USA, 5University of Heidelberg, Department of Cardiology, Heidelberg, Germany
and 6Department of Electrical and Computer Engineering, Johns Hopkins University, Baltimore, MD, USA
Email: Amr Youssef* asyoussef@yahoo.com; El-Sayed H Ibrahim elsayed.ibrahim@jax.ufl.edu;
Grigorios Korosoglou gkorosoglou@hotmail.com; M Roselle Abraham mabraha3@jhmi.edu; Robert G Weiss rweiss@jhmi.edu;
Nael F Osman nael@jhu.edu
* Corresponding author



Published: 4 July 2008 Received: 3 June 2008
journal of Cardiovascular Magnetic Resonance 2008, 10:33 doi:10.1 186/1532-429X- 10- Accepted: 4 July 2008
33
This article is available from: http://www.jcmr-online.com/content/10/1/33
2008 Youssef 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.



Abstract
Background: Tissue tagging by cardiovascular magnetic resonance (CMR) is a comprehensive
method for the assessment of cardiac regional function. However, imaging the right ventricle (RV)
using this technique is problematic due to the thin wall of the RV relative to tag spacing which limits
assessment of regional function using conventional in-plane tagging.
Hypothesis: We hypothesize that the use of through-plane tags in the strain-encoding (SENC)
CMR technique would result in reproducible measurements of the RV regional function due to the
high image quality and spatial resolution possible with SENC.
Aim: To test the intra- and inter-observer variabilities of RV peak systolic strain measurements
with SENC CMR for assessment of RV regional function (systolic strain) in healthy volunteers.
Methods: Healthy volunteers (n = 21) were imaged using SENC. A four-chamber view was
acquired in a single breath-hold. Circumferential strain was measured during systole at six
equidistant points along the RV free wall. Peak contraction is defined as the maximum value of
circumferential strain averaged from the six points, and regional function is defined as the strain
value at each point at the time of peak contraction.
Results: Mean values for peak circumferential strain ( standard deviation) of the basal, mid, and
apical regions of the RV free wall were -20.4 2.9%, -18.8 3.9%, and 16.5 5.7%, Altman plots
showed good intra- and inter-observer agreements with mean difference of 0. I 1% and 0.32% and
limits of agreement of -4.038 to 4.174 and -4.903 to 5.836, respectively.
Conclusion: SENC CMR allows for rapid quantification of RV regional function with low intra-
and inter-observer variabilities, which could permit accurate quantification of regional strain in
patients with RV dysfunction.




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Open Access







Journal of Cardiovascular Magnetic Resonance 2008, 10:33



Background
Despite the rapid advances in the field of cardiovascular
imaging over the past decade, assessment of the right ven-
tricular (RV) function is still challenging [1]. However,
accurate assessment of RV function is an important pre-
dictor of clinical outcome in patients with congenital
heart disease, pulmonary hypertension [2,3], myocardial
infarction [4,5], heart failure [6], dilated cardiomyopathy
[7], and arrhythmiogenic RV dysplasia (ARVD) [8].

Cardiovascular Magnetic Resonance (CMR) with its supe-
rior tissue contrast, high spatial and temporal resolution,
and non-invasive nature is an important modality for
assessment of global RV function [9]. By imaging the
induced magnetization of different tissues, and not just
their anatomic borders, CMR provides greater flexibility in
imaging the structure and function of the heart. Specifi-
cally, in CMR tagging, parallel planes of saturated magnet-
ization can be applied orthogonal to the imaging plane,
which create non-invasive MR-visible markers, or tags,
that move with the contraction of the heart [10,11] and
permit quantification of its strain [12] in the three-coordi-
nate directions (circumferential, longitudinal, and radial).
With advances in signal processing, the amount of dis-
placement of these tags within the myocardium can be
automatically quantified using harmonic phase (HARP)
analysis, which allows for rapid and accurate analysis of
myocardial regional function [13 CMR tagging is consid-
ered the gold standard technique for assessment of left
ventricular (LV) regional function [14]. However, the thin
wall of the RV (normally < 5 mm) results in tags those are
too far apart for accurate assessment of thin walled RV
regional function.

