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Growth of the myocardial volumes of the individual cardiac segments in the rat embryo.

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THE ANATOMICAL RECORD 243:93-100 (1995)
Growth of the Myocardial Volumes of the Individual Cardiac
Segments in the Rat Embryo
M.W.M. KNAAPEN, B.C.M. VROLIJK, AND A.C.G. WENINK
Department of Anatomy and Embryology, University of Leiden, The Netherlands
ABSTRACT
Background: Although the growth of the developing heart
in relation to an increase of ventricular systolic pressure and the growth of
the entire embryo during development has been described, no data are
available on the growth of the individual segments and intersegmental
junctions. Because these different portions are known to function differently, the need for data on their individual development is obvious.
Methods: We have measured the volumes of these different compartments
by Cavalieri’s point counting method in rat embryos from 11 to 17 days.
Results: It is shown that sinus venosus and sinu-atrialjunction as well as
the main compartments atrium, inlet, and proximal outlet segment grow
roughly proportional to the total myocardial volume. Atrio-ventricular canal and distal outlet segment show a restricted growth and their proportional volumes decrease in time. The inlet segment is the most important
part of the ventricular mass at 11 days of gestation, when it is still larger
than the proximal outlet segment and, thus, takes the greater part in systolic action of the ventricular mass. The growth of the primary fold increases from day 13 onwards and can be considered as part of the wall of
the inlet segment which gives rise to the main part of the ventricular septum.
Conclusions: The timing of the septa1 volume increase fits with qualitative descriptions of ventricular septation. The atrio-ventricular canal and
distal outlet segment have an important constrictive function in early
stages, when valves are not yet present. Slow conduction and contraction
patterns have been reported to be a characteristic feature of these portions
of the embryonic heart. With development of valves these segments are
loosing their mechanical function and, thus, their proportional volume
declines. 0 1995 Wiley-Liss, Inc.
Key words: Heart, Development, Myocardium, Stereology
During development the embryonic blood pressure
and blood volume increase linearly with body weight
and so does the myocardial volume (Van Mierop and
Bertuch, 1967; Clark et al., 1986).However, it has been
reported that the growth rate of the entire embryo
shows sudden changes in certain stages, which could be
due to changes in cell activity and cell differentiation of
several organs and/or tissues (Goedbloed, 1972). More
specifically, cardiac growth rate changes have been described in relation to the embryonic crown-rump length
(Mandarim-de-Lacerda, 1991). These might reflect certain changes in cardiac differentiation. Indeed, some
cardiac components have specific functions during embryonic life, such as the sphincter-like function of the
junctions which contain endocardia1 cushion tissue
(Goerttler, 1955; Jaffee, 1965). Moreover, different action potential and contraction patterns have been related to different expression patterns of myosin isoforms in the various segments of the developing heart
(de Jong et al., 1987; Evans et al., 1988; Agata et al.,
1993). Thus, myocardial growth seems to be governed
0 1995 WILEY-LISS, INC.
by the expression of several genes which regulate typical cell activities and cell differentiations of different
segments in the developing heart. Yet, the individual
growth of these segments and intersegmental junctions
has never been described. We have approached this
subject by measuring the myocardial volume of the entire heart as well as the myocardial volumes of the
individual segments in rat embryos ranging from 11to
17 days of development.
MATERIAL AND METHODS
We used 35 Wistar rat embryos ranging from day 11
to day 17 post coitum. After ether anaesthesia and cervical dislocation of the pregnant females, the embryos
were excised from the uterus. Then, the embryos were
Received August 18,1994;accepted February 15,1995.
Address reprint requests to Dr. A.C.G. Wenink, Department of
Anatomy, PO Box 9602,2300RC Leiden, the Netherlands.
94
M.W.M. KNAAPEN ET AL.
fixed by perfusion in the right atrium with half
strength Karnovsky buffered in Cacodylate, pH 7.2.
