(Circulation. 1995;91:2359-2370.)
© 1995 American Heart Association, Inc.
Articles |
Regional Left Ventricular Systolic Function in Relation to the Cavity Geometry in Patients With Chronic Right Ventricular Pressure Overload
A Three-Dimensional Tagged Magnetic Resonance Imaging Study
From the Department of Medicine (S.J.D., Y.F.P., D.W.B., I.B., E.R.S., J.V.T.) and Department of Radiology (A.P.C., J.H.M.), University of Calgary, Alberta, Canada, and the Heart System Research Center (R.B.), Technion-IIT, Haifa, Israel.
Correspondence to Rafael Beyar, MD, DSc, Department of Biomedical Engineering, Technion-Israel Institute of Technology, Haifa 32000, Israel.
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Abstract |
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 Top Abstract IntroductionMethods Results Discussion References |
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Background Distortion of the left ventricular (LV) cavity in patients with right ventricular pressure overload (RVPO) is well known. However, no direct measurements of regional myocardial function in terms of myocardial shortening and wall thickening are available; therefore, exactly how RVPO disturbs LV regional performance remains unclear. By using three-dimensional (3D) tagged magnetic resonance imaging, we were able to measure regional systolic function directly. Our objective was to study the relation between the distortion of the LV circular shape and regional LV function.
Methods and Results In nine patients with RVPO and six healthy volunteers, four parallel short-axis images (with 12 radial tags) and two mutually orthogonal long-axis images (with four parallel tags) were generated, and endocardial and epicardial borders were manually traced. By integration of the short- and long-axis images, 3D reconstruction of the LV tracking points from end diastole to end systole was obtained. Data from the midventricular two short-axis image slices were analyzed. These were then divided into anterior, lateral, posterior, and septal regions. Circumferential and longitudinal shortening were then calculated from the endocardial and epicardial tag intersection points. Wall thickness and thickening were calculated by the 3D volume-element approach. An eccentricity index (EI), the ratio of septum-to-free-wall to anteroposterior diameters, was used to describe the shape of the LV cavity. The regional curvature was also measured. The RVPO group was characterized by flattening of the septum and LV lateral wall, decreased EI reflecting the distorted LV shape, altered distribution of endocardial circumferential shortening, and preserved ejection fraction. Changes in EI closely correlated with the septal curvature. The EI was smaller at end systole, reflecting further shape distortion relative to end diastole. Reduced myocardial performance, as measured by wall thickening and circumferential and longitudinal shortening fractions, was observed for the septum. A reduction in endocardial circumferential shortening of the septal and lateral walls was directly related to the end-systolic EI. In addition, whereas for healthy subjects a linear relation between area ejection fraction and endocardial circumferential shortening was observed, in RVPO patients a curvilinear (quadratic) relation was observed.
Conclusions In patients with RVPO, compared with healthy subjects, the septal function was reduced, as evidenced by reduced thickening and shortening fractions. The distortion in LV cavity at end systole due to the flattening of the septum contributes to preserved systolic ventricular function and nonuniform distribution in endocardial circumferential shortening.
Key Words: ventricles • pressure • systole • magnetic resonance imaging
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Introduction |
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TopAbstractIntroductionMethods Results Discussion References |
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It is well recognized that, in the conditions of both acute and chronic right ventricular pressure overload (RVPO), the left ventricular (LV) cavity is distorted by the flattening or leftward displacement of the ventricular septum.1 2 3 4 5 6 7 8 9 10 11 12 13 Since the myocardial fibers of RV free walls are connected with those of the septum and LV free walls and since the septum is common to both LV and RV, RVPO and the septal flattening should be accompanied by changes in the LV regional systolic function. Using acute animal models, we9 and others14 15 have shown that acute RVPO induced by pulmonary arterial constriction leads to a decrease in LV regional end-diastolic segment length as well as to a decrease in systolic segment shortening (both septum and free walls)14 15 ; these segmental changes are heterogeneously distributed circumferentially14 15 and transmurally.16 In chronic RVPO, however, the LV systolic regional function has been poorly elucidated because of the limitations of the methodology: two animal studies from the same group measured regional segment shortening at only one location by a pair of sonomicrometry crystals,17 18 and one human study measured the planar thickness and thickening of the septum and LV posterior wall by M-mode echocardiography.19 There has been no study on patients with RVPO in which regional segment shortening is directly measured, since such measurements typically require myocardial markers, which greatly limit clinical applicability.