In this work, we propose to use the through-plane tags in
strain encoding (SENC) CMR [15] in order to overcome
the limitations posed by the thin-walled RV and to allow
for quantitative assessment of the RV regional function.
SENC CMR has several advantages over regular tagging: 1)
Spatial and temporal resolution are improved. 2) The sig-
nal intensity depends on the spacing of the invisible tags
in the through-plane direction, which allows for strain
calculation in the direction perpendicular to the imaging
plane [16]. Because of the latter, circumferential strain can
be measured from the long-axis view, while the presence
of the tags does not affect visualization of different cardiac
structures. 3) The circumferential strain of the RV free wall
can be measured from a single four-chamber view instead
of multiple short-axis views in conventional tagging.
Despite these theoretical advantages, the value of SENC
CMR for studying human RV function has not been inves-
tigated thoroughly. In this study, the intra- and inter-
observer variabilities of SENC CMR were evaluated for
assessment of RV regional function in healthy volunteers.


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Methods
The study was approved by the Institutional Review Board
of Johns Hopkins Medical Institutions, and informed con-
sent was obtained from all participants prior to the MR
exam. The study was Health Insurance Portability and
Accountability Act (HIPAA) compliant.

Volunteer selection
Healthy volunteers (n = 21) with no history of heart dis-
ease and no abnormal cardiac structure or function were
studied by CMR.

SENC CMR
SENC CMR is based on the acquisition of two images with
different frequency modulation, or tuningss", in the slice-
selection direction. We call these images the low-tuning
(LT) and high-tuning (HT) images. Bright regions in the
LT and HT images represent static and contracting tissues,
respectively [16]. The two SENC images were combined as
described in [16] to result in a strain image, where signal
intensity is proportional to through-plane strain. Strain
measurements calculated from SENC images have
recently been validated against standard Spatial Modula-
tion of Magnetization (SPAMM) tagged images [17,18].
Figure 1 shows a diagram of the SENC pulse sequence
[16]. It consists of two major modules: tagging and imag-
ing. The tagging part is implemented after the detection of
the R-wave of the electrocardiogram (ECG), and it is com-
posed of two 900 non-selective radiofrequency (RF)
pulses interspersed by a modulation gradient in the slice-
selection direction and followed by crusher gradients in
all directions. A spectral-selective fat suppression RF pulse
was applied immediately before the tagging module [19].
Imaging started directly after the tagging module, where a
series of slice-selective RF pulses were applied with alter-
nating SENC modulations tuningss) and ramped flip
angles [20]. K-space was filled in a segmented fashion
with spiral acquisition for efficient readout.

CMR scan protocol
Studies were performed on a 3.0T MR scanner (Philips
Medical Systems, Best, The Netherlands) using a 6-ele-
ment phased-array cardiac coil. Four ECG leads were
placed on the volunteers' chests for triggering the pulse
sequence at the R-wave of the ECG. The volunteers' posi-
tion was head first and supine. After initial scouting
images and reference scan, gradient echo vertical long axis
cine (pseudo two-chamber view) images were obtained
from the coronal images by aligning the left ventricular
apex with the center of the mitral valve. From the end-
systolic vertical long-axis image, an initial horizontal
long-axis plane (pseudo four-chamber view) was
obtained by aligning through the apex and the midpoint
of the mitral valve. Then, a single short-axis plane was
obtained from the end-systolic horizontal long axis


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Journal of Cardiovascular Magnetic Resonance 2008, 10:33


SS Cm .'-her
I I I
i ,ng n t n ,,




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SSpirnl Aquition



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Figure I
SENC pulse sequence diagram (FS: fat suppression, RF: radiofrequency, SS: slice selection, PE: phase encod-
ing, RO: readout, HT: high-tuning, LT: low-tuning).


image. The final four-chamber view was obtained from
the-short axis plane by bisecting both ventricles and going
parallel to the diaphragm. The measurement points on
the SPAMM and SENC images were determined with the
help of the geometry scouting images, in order to assure
that the measurement positions in the SPAMM images
correspond to their counterparts in the SENC images.