After perfusion the embryos were fixed by immersion
in the same fixative for 24 hr. Complete embryos of 11
days were washed in Cacodylate buffer and embedded
in Epon 812. From older embryos, only the hearts were
embedded. After the embedding procedure, they were
serially sectioned at 2 Fm and stained with toluidineblue.
Morphologic Determination of Cardiac Segments
The boundaries of the individual segments and intersegmental junctions of the heart were morphologically defined in the sectioned embryos. In Figures 1
and 2, light microscopic photographs of hearts from 11
days and 14 days of development are shown. A reconstruction of a 12 day old embryonic heart shows the
successive arrangement of the individual segments and
intersegmental junctions (Fig. 3). At day 11 post coitum, the sinus venosus is that part of the heart which
receives all the veins of the embryo. The sinu-atrial
junction is the myocardium that lies between the sinus
venosus and atrium. In the young embryos, where the
sinus venosus has two sinus horns, the sinu-atrial junction is a constricted area, a t the site where the lumina
of the sinus horns discharge into the lumen of the
atrium. When the sinus venosus incorporates into the
atrium, the sinu-atrial junction becomes a double layer
of cells and looks like two valves between sinus venosus and atrium. The atrium is the segment which receives the blood from the sinus venosus in the younger
embryos. In the older embryos, where the atrium is
septated, the blood from the venae cavae enters that
part of the right atrium which is derived from the incorporated sinus venosus. The right atrium is connected with the left atrium, receiving the lung veins,
by the oval foramen. The atrio-ventricular junction is
the canal lying between atrium and ventricular inlet
segment. In the younger embryos, 11and 12 days post
coitum, the atrio-ventricular canal is a tubular structure containing cushion tissue. In the older embryos,
the myocardium of the atrio-ventricular canal is still
recognized by the location of these cushions, although
the canal is relatively shorter. Furthermore, in these
stages of development the cells of the atrio-ventricular
canal show several cytoplasmic extensions, whereas
the cells of the atrium and inlet segment are more
rounded. The ventricular part of the heart consists of
two separate segments. The inlet segment is the compartment which receives the blood from the atrium via
the atrio-ventricular canal in the very young embryos.
In older embryos only the blood of the left atrium is
received by the inlet segment via the left part of the
atrio-ventricular junction. The inlet segment has apical trabeculations. The primary fold is the junction lying between the inlet segment and outlet segment. It
lies in a more or less sagittal plane and it delimits the
primary foramen, i.e., the communication between the
ventricular inlet and outlet segments. In the inner curvature of the heart tube, the primary fold is continuous
with the right side of the atrio-ventricular wall. In the
outer curvature of the heart tube, the primary fold corresponds with a groove between the two ventricular
segments, when seen from the outside of the heart. The
primary fold develops into the larger part of the ven-
Fig. 1. In the embryonic heart of a 11-day rat embryo, the atrium
(Atr) is connected to the inlet segment (Inl) by the atrio-ventricular
canal (AV). The primary fold (PF) forms the junction between inlet
segment and proximal outlet segment (PO). The distal outlet segment
(DO) contains endocardial cushion tisuue. x 125.
tricular septum in the cardiac apex. The outlet segment can be divided in two parts, the proximal outlet
segment, which is trabeculated as the immediately
neighbouring inlet segment, and the distal outlet segment which is smooth and contains the endocardial
outlet ridges. This segment is connected with the mesenchymal arterial trunk, which gives rise to the great
arteries.
Stereology
The total myocardial volumes of the hearts were estimated by the Cavalieri method (Gundersen and
Jensen, 1987). We counted the number of points on a
grid hitting the myocardium in ten sections, taken systematically at equal distances. The magnification was
x 40 and the point area of the point grid used was 225
mm'. The myocardial volumes of the individual segments were also estimated using this method. For the
large segments such as atrium, ventricular inlet, and
outlet segment, we used a point area of 225 mm2 and a
magnification of x 40.For the smaller segments, sinus
venosus, sinu-atrial junction, atrio-ventricular canal,
and distal outlet segment the magnification was x 100
and the point area was 25 mm'. In the smallest embryos, only this latter grid and magnification were
used. Calculation of the total myocardial volume and
the myocardial volumes of the individual segments was
done by Cavalieri's formula:
Volume = M - 2x a x d x ZP
Here M is the magnification, a is the point area in
mm', d is the distance between the counted sections in
MYOCARDIAL GROWTH
95
Fig. 2. In the embryonic heart of a 14-day rat embryo, the atrium
(Atr) is connected to both inlet segment (Inl) and proximal outlet
segment (PO). The sinus venosus (SV) incorporates into the right
atrium where the sinu-atrial (SA) junction functions as the venous
valves. The distal outlet segment (DO) contains still endocardia1cushion tissue. ~ 4 0 .