Magnetic resonance imaging (MRI) tagging is a recently developed technique20 21 by which presaturation tags can be noninvasively placed at any location in the myocardium and at any phase of the cardiac cycle. Tagging the myocardium at end diastole and following the tags to end systole enables direct measurement of regional systolic myocardial deformation. Since this accounts for the motion of the heart in both longitudinal and circumferential directions, the LV can be precisely reconstructed in three dimensions (3D),22 23 permitting accurate measurements of strain in the different directions. Furthermore, the 3D volume-element approach has been validated as presenting an accurate measurement of myocardial thickness and thickening, an accurate parameter reflecting local myocardial function, and is advantageous over the standard planar methods.24 25
We hypothesized that large changes in shape of the LV imposed by RVPO might alter load distribution in the LV and thereby alter regional ventricular functions. Our objective, therefore, was to study the relation between the LV distortion and global and regional functions in patients with chronic RVPO. By using MRI tagging and 3D reconstruction, we measured LV regional systolic function in terms of systolic circumferential and longitudinal segment shortening as well as wall thickening. By observing these relations, we could demonstrate that the septum and the lateral wall that are flattened by RVPO exhibit reduced regional function in proportion to the degree of LV distortion. To compensate for that, a bellows-like motion of the septum toward the LV free wall in these patients, probably generated by the high systolic pressure on the right side of the septum, helps to maintain global LV ejection fraction despite the reduced regional function in the septum and lateral wall.
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Methods |
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Patient Selection
Nine patients, three men and six women, 20 to 61 years old (mean±SD, 38±15 years), with various degrees of chronic RVPO were studied (Table 1
). All patients were in sinus rhythm,
were in either class I or II (cardiac function according to the New
York Heart Association classification), and had no contraindications
for MRI. Peak systolic RV pressure, as estimated by the Doppler
technique, ranged from 51 to 120 mm Hg. A control group of six healthy
volunteers, five men and one woman, 31 to 40 years old, was also
studied for comparison.
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MRI Acquisition
MRI was performed on a Signa 1.5-T scanner
(General Electric Co
Medical Systems). After the patient had been positioned in the magnet,
six series of images were acquired: the first four series were planning
scans to ascertain the orientation of the heart, the location of the
image and tag planes for series 5 and 6, and the timing of end systole;
series 5 and 6 were performed to obtain the final images for the
study.
First, a nongated single sagittal image at the left parasternal border was acquired to quickly locate the heart (series 1). From this, a coronal multislice spin-echo image encompassing the silhouette of the heart from series 1 was acquired (series 2). The coronal slice that covered the largest LV cavity area and included the aortic valves was selected, and a "cine" scan (series 3) was generated for that slice. End systole was then identified as the moment at which the LV cavity was the smallest and preceding which aortic flow reversed. From the coronal image with largest LV cavity area in series 3, we selected an oblique long-axis image plane that passed through both the LV apex and the aortic orifice and acquired two cardiac-phase gated spin-echo images, at end diastole and end systole (series 4).
From the oblique
long-axis images at end systole, four parallel
short-axis image planes (perpendicular to the long axis) were
identified (series 5). Basal and apical planes were first located. The
basal plane passed just below the mitral valves and cut through the
muscular septum. The apical plane passed just above the apical
endocardium. The remaining two midventricular image planes were then
defined to trisect equally the interval between the basal and apical
planes. The tag lines were placed at end diastole by six tag planes
perpendicular to the image planes (I through VI in Fig 1A),
separated by 30° of arc, that were made to
intersect along the long axis of the LV, producing 12 radial tag lines
in each short-axis image, with one of the tag planes intersecting the
midseptum at the midventricular level (see Fig 2). Two
mutually orthogonal long-axis image planes (series 6) were identified
from the short-axis images, with one plane superimposed on the tag
plane that cut through the middle of the ventricular septum (imaging
planes 1 and 2 in Fig 1B). Four parallel tags were placed at
the
corresponding end-diastolic short-axis image plane
locations (Fig 1B). (As can be seen in Fig 2,
our program places six
parallel tag planes rather than four; however, having ensured that the
lower four tag planes were aligned with the four short-axis image
planes, we ignored the additional two planes that were above the valve
level.) Gated acquisition of the four parallel short-axis images at
four time points (from end diastole to end systole) and two orthogonal
long-axis images (at end diastole and end systole) was accomplished by
a multislice, multiphase spin-echo technique (echo time, TE, of 14 ms;
recovery time, time to repetition, TR, equal to the RR interval). The
gated images were acquired by entering the desired delay after the R
wave. The parameters for these images were a 256x128 matrix, two
averages, 32- to 40-cm field of view, 1.25- to 1.56-mm pixel size, and
a 10-mm slice thickness. All series except for the tagged series
included flow compensation. The tagged series included asymmetric
echoes instead. For both the short- and long-axis images, the tags were
placed at end diastole and persisted (for about 500 ms) to end systole.