The imaging parameters for the gradient echo cine acqui-
sitions were: repetition time (TR) = 5 ms; echo time (TE)
= 2.9 ms; flip angle = 15 ; scan matrix = 176 x 138 recon-
structed to 256 x 256 pixels; field of view (FOV) = 35 x 35
cm; and slice thickness = 8 mm. Four-chamber SENC
images were then acquired during a single breath-hold of
13 heartbeats using prospective ECG gating. SENC imag-
ing parameters were similar to those of the cine images,
except for: spiral acquisition (for efficient signal readout)
with 12 spirals x 12 ms; scan matrix = 176 x 176; TR =
14.4 ms; TE = 0.8 ms; flip angle = 40 ; and slice thickness
= 8 mm. For SENC images, the temporal resolution was
15 msec and the spatial resolution was 2 x 2 x 8 mm3.
Finally, dynamic short-axis SPAMM grid-tagged images
were acquired at the same locations as the cine images,


and with similar imaging parameters, except for: TR = 12
ms; TE = 1.8 ms and flip angle = 35 .

CMR data analysis
Tagging and SENC CMR data were analyzed using the
HARP and SENC software packages (Diagnosoft Inc., Palo
Alto, California), respectively. For each four-chamber
SENC image (Figure 2), six points were manually selected
(by observer AY) along the RV free wall in the end systolic
frame, starting from the base toward the apex with equal
distances from each other. Systolic circumferential strain
was calculated at each of the six points on the SENC
image, as described in [16]. Strain estimates were also
computed from the short-axis SPAMM tagged images, as
described in [13]. Myocardial strain was defined here as
the percentage change in tissue length from the resting
state at end-diastole (ED) to the one achieved following
myocardial contraction at end-systole (ES): Myocardial
strain = (ED ES)/ED x 100%.

In order to detect the timing of end-systole in the SENC
cine, the time point of maximum average strain was
selected to represent end-systole with the peak systolic



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I


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Journal of Cardiovascular Magnetic Resonance 2008, 10:33


Figure 2
Four-chamber SENC CMR view at the end-systolic frame. A) The RV as appears on the acquired image before soft-
ware processing. B) The processed image showing the position of the six points along the RV free wall and the corresponding
strain curve. Y-axis shows the strain values while the X-axis shows the time frames.


strain is the stain estimate recorded at this time point as
shown in figure 2B at time frame 21.

The SENC derived myocardial strain values were calcu-
lated by the same observer (AY) two weeks after the first
reading to report the intra-observer variability. The strain
values were also calculated by a second independent
observer (GK), blinded to the results obtained by the first
observer, to determine inter-observer variability. SENC
and SPAMM strain estimates of the interventricular sep-
tum were calculated by the first observer, using the same
method described above, to serve as a reference for the RV
free wall strain estimates.

Strain noise was then calculated for the RV free wall in the
21 SENC CMR scans. This was done by quantifying the
noise in the strain estimate by examining a small region
around points within the base, mid and apical RV free
wall and reporting the standard deviation in the strain
estimate at those points. The standard deviation in the


strain estimates were divided by the mean strain estimates
at those regions. Then, SENC strain estimate was corre-
lated with strain noise. A subgroup of SENC CMR scans
with the least strain noise and absence of image artifacts
were then selected. The purpose of this sub-grouping was
to examine the effect of image quality on the intra- and
inter observer variabilities of the strain estimates.

Statistical analysis
Statistical analysis was performed using commercially
available software (STATA, version 9.2, College Station,
Texas). Strain estimates were presented as mean + stand-
ard deviation (SD). Circumferential strain estimates were
compared using a paired t-test for normally distributed
data, Wilcoxon signed rank sum test for non-normally dis-
tributed data. Multiple measures analysis of variance
(ANOVA) analysis was used to compare the average cir-
cumferential strain measurements of the base, mid, and
apical parts of the RV free wall. P < 0.05 was considered
statistically significant.


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Journal of Cardiovascular Magnetic Resonance 2008, 10:33



Intra- and inter-observer agreements were evaluated using
the 95% limits-of-agreement approach proposed by
Bland and Altman [21], by plotting the differences
between each pair of measurements against their means.
"Limits of agreement" was presented as mean difference +
2 SD. Assuming normal distribution, it is expected that
most differences (>95%) would lie between mean 2SD
and mean + 2SD (limits of agreement). To test if the vari-
ances of strain estimates were the same within the same
observer and between observers, Pitman's test [22] for cor-
related variances was used. Also, linear regression analysis
was performed between the end-systolic circumferential
strains of the RV free wall measured by the first observer
two weeks apart, and between the first and second observ-
ers. Intra-observer and inter-observer variabilities were
calculated from the linear regression analysis using the
intra-class correlation coefficient (r).