mm, and X P is the total of counted points on the ten
sections. The absolute volumes of the myocardium of
the entire heart and of the individual cardiac segments
were examined by the statistical package SPSS (version 5.0).In the statistical analysis, the developmental
stages were fixed in days of gestation according to
Berkson (Snedecor and Cochran, 1980). Multivariate
analysis of variance with a significance level of 0.05
was used to compare the growth curves of the individual segments.
RESULTS
The Total Myocardial Growth
During the developmental stages from 11 days to 17
days post coitum, the total myocardial volume showed
an exponential growth curve (Fig. 4). The myocardial
volume increased from 0.0416 mm3 a t day 11 to 2.7785
mm3 a t day 17. In Figure 5 the total myocardial volume for each developmental day studied is given on a
logarithmic scale. It seems to show a change of slope a t
day 14. This suggests that there are two different
growth rates. The growth rate from day 11 to day 14
differs with slight significance (Manova, P = 0.034)
from the growth rate between 14 and 17 days of development.
The Myocardial Growth of the Individual Segments
The growth curves of the myocardial volumes of the
individual segments are shown on a linear and logarithmic scale respectively (Figs. 6, 7). In Table 1, the
mean myocardial volumes of the individual segments
Fig. 3. 3-D Graphic reconstructions (ventral view) to show the sequential arrangement of the cardiac segments and intersegmental
junctions of a 12-day rat embryo in relation to each other. The compartments are shown from the venous to the arterial pole, and in each
figure the more downstream region has been added. a: sinus venosus
(SV). b sinus venosus and sinu-atrial junction (SA). c: the same with
addition of the atrium (Atr). d the atrio-ventricular canal (AV) has
been added. e: the inlet segment (Inl) has been connected with the
atrio-ventricular canal. f: the same with addition of the primary fold
(PF).Note that, in the inner curvature, the primary fold is continuous
with the atrio-ventricular canal (see e). g: the same with addition of
the proximal outlet segment (PO). h the complete heart after addition
of the distal outlet segment (DO).
for each developmental day studied are given. The increase in myocardial volume of the sinu-atrial junction
did not differ significantly from that of the sinus veno-
96
M.W.M. KNAAPEN ET AL.
Volume (mm3)
Volume (mm3)
10 r
ll
.i...i
0.5
0
10
0.1
11
12
13
14
Age in days
15
1
I
16
17
0.01
10
11
12
4
13
14
15
16
17
5
Age in days
Volume (mm3)
Volume (mm3)
1
0.1
0.01
0.4
0.001
0.2
0
1
-
4.0001
10
11
12
13
’
14
1
15
16
Age in days
‘SV
Fig. 4.The growth of the total myocardial volume and its standard
deviation of the embryonic rat heart in mm3 from day 11 to day 17
post coitum.
Fig. 5. As Figure 4, with the volumes given on a logarithmic scale.
*SA
OATR B A V *INL
+PF
17
7
*PO +DO
tersegmental junctions in mm3 from 11 day to 17 day embryonic rathearts. SV, sinus venosus; SA, sinu-atrial junction; Atr, atrium; AV,
atrio-ventricular canal; Inl, inlet segment; PF, primary fold; PO, proximal outlet segment; DO, distal outlet segment.
Fig. 7. As Figure 6, with the volumes given on a logarithmic scale.