By following the motion of the tags, in the short-axis images, we could
assess the rotation of each tag intersection point, and in the
long-axis image, we could assess the magnitude of short-axis
through-plane motion.
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Data Analysis
Image Processing
The images were
transferred to an IBM-compatible personal
computer (Pack-mate 386X/25, Packard Bell) on which the original MRI
data were linearly converted to a PC image file (an array of 256x256
gray levels). LV endocardial and epicardial borders on the short-axis
images were manually marked at the intersection with each of the 12
tags. An Akima26 smoothing algorithm was used to
interpolate between the points of intersection, and one interpolated
point was created midway between adjacent marked points. The resulting
smooth contour was superimposed on the image for comparison. The
contour point was adjusted until satisfactory matches with the
endocardial and epicardial borders were obtained. The tracing procedure
resulted in two (LV endocardial and epicardial) sets of four (slice)
contours at both end diastole and end systole. Each of these output
files contained 24 data points: 12 manually marked points of
intersection and 12 interpolated points. (Twenty-four segments were
then produced by connecting corresponding endocardial and epicardial
points.)
We also traced the intersections between tags and endocardial and epicardial borders of the long-axis LV images to calculate the degree of base-to-apex translation of the short-axis images.
3D
Reconstruction With Correction for Base-to-Apex Translation of
Short-Axis Images
As seen in the long-axis images in the bottom panel
of Fig 2
, as
the heart contracts, the myocardial tag lines moved downward toward the
apex, which moved hardly at all. The magnitude of this systolic descent
(which was calculated as the pixel difference between end diastole and
end systole times the pixel dimension) decreased from the basal to the
apical slice and was linearly related to the end-diastolic
(tag) distance from the epicardial apex (Fig 3).
Therefore, the image-acquisition technique produced
end-diastolic and end-systolic images that were identical
in terms of their location in space but were obtained from different
myocardial segments (because of base-to-apex translation).
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To correct for this longitudinal translation, we used an algorithm that was detailed in our previous study23 and is similar in principle to that used by Azhari et al22 for the calculation of principal strains in the myocardium. (In that study, the accuracy of tracking tag intersection points was validated by a moving phantom, and the strain results in dogs were similar to those reported when metal markers were used.27 ) This algorithm matches the short- and long-axis images to obtain the complete 3D information and calculates the corrected position of the tag-endocardial and tag-epicardial intersections of the end-systolic short-axis images through a linear interpolation. The new interpolated points are the physical points that have translated with the muscle, both in the short-axis plane and in the long-axis direction, to its end-systolic location. This procedure was performed to calculate the endocardial and epicardial points for all four slices.
Calculation of
Geometric Parameters
To minimize the interference of the stiffer
mitral valve orifice
and because the LV apex is free of attachment of the RV free wall and
is considerably different in shape from the equatorial slices, we
analyzed only the data from the middle two slices of the short-axis
images, which defined a 3D muscle ring. We then divided the ring into
four equal regions: anterior, lateral, posterior, and septal (each of
the regions contained three tag lines [Fig 1C]). From
the tracings of
the upper and lower surfaces of this equatorial ring (ie, short-axis
images 2 and 3), the following parameters were calculated and averaged
to yield the measurements of the ring. The LV cross-sectional cavity
area was calculated as the area within the tracing, and the area
ejection fraction (EF) was calculated as
EF=(Aed-Aes)/Aed, where
Aed and Aes were the end-diastolic
and end-systolic areas, respectively. The LV septum-to-free wall
diameter (Ds-fw) and anteroposterior diameter
(Da-p) were measured as the distances between the
endocardial surfaces along the tag lines (or planes), which were the
planes of two mutually perpendicular long-axis images. The diameter
shortening fraction was calculated as
(Ded-Des)/Ded, where
Ded was the end-diastolic and Des
was the end-systolic diameter. The LV cavity shape was estimated by the
eccentricity index (EI), which was calculated as the ratio of
Ds-fw to Da-p.
The 3D muscle ring (Fig
1C) was divided by connecting the corresponding
points that defined each of the 24 segments in each surface (four
points for each segment of each plane) into 24 3D volume elements (Fig
1D), from which the regional curvature, thickness and
thickening, and
circumferential shortening were calculated.