Results
Twenty-one healthy volunteers with ages ranging from 23
to 45 years (mean age of 35 7 years standard deviation)
were included in the study. All the scans were done at
Johns Hopkins University during the year 2006. The aver-
age scanning time was 35 minutes. All the images
acquired from the twenty-one studies were suitable for
analysis. The contracting RV gives bright signal on the
four-chamber SENC CMR against a dark background (Fig-


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Base


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ure 2). The acquired images were then processed for strain
analysis using the SENC software.

The peak circumferential systolic strain estimates of RV
free wall and interventricular septum
The average peak circumferential strain of the RV free wall
measured by SENC CMR was -18.7 4.3% (the minus
sign means positive contraction). The average strain +
standard deviation for the basal, mid, and apical regions
of the RV free wall were -20.7 2.8%, -19.1 + 3.3% and -
16.9 + 4.8%, respectively (Table 1 and Figure 3). There is
a statistically significant difference in the SENC circumfer-
ential systolic strain estimates among the base, mid and
apical segments of the RV free wall (P = 0.0015). Myocar-
dial areas of consistent low circumferential strain were
found in 8 out of the 21 scans close to the site of insertion
of the papillary muscle into the RV free wall (Figure 4).

The average RV free wall circumferential strain measured
from the short-axis SPAMM tagged slices in the same sub-
jects was -18.5 2.7% (P = 0.42). The SPAMM circumfer-
ential strain estimates for the base, mid, and apical slices
of the RV free wall were -18.8 2.5% (P = 0.03), -18.5 +
2.7% (P = 0.35) and -18.3 3.0% (P = 0.08), respectively.
There is no statistically significant difference in the
SPAMM circumferential systolic strain estimates between


Mid-wall


Apex


Figure 3
Box-and-whisker plots of peak SENC strain estimates for the base, mid-wall and apex of the RV free wall. The
whiskers are drawn from the box to the highest and lowest values that are within 1.5 times the interquartile range of the
median with any points more extreme than this are plotted individually.




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T








Journal of Cardiovascular Magnetic Resonance 2008, 10:33


Table I: The average values for SENC peak circumferential systolic strain estimates of the RV free wall.


Region/Observer


Basal segment of RV
free wall
Middle segment of RV
free wall
Apical segment of RV
free wall


Average SENC peak
systolic strain estimate
( SD) measured by the
Ist observer


-20.7% ( 2.8)

-19.1% ( 3.3)

-16.9% ( 4.8)


Average SENC peak
systolic strain estimate
( SD) measured by the
I st observer (second
time)


-20.4% ( 2.8)

-19.0% ( 3.4)

-16.7% ( 5.1)


Average SENC peak
systolic strain estimate
( SD) measured by the
second observer


-19.9% ( 2.9)

-19.6% ( 3.8)

-17.8% ( 4.6)


Average SPAMM peak
systolic strain estimate
( SD) (P value)



-18.8% ( 2.5) (P = 0.03)

-18.5% ( 2.7) (P = 0.35)

18.3% ( 3) (P = 0.08)


the base, mid and apical segments of the RV free wall (P =
0.67).

The average value of the circumferential peak systolic
strain estimate of the interventricular septum was -21.2
3.2% as measured by SENC CMR in four-chamber view


and -20.6 2% (P = 0.14) as measured by HARP analysis
of grid tagging in short-axis views. The SENC circumferen-
tial strain estimates for the base, mid, and apical slices of
the interventricular septum were -20.5 2.7%, -21.7
3.1% and -20.3 3.0%, respectively. Compared with
SENC circumferential systolic strain estimates of the RV


Figure 4
Site of attachment of the papillary muscle into the RV free wall shows area of low strain as compared to the
rest of the RV free wall. A) Gradient echo image with the arrow pointing to the papillary muscle. B) Same view on SENC
CMR. C) SENC strain analysis showing area of low strain estimate on RV free wall corresponding with the site of attachment
of papillary muscle.




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Journal of Cardiovascular Magnetic Resonance 2008, 10:33



free wall, there was no significant difference between the
basal segments (P = 0.13), while mid and apical segments
of the RV free wall were significantly less (P < 0.01) than
those of the interventricular septum.