Fig. 6. The myocardial volumes of the individual segments and in-
sus and neither from the atrium although the inter- when the myocardial volume of the primary fold was
cepts were of course different. The growth curves of the added to the proximal outlet segment the growth
three main compartments; atrium, inlet segment, and curves of the inlet segment and the enlarged proximal
proximal outlet segment are not identical. The curves outlet segment differed significantly also (P = 0.005).
of the proximal outlet segment and the inlet segment The growth curves of atrio-ventricular and distal outlet
are significantly different (P = 0.022). The primary segment were remarkable (Fig. 7). They differed with
fold, including the ventricular septum, differs signifi- small significance (P = 0.042) from each other, but
cantly from the atrium (P < 0.001), inlet segment (P = they differed with high significance (P < 0.001) from
0.002), and proximal outlet segment (P = 0.015) (Fig. the other segments and intersegmental junctions.
The relative growth of the individual segments is
8). However, there are reasons to consider the primary
fold, giving rise to the ventricular septum, as part of evaluated in Figure 10, where each individual volume
the inlet segment. Thus, when the myocardial volume is expressed as the percentage of the total myocardial
of the primary fold was added to the myocardial volume volume. The relative myocardial volumes of sinus
of the inlet segment, the resulting curve did not differ venosus and sinu-atrial junction remained the same
significantly from the growth curve of the atrium and during the period studied. The residual values of the
that of the proximal outlet segment (Fig. 9). However, atrium to the total myocardial volume did not differ
97
MYOCARDIAL GROWTH
TABLE 1. The myocardial volumes of the individual segments and intersegmental junctions in mm3 at each day
of gestation in the period studied'
Age
11
12
13
14
15
16
17
S.V.
S.A.
Atr.
A.V.
0.0005
0.0015
0.0036
0.0073
0.0162
0.0173
0.0317
0.0004
0.0015
0.0025
0.0080
0.0141
0.0195
0.0317
0.0077
0.0195
0.0585
0.1525
0.2774
0.4949
0.6104
0.0059
0.0106
0.0119
0.0241
0.0308
0.0373
0.0436
Inl.
0.0120
0.0246
0.0504
0.1483
0.3012
0.4835
0.7095
P.F.
0.0014
0.0039
0.0127
0.0518
0.1055
0.1881
0.4122
P.O.
0.0091
0.0157
0.0522
0.1319
0.3002
0.5095
0.8601
D.O.
0.0047
0.0101
0.0229
0.0444
0.0681
0.0882
0.0793
'SV, Sinus Venosus; SA, Sinu-Atrial junction; Atr, Atrium; AV, Atrio-Ventricular canal; Inl, Inlet segment; PF, Primary Fold; PO, Proximal
Outlet segment; DO, Distal Outlet segment.
significantly indicating that the relative growth curve
of the atrium shows the same evolution as the total
myocardial volume although there was a small increase of the relative atrial volume between day 11and
day 14, and a small decrease from day 16 to day 17. The
inlet segment showed an equal contribution to the
myocardial volume of nearly 27% in all the developmental stages. However, it is remarkable that a t day
11,the inlet segment showed the highest proportion of
the total myocardial volume, which is 0.01196 mm3 in
absolute myocardial volume. The proximal outlet segment increased slightly from day 11to day 17 of development, and its growth curve differed not significantly
from that of the total myocardial volume. An interesting phenomenon is shown by the junctions atrio-ventricular canal, primary fold and distal outlet segment.
The atrio-ventricular canal showed a rapid decrease
from 14% at day 12 to 4% a t day 14, whereafter the
relative growth of the atrio-ventricular canal declined
slowly. Between day 12 and 14 the relative myocardial
volume of the primary fold increased from 4% at day 12
to 10% a t day 14. The distal outlet segment showed a
gradual decline during the developmental stages studied.