Regional curvatures of the midwall surface were calculated in both circumferential and meridional directions with an algorithm reported previously by Lessick et al.28 29 In brief, the midwall points are calculated for both end diastole and end systole from the corresponding endocardial and epicardial data points. This generates a matrix of 24x3 midwall points for both end diastole and end systole. In addition, midwall points between slices were also calculated by linear interpolation. Surface elements were defined by three adjacent points on each of every two adjacent cross sections, creating by that a total of 3x12 surface elements. The curvatures were calculated at the center of the three midslice points in each surface element. The principal curvatures in the circumferential and meridional directions are calculated as follows. Local tangents to the midwall surface are approximated and then used in the following equation:
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where Kj is curvature in the j direction; j is circumferential or meridional direction; ti is tangent vector at points i=a and b; a and b are points located before and after the central point at which the curvature is calculated in the circumferential case or below and above it in the meridional case; and Ds is the segment length between points a and b.
The curvature in a plane perpendicular to the endocardial surface is then given by
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where
is the angle between the normal (ni) in
the plane containing the data points and a local normal
(Ni) to the endocardium. The latter is the vector (A,B,C),
where A, B, and C are the coefficients of the local tangent plane at
the surface:
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This local tangent plane is estimated by least-squares fitting of four points on the surface element, located symmetrically around a midslice central point. The calculation of curvatures required knowledge of the normal vectors at points on either side of the central point in the circumferential case and at midslice points below and above it in the meridional case. The least-squares method was used for this step, followed by calculation of the normal to the plane passing through these three (horizontal or vertical) midslice data points. This was done by the cross-product of two vectors defined by these points. The tangent vectors at the three points were then calculated by the cross-product of their local normals to the surface and the normal to the plane on which they were located. Finally, the vector ni was calculated from the cross-product of the tangent vector at the central midslice point and the normal to the plane passing through the points.
At the end of the procedure, circumferential data for three levels for circumferential curvature and for the midlevel for the meridional curvature were present. The data for curvature for the middle slice were used here in conjunction with the corresponding data on thickening and circumferential shortening.
Thickness was calculated for each of the 24 3D volume elements by use of a 3D volume-element approach.24 25 Briefly, we first calculated the endocardial (Aendo) and epicardial (Aepi) surface areas and the volume (V) of the element geometrically. Thickness (T) was then calculated as T=2V/(Aendo+Aepi), and thickening fraction (Th) as Th=(Tes-Ted)/Ted, where Ted and Tes were the end-diastolic and end-systolic thicknesses, respectively.
Circumferential segmental
lengths of both endocardium and epicardium
were measured in each segment of each slice (Fig 1D). Regional
shortening fraction (Sh) was calculated as
Sh=(Led-Les)/Led, where
Led was the end-diastolic and Les
the end-systolic circumferential segmental length. The shortening
fraction of the volume element in the circumferential direction was
then calculated as the averaged shortening of these two slices.
Longitudinal shortening was calculated as the shortening fraction
between apical and basal tag lines as measured from
end-diastolic and end-systolic long-axis images. LV
volumetric EF was calculated from the end-diastolic and
end-systolic volumes between the basal and apical slices of the
short-axis images. Muscle volume was calculated accordingly.
Statistical Analysis
The values are expressed as
mean±SEM. ANOVA was used to assess
the significance of the differences between the different regions with
Student-Newman-Keuls test for multiple comparisons. Student's unpaired
t tests were used to compare the differences in global and
cavity dimensional parameters between RVPO patients and normal
subjects. Student's paired t tests were used to compare the
calculations obtained with and without the corrections for the
base-to-apex translation. A value of P
.05 was considered
to be significant.
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Results |
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LV Cavity Dimensions and Regional Curvature
An example of a distorted LV at end diastole and end systole in a patient with severe RVPO is shown in Fig 2
. Note the flattening
of the
septum and the severe distortion of the LV cavity typical of this
condition. The EI was decreased in RVPO patients compared with healthy
subjects at both end diastole and end systole (Table 2).
(The smaller the EI, the more distorted the LV.) This EI was smaller at
end systole than at end diastole (P=.06),
representing flattening of the septum during systole in this
group of patients (Table 2). As seen in Fig 4,
both
volume and area EFs in patients with RVPO were not significantly
different from those of healthy subjects. In RVPO patients, the
shortening fraction of the anteroposterior diameter,
Da-p, was decreased compared with healthy subjects,
but there was no difference in the shortening fraction of the
septal–to–free wall diameter, Ds-fw, between
patients with RVPO and healthy subjects (Fig 4).