Intra-observer and inter-observer agreements
Regional peak circumferential systolic strain measure-
ments demonstrate low intra- and inter-observer variabil-
ities (Figure 5) as indicated by the interclass correlation
coefficient (r = 0.82/0.81; 0.80/0.79; 0.94/0.81 for the
basal, mid, and apical regions, respectively). The overall
intra- and inter-observer variabilities were r = 0.88 and
0.80, respectively.

Bland Altman plots have shown the mean difference
between the SENC strain estimates obtained by the same
observer to be 0.11% (95% confidence interval = -0.24%
to 0.46%) and between the two observers to be 0.32%
(95% confidence interval = -0.14 to 0.79%). The intra-
observer and inter-observer limits of agreement were -
4.038 to 4.174 and -4.903 to 5.836, respectively (Figure
6). There was no significant intra-observer or inter-
observer difference in variances (Pitman's coefficient [r] =
0.1, P = 0.28; and [r] = 0.14, P = 0.13, respectively).

Effect of image quality on strain estimates, intra- and
inter-observer agreements
The SENC average peak circumferential systolic strain esti-
mates from the group of subjects with highest image qual-
ity was 1.8% (-20.5 2.8% versus -18.7 4.3%, P < 0.02)
higher than the average strain estimates. Also, there was
slightly higher agreement among the group of highest
image quality scans than the average agreement on Bland


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Altman plots with a mean intra-observer difference of
0.027% (95% confidence interval = -0.53% to 0.58%)
and inter-observer difference of 0.30% (95% confidence
interval = -0.35 to 0.94) and limits of agreement of -3.3 to
3.3 and -3.5 to 4.1 for the intra-observer and inter-
observer, respectively (Figure 6).

Discussion
This study demonstrates that circumferential strain of the
RV free wall can be obtained using SENC CMR with low
intra- and inter-observer variabilities. The average RV free
wall circumferential strain estimate with SENC (-18.9
4.1%) was in good agreement with previous results
obtained by CMR tagging [23] using one-dimensional
SPAMM tagging. In that study, the RV free wall average cir-
cumferential strain in normal volunteers ranged from -
16.4 1% in the RV outflow tract to -22.4 1.5% at the
RV apex. However, the lower strain values of the RV apex
in our study could be attributed to 1) the method of
selecting the points for strain analysis from areas with low
signal (e.g., around the insertion site of the papillary mus-
cle); and/or 2) the weaker signal captured from the thin
walled apex in low image quality studies, which resulted
in abnormally low strain values, shown as outliers in Fig.
3. In our study, the SPAMM grid-tagged circumferential
systolic strain estimates from the apical portion of the RV
free wall was -1.4% higher than the SENC strain estimates,
but this difference did not reach statistical significance (P
= 0.08). With not much difference in the strain estimates
between SENC and SPAMM grid tagging for the RV free
wall, the major advantages of SENC are 1) obtaining the
entire strain data from a single view rather than 3 short-
axis views in grid tagging; 2) better visualization of the


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Figure 5
Intra and inter-observer variabilities as indicated by interclass correlation co-efficient (r) on linear regression
analysis.




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Intra-observer Agreement


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Average strain estimate


intra-observer Agreement in higher image quality scans
















-2 -21 -14 -7 0
Average strain estimate


Inter-observer Agreement








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Average strain estimate


Inter-observer Agreement in higher image quality scans
















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Figure 6
Bland-Altman plots for intra-observer and inter-observer agreements. Higher image quality scans showed higher
degree of agreements. In all plots, the dashed lines represent the mean difference and the gray shaded areas represent the lim-
its of agreements.


contracting myocardium which allows for more accurate
localization of the region of interest; and 3) the resulting
strain curves are interpretable from the entire RV free wall.

To be more confident about our strain estimates and to
avoid any systematic bias, we used both SENC and
SPAMM grid-tagging circumferential strain estimates of
the interventricular septum, where excellent strain curves
were obtained in almost all subjects, as a reference. There
was no significant difference in the circumferential strain
estimates of the interventricular septum between the
methods (-21.2 + 3.2% for SENC CMR versus -20.6 + 2%
for SPAMM grid tagging (P = 0.14)). Also, there was no
significant difference between the basal segments of RV
free wall and interventricular septum (P = 0.13). However,
the circumferential strain estimates of the mid and apical
segments of the RV free wall were significantly less (P <


0.01) than those of the interventricular septum. This
could be attributed to the lower strain SNR of apical
regions in images with marginal quality or the attachment
site of the papillary muscle into the RV free wall in other
images.