DISCUSSION
Our data show a steady increase of both the total
myocardial volume and the myocardial volumes of the
individual segments and junctions. The total myocardial volume increases from 0.0416 mm3 at day 11 to
2.7785 mm3 at day 17. The growth rate of the total
myocardial volume is higher between day 11 and day
14 than from day 14 to day 17. This supports the data
of Goedbloed (1972) who found that in the developing
rat embryo there are changes in growth rates. He suggested that these changes correlate with the changes in
cell activity and cell differentiation. Around day 14,
Goedbloed (1972)found a sudden change in growth rate
of the volume of the entire rat embryo. Mandarim-deLacerda (1991) found also a change in growth rate, in
human embryos, when the volumes of the hearts were
plotted against the crown-rump length. He suggested
that this phenomenon could be due to a more intensive
ventricular growth to supply the entire embryo with
blood. The systolic pressure shows a linear relationship
to the embryonic weight (Van Mierop and Bertuch,
1967) and the volume of the entire embryo correlates
linearly with the total myocardial volume of the developing heart (Clark et al., 1986). Goedbloed (1972) re-
ported a growth change of the entire embryo at day 14
post coitum. If this change in growth rate is correlating
to cardiovascular changes which reflect increasing
blood volume and blood pressure, then typical differentiation processes in specific areas of the developing
heart have to be hypothesized. It is remarkable that
around day 14 the septation has been reported to have
proceeded to such an extent that a separate right blood
stream into the outlet is evolving (Wenink et al., 1994).
Thus, systolic pressure increases a t that time, especially in the ventricles (Van Mierop and Bertuch,
1967). Besides, the amount of myofibrils increases and
they become more orientated, whereas the volume of
the cytoplasm relatively decreases in the myocytes of
the ventricular wall (Manasek, 1970). Therefore, the
developmental regulation of myosin heavy chain isoforms could change the contractile characteristics of
the developing atria and ventricles in response to
changes in blood volume and blood pressure during development, as supposed by Evans (1988).
Sinus Venosus and Sinu-Atrial Junction
The myocardial volumes of the sinus venosus and
sinu-atrial junction as percentages of the total myocardial volume remain the same, whereas the absolute
myocardial volumes of these segments show a slight
increase during the period studied. Also the sinu-atrial
junction shows the same growth curve as the atrium,
indicating that this junction is partly sinus venosus
and partly atrium. In the young embryos, the sinuatrial junction does not seem to function to avoid backward flow from the atrium to the sinus venosus. In the
older embryos the sinu-atrial junction is partly transformed to the venous valves due to incorporation of the
sinus venosus into the right atrium (Odgers, 1935;
Wenink, 1987; Steding, 1990). In this stage of development, the venous valves might have acquired the function of avoiding backward flow, because the blood pressure in the atrium increases, although it is much lower
than in the ventricular part (Faber, 1968). The right
venous valve gives rise to the Eustachian and Thebesian valves, whereas the left venous valve fuses partly
with the atrial septum. However, these cardiac components do not seem to be of great functional importance
and morphological variations of the valvular apparatus
in the right atrium such as the absence of the Thebesian valve are frequent (Steding, 1990; Felle and Bannigan, 1994). Our own measurements are of course inadequate to reflect such variations.
98
M.W.M. KNAAPEN ET AL.
Atrium, Inlet, and Proximal Outlet Segment
Volume (mm3)
'r
I
1
0.01
O.lI
i
I
0.001 L
10
11
12
13
14
15
Age in days
O-
ATR
* INL + PF * P O
Volume (mm3)
lor
I
0.001
10
1
11
I
13
12
14
15
Age in days
0 ATR f PO
+ IP
Proportional volume (%)
35
r
15t
Undoubtedly, these segments must show functional
changes during development. In the straight heart
tube stage, when atrium, inlet, and proximal outlet
segment are sequentially arranged to each other
(Wenink, 19871, the myocardium of the heart tube
shows peristaltoid contractions (Goss, 1938). By day 11
of development, that is the youngest stage studied presently, the heart has already looped but it maintains the
sequential arrangement of those segments. As we have
shown, the inlet segment has then the highest proportion of the total myocardial volume. In this stage the
proximal outlet segment hardly collects any blood from
the atrium