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In
contrast to the healthy subjects, in whom there were no significant
differences in either circumferential or meridional (midwall)
curvatures between the regions, the regional curvatures varied in
patients with RVPO (Table 3). Circumferential curvatures
were smaller at the septum and lateral wall than those at anterior and
posterior regions at both end diastole and end systole. Meridional
curvatures were smaller at septal and posterior regions than those at
anterior and lateral regions at end diastole only. Compared with the
healthy subjects, the circumferential curvatures at the septal and
lateral regions were significantly decreased.
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To examine the
correlation between the regional curvatures and LV
distortion, we related the curvatures to the EI. As shown in Fig
5, there was an inverse relation between curvature at
the anterior region and EI (Fig 5A) and a direct relation
between the
septal curvature and EI (Fig 5D). In addition, a tendency
toward a
direct relation between the curvature at the lateral region and EI
(P=.09, Fig 5B) was also observed. No relation
between
curvature and EI was observed at the posterior region (Fig 5C).
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Thickness and Thickening
The end-diastolic thickness in
patients with RVPO was
significantly greater than that in healthy subjects only in the septal
regions (11.0±0.9 versus 8.4±0.3 mm, P<.05), whereas
there was no significant difference in absolute thickening between RVPO
and healthy subjects (range, 3 to 3.6 mm and 3.9 to 4.7 mm,
respectively); thickening fraction was reduced in all regions in
patients with RVPO (range, 0.28 to 0.36 versus 0.48 to 0.56,
respectively) (Fig 6). In healthy subjects and in
patients with RVPO, neither thickness nor thickening was significantly
different between the different regions. LV muscle volume was
calculated for the imaged portion of the LV (excluding base and apex).
As indicated by the increased septal thickness, LV hypertrophy in RVPO
patients was suggested by these measurements as well (LV muscle volume
of 49.3±4.0 mL in healthy subjects versus 67.6±5.1 mL in RVPO,
P=.02).
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Longitudinal Shortening
As shown in Fig 7,
longitudinal shortening fraction
was smaller at every region in RVPO than that in healthy subjects, but
significantly so at the septum (0.13±0.01 versus 0.20±0.01,
P<.01, at the endocardium and 0.09±0.03 versus
0.18±0.01,
P<.05, at the epicardium) and anterior wall (0.13±0.02
versus 0.19±0.02, P<.05, at the endocardium and
0.10±0.02
versus 0.18±0.03, P<.05, at the epicardium). There was no
significant difference between the regions in either RVPO or healthy
subjects. The longitudinal shortening tended to be greater in the
endocardium than at the epicardium in both groups (19% to 20% versus
16% to 18% in the healthy subjects and 13% to 18% versus 9% to
14% in RVPO, respectively, P=NS).
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Circumferential Shortening
In patients with RVPO, the
endocardial segmental shortening
fraction in the septum was significantly less than in the other
regions, and the epicardial segmental shortening fraction was greater
in the lateral wall than in posterior regions (Fig 8).
In healthy subjects, the difference in endocardial segmental shortening
fraction was not significant between the regions, and epicardial
segmental shortening fraction was significantly greater in the anterior
wall than in the posterior and septal regions (Fig 8). The
endocardial
shortening fraction in patients with RVPO was significantly reduced in
the lateral and septal regions compared with the healthy subjects
(0.30±0.03 versus 0.42±0.05, P=.05, and
0.17±0.04 versus
0.34±0.02, P<.01, respectively), whereas the epicardial
shortening fraction was significantly decreased only in the anterior
region (P<.005) (Fig 8).
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Relations Between Regional Endocardial Circumferential Shortening
and LV Geometry
As expected, in the healthy subjects there was a close
linear
relation between area EF and mean endocardial circumferential
shortening fraction (r=.99, P<.001) (Fig
9,
top). However, the relation between area EF and mean
endocardial circumferential shortening fraction in patients with RVPO
was better described by a quadratic equation (r=.87,
P<.05) (Fig 9, bottom), indicating that factors
other than
circumferential shortening also play a role in determining the area
EF.
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In patients with RVPO, the endocardial circumferential segmental
shortening fraction in the lateral and septal walls was closely related
to the LV end-systolic cavity shape. There was a linear relation
between end-systolic EI (an indicator of the LV cavity shape) and both
lateral (r=.70, P<.05) and septal
(r=.83, P<.01) endocardial circumferential
segmental shortening fraction (Fig 10B and
10D). There
was no such relation for the anterior and posterior regions (Fig
10A and 10C).