The completely automatic calculation of RV strain values
with SENC produces good intra-observer and inter-
observer agreement. This was particularly evident in the
high-quality images where there is less noise to confound
the actual strain results.

The effect of image quality on circumferential myocardial
strain quantification was also addressed in our study. The
average RV circumferential strain measured from the
group of scans with the least strain noise and image arti-
fact was found to be statistically significant higher than



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Journal of Cardiovascular Magnetic Resonance 2008, 10:33



the average strain estimate of the 21 studies (-20.5 2.8%
versus -18.7 4.3%, P < 0.02). Also, plotting the SENC
strain estimates against noise in the strain estimates
revealed a significant linear relation. It should be noted
that SENC imaging is one type of STEAM (stimulated-
echo acquisition mode) pulse sequence, which suffers
from 50% signal loss, making SENC imaging sensitive to
image SNR.

Circumferential strain measurements were conducted in
this study based on the observation that myocardial con-
traction is principally circumferential [24]. On the con-
trary, tissue Doppler data suggested that RV contraction is
mainly longitudinal [25]. However, tissue Doppler could
only reliably calculate the longitudinal functional param-
eters of the RV due to its thin wall [26]. Another study of
the RV strain in open-chest, open-pericardium animal
models [27] showed that the RV longitudinal strain corre-
lates with the RV global function during both basal condi-
tions and following an increase in afterload, whereas
circumferential strain is influenced by changes in after-
load. This could make circumferential strain analysis even
more specific and clinically useful in pressure overload
conditions, like pulmonary hypertension, which consti-
tute the majority of RV pathologies.

Overall, it should be noted that the use of spiral acquisi-
tion for data readout, automated software for strain anal-
ysis and acquisition of circumferential strain estimates for
the entire RV from a single four-chamber view made the
entire process time-efficient and practical.

Study limitations and future directions
As this study was conducted only on normal volunteers,
one limitation is that the diagnostic utility of the strain
measurements were not tested on patients with known RV
dysfunction. However, this did not interfere with the aim
of this study which was mainly designed to test the feasi-
bility and applicability of circumferential strain estimates
of the RV free wall as a surrogate of function before testing
this method on patients with RV dysfunction. It should be
noted that although the current study addressed intra-
observer, inter-observer and inter-subject reproducibility,
the scan-rescan reproducibility for the same subjects was
not examined. This point is intended to be addressed in a
more comprehensive future study.

It should also be noted that evaluation of regional heart
function, which naturally occurs in the three dimensions,
from a single circumferential plane is another limitation
of the method used. Also, the imaging technique used did
not correct for tissue through-plane motion that could
affect the accuracy of the strain estimates. However, devel-
opment of new methods for tissue slice-following [28]


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and motion tracking [29] could correct for this through-
plane displacement.

Finally, areas with consistent low circumferential strains
were found at the insertion site of the papillary muscle
into the RV free wall. These areas are not likely identified
in prior studies relying on imaging techniques with intrin-
sically lower spatial resolution. These findings direct
attention to the cautious interpretation of strain estimates
in light of image quality and the presence or absence of
image artifacts, especially in high-field CMR systems.

Conclusion
SENC CMR allows for rapid quantification of RV regional
function with low intra- and inter-observer variabilities,
which could permit accurate quantification of regional
function in patients with RV dysfunction.

Competing interests
Dr. Nael F. Osman is a founder and shareholder in Diag-
nosoft Inc. The terms of this arrangement have been
approved by the Johns Hopkins University in accordance
with its conflict of interest policies.

Authors' contributions
AY participated in the study design and CMR exams, car-
ried out the image and statistical analysis, and wrote and
revised the manuscript. EHI assisted in the development
of the CMR pulse sequence and participated in the CMR
exams. GK participated in the analysis of the CMR data
and in manuscript editing. MRA participated in the study
design. RGW participated in the study design and critically
reviewed the manuscript. NFO conceived and supervised
the study and participated in its revision. All authors read
and approved the final manuscript.

Acknowledgements
The authors would like to thank Ahmed S. Fahmy, PhD; Li Pan, PhD and
Hugh Wall for their help in MR imaging, as well as Dr. Shenghan Lai and his
team for their help in recruiting volunteers.

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