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Comparison of Results Before and After the Correction of
Base-to-Apex Translation
Without the correction for the base-to-apex
translation and
therefore longitudinal shortening, the muscle mass of the 3D volume
elements would be expected to be greater at end systole than at end
diastole. On the average, end-systolic mass was 30% greater than
end-diastolic mass in the healthy subjects and 20% in RVPO
without the correction for base-to-apex translation. However, with the
correction, the mass of the volume elements at end systole was 5% less
than at end diastole in the healthy subjects and 3% less in RVPO.
There were no significant differences in the measurements of
end-systolic thickness, absolute thickening, and fractional thickening
with or without the correction. Circumferential shortening was smaller
without the correction than with the correction: 0.28±0.02 versus
0.37±0.03 (P<.05) and 0.04±0.01 versus
0.10±0.02
(P<.05) for the endocardial and epicardial shortening of
the healthy subjects, respectively, and 0.23±0.02 versus
0.27±0.02
(P=NS) and 0.04±0.01 versus 0.07±0.01
(P<.05)
for endocardial and epicardial shortening of RVPO, respectively.
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Discussion |
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TopAbstractIntroductionMethods Results Discussion References |
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By MRI tagging and 3D volume-element reconstruction, we directly measured regional function in patients with RVPO and related it to LV cavity shape. In patients with RVPO, (1) the LV cavity was distorted as measured by the eccentricity index, and this distortion was greater at end systole than at end diastole because of the systolic flattening of the septum; (2) while global ventricular ejection fraction was within the normal range, septal and lateral wall myocardial performance was reduced; (3) endocardial circumferential shortening, which was reduced for the septal and lateral regions, corresponded to a parallel decrease in the shortening of the anteroposterior diameter, Da-p; and (4) in contrast to the linear relation between the area ejection fraction and mean circumferential endocardial shortening fraction in the healthy subjects, there was a curvilinear relation in the RVPO group.
Alterations in LV Geometry in RVPO
Changes in the LV cavity
shape in chronic RVPO observed here are
similar to previous
data.2 3 4 5 11 12 13
The LV cavity at end
diastole and end systole is distorted from the normal circular shape by
a flattening or inversion of the septum. Reflecting the flattening of
the septum, the eccentricity index decreased significantly in RVPO
patients compared with healthy subjects. Although factors such as
myocardial contractile performance,2 force balance at the
junctions,30 compressive stress on the RV surface of the
septum,30 31 and LV transmural
pressure32
might affect the systolic septal shape and position, the main
determinant is the degree of RVPO. Previous studies have shown a close
correlation between the pressure difference10 or the
pressure ratio2 3 between RV and LV and septal shape
and
position. After relief of the RVPO, the septum returned to its normal
position.5
The circumferential curvature at the lateral
free wall was reduced in
patients with RVPO compared with the anterior and posterior regions and
compared with the lateral region in the healthy subjects (Table
3).
This observation is different from that of others3 who
divided the LV circumference into two (ie, septal and free wall)
regions and, therefore, did not report significant alterations in LV
free-wall circumferential curvature. Indeed, when we pooled and
averaged all the regional free-wall curvatures, we did not detect any
curvature difference in LV free wall between RVPO patients and healthy
subjects (0.040±0.002 versus 0.039±0.002 mm-1
at
end diastole and 0.050±0.003 versus 0.051±0.003
mm-1 at end systole, respectively). Regional
variations in the meridional curvature between the three free-wall
segments were observed only at end diastole in patients with RVPO: the
curvature of the posterior region was significantly smaller than that
of the anterior and lateral regions (Table 3).
Septal and Ventricular Hypertrophy
LV hypertrophy is
suggested here by the increase in septal wall
thickness and LV muscle volume in patients with RVPO compared with
healthy subjects. A number of animal studies have clearly shown that
septal hypertrophy exists in RVPO produced by pulmonary arterial
banding17 18 33 34 35
or emphysema36 and that
the magnitude of the hypertrophy is well correlated with the duration
of RVPO.33 The thickness of the LV free wall also tended
to be greater than in the healthy subjects, but the difference was not
statistically significant. This phenomenon has also been demonstrated
in animal33 35 and human pathological37
studies.
Systolic Function of the Ventricular Septum
Reduced septal
systolic myocardial function was detected by all
indexes in the patients with RVPO. Reduced septal performance may be
due to increased septal afterload by stretching of the septum at the
junctions. A decreased septal preload may also be present, as
suggested by previous animal studies.35 36 A decrease
in
septal contractility may also be present, since depressed systolic
function has been demonstrated in papillary muscles38 and
in myocytes39 in experimental RV hypertrophy. Finally,
thicker portions of the LV may be associated with reduced function, as
previously demonstrated in patients with hypertrophic
cardiomyopathy23 and in hypertensive patients with normal
LV function.40
Relation of Endocardial Circumferential Shortening to LV Cavity
Shape
In contrast to the observations in healthy subjects, in whom the
endocardial circumferential shortening was circumferentially
homogeneous,40 41 the regional circumferential
shortening
in patients with RVPO was markedly nonuniform: segmental shortening
fractions in anterior and posterior regions were preserved, and the
segmental shortening fractions in lateral and septal regions were
reduced. Similar nonuniform shortening of the major diameters of the LV
was also found here, with normal Ds-fw and decreased
Da-p shortening fractions, respectively. A close relation
between the lateral segment length and anteroposterior diameter has
also been demonstrated in a canine model.7 This preserved
normal performance in the septal–free wall direction and decreased
performance in the anteroposterior direction may be due to the high RV
pressure, which affects the balance of forces in the anteroposterior
direction, increasing the load on the septum and lateral wall and
displacing the septum toward the LV free wall.
The curvature,
segment-shortening, and ventricular-diameter changes are
all interrelated in patients with RVPO: endocardial circumferential
shortening at the septum and lateral wall is related to the EI (Fig
10), which is correlated with the septal curvature (Fig
5). The
importance of this observation is that, in patients with RVPO, changes
in myocardial performance as measured by circumferential shortening can
be predicted by changes in LV shape (ie, by EI) that can be easily
measured by echocardiography.
Relation of LV Global Function to Its Geometry
As shown in
Fig 9, the relation between mean circumferential
segmental shortening fraction and area EF is linear in healthy
subjects, whereas it becomes curvilinear (quadratic) in patients with
RVPO. Whereas in the healthy subjects, a linear relation is indeed
expected, septal flattening distorts the circular shape of the LV
cavity in patients with RVPO. With mild to moderate degrees of RVPO,
the relation between area EF and shortening is similar to the healthy
control subjects. However, in severe RVPO patients, in whom the septa
are flat or inverted, an inverse relation is observed between
circumferential segmental shortening and area EF. It can be easily
understood that, by a mechanism of a systolic decrease in EI, a change
in LV volume can occur without circumferential shortening. Therefore,
in extreme RVPO cases, an increased systolic distortion of the LV by
septal flattening (a bellows-like function of the septum) maintains
global LV systolic function despite the markedly reduced average
circumferential endocardial shortening fractions.
Ventricular interaction is mediated by, among other mechanisms, the changes in the shape and position of the ventricular septum. The animal studies in isovolumic contracting hearts,42 43 in ejecting hearts,44 and in hearts with intact circulations45 46 have shown that increased RV volume or pressure results in an increase in LV pressure development, an increase in LV ejected volume, and an upward and leftward shift of the LV end-systolic pressure-volume relation45 and LV stroke work–end-diastolic volume relation.46 Thus, such direct systolic ventricular interaction favors LV global performance. However, it is believed5 47 that end-diastolic ventricular interaction mediated by septal flattening in RVPO might impair LV function, since this interaction limits the LV filling and decreases LV end-diastolic volume. After relief of chronic RVPO, LV end-diastolic geometry returns to normal with improved LV diastolic5 and systolic5 47 function. Kieffer et al1 reported inverted septa in three patients who died from primary pulmonary hypertension, which resulted in a round RV and a crescent-shaped LV. We would expect that these morphological changes might alter the contraction patterns such that the septum functions as part of the RV, the RV would contract concentrically, and the LV would contract as a bellows.48
Evaluation of 3D-Based Measurements of Thickening and
Shortening
The magnitude of the base-to-apex translation measured here
is
similar to those reported previously.49 50 Due to
base-to-apex tapering of the LV cross-sectional area,51
measurement of circumferential shortening is sensitive to longitudinal
motion if not corrected as shown above. The present value of
endocardial circumferential shortening at the equator in the healthy
group (37%) is similar to that reported by Clark et al,41
who used spatial modulation of magnetization MRI measurements validated
by sonomicrometry.52 These values are greater than those
(28%) reported by MacGowan et al,53 who used radial MRI
tags. Our values of epicardial circumferential shortening are lower
(average, 10%, ranging from a minimum of 4% [at the posterior
region] to a maximum of 17% [at the anterior region]) than
those
(about 20%) reported by Clark et al but similar to those (8%)
reported by MacGowan et al.
Wall thickening is an important parameter of regional systolic function and has been studied clinically by a variety of methods.51 54 55 56 57 58 59 60 61 62 Measured values of thickening vary from 20% to 80%. We suggest that our method using the tag-based 3D volume-element approach is the most accurate noninvasive method available so far. In the healthy-subject group, we observed LV wall fractional thickening that ranged from a minimum of 0.48±0.05 at the septum to a maximum of 0.56±0.09 at the posterior wall. It is important to note that the muscle mass of the volume elements between end diastole and end systole were not different (on the average, end-systolic muscle mass was 5% less than that at end diastole in healthy subjects [P=NS] and 3% less in RVPO [P=NS]). These results are consistent with those observed in dogs,63 64 which did not show a significant decrease in the muscle mass at end systole compared with those at end diastole.
Wall thickening was not sensitive to correction of the base-to-apex translation. These results are expected, since the apex-to-base change in wall thickness is much smaller than the apex-to-base change in the cross-sectional circumference. Therefore, even if an element at end systole does not precisely correspond to its matched element at end diastole, the calculation of thickening fraction would not be markedly affected. Yet, correction for longitudinal motion is important, because a considerable error is expected if longitudinal heterogeneity in wall thickness is significant. Such heterogeneity may occur in asymmetrical hypertrophic cardiomyopathy, myocardial infarction, and other cases.
Longitudinal Shortening
In the healthy subjects of the
present study, longitudinal
shortening is similar to that of previous
studies,40 56
and we demonstrated no differences among the different regions or
between the endocardium and epicardium.
Integrated Hypothesis
To understand the mechanisms of
ventricular performance in
systolic RVPO, one has to consider a model that looks at the three
major segments—the RV free wall, the LV free wall, and the
septum—all
interacting at the RV-to-LV insertion points.16 The high
systolic RV pressures have complex effects on ventricular shape and
cardiac mechanics. High systolic forces at the septal insertion points
possibly increase systolic afterload on the septum and the LV free wall
and may be the mechanism for reduced shortening of the septum and free
wall. The high RV pressure also pushes the septum leftward in systole,
decreasing its curvature and the EI, and generates the bellows-like
function of the LV. This "help" from the RV in systole is
responsible for the relatively normal shortening of the
septum–to–free-wall dimension, which is also expressed as normal
segment shortening in the anterior and inferior walls. Yet, the high
systolic RV pressure is added as a primary load, opposing the
shortening of the entire heart in the longitudinal directions.
Therefore, reduced longitudinal shortening is observed here,
particularly in the septum and anterior walls. The combination of
forces in both directions produces a maximum load on the septum and
leads to septal hypertrophy, which is observed here. Since wall
thickening is a combination of shortening in both circumferential and
longitudinal directions, reduction of either of the two will result in
decreased wall thickening, as is indeed observed here throughout the
circumference of the LV. Finally, despite the reduction in shortening
and thickening, LV ejection fraction is maintained, primarily because
of the bellows-like function of the septum relative to the lateral
wall.
Summary
In patients with RVPO, we studied systolic global and
regional LV
performance in relation to the distortion of the cross-sectional shape
of the LV and the severity of the disease, using MRI tagging techniques
and 3D reconstruction. A distorted LV in diastole and systole is
associated with preserved overall ventricular performance despite
reduced septal myocardial performance, as assessed by systolic wall
thickening and segment shortening analysis. An altered distribution
of circumferential myocardial shortening of the different LV walls was
observed: circumferential shortening in the septal and lateral walls
was decreased, and the magnitude of this decrease was closely related
to the degree of LV distortion. In severe cases of RVPO, global
ventricular function was maintained despite reduced myocardial
performance because of a bellows-like systolic motion of the septum and
LV free wall relative to each other. This study may have important
implications for the mechanisms of ventricular and myocardial
performance under conditions of extreme RVPO.
|
Acknowledgments |
|---|
Dr Beyar was Visiting Scientist of the Medical Research Council of Canada (Ottawa) and the Alberta Heritage Foundation for Medical Research (AHFMR, Edmonton) from the Technion (Haifa, Israel) and was supported in part by donations from Alvin and Mona Libin and Ted and Lola Rozsa. Dr Tyberg is a Medical Scientist of the AHFMR. The study was also supported by a grant from the Foothills Hospital Research and Development Committee and by grants-in-aid from the Heart and Stroke Foundation of Alberta (Calgary). We thank Dr Elias A. Zerhouni of Johns Hopkins University for his generosity in providing the MRI tagging program; Pierre La Forge of the Department of Radiology, University of Calgary, for his assistance in image acquisition; and Dr Nanette A. Alvarez, University of Calgary, for providing patients.
Received August 30, 1994; revision received November 10, 1994; accepted November 26, 1994.
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References |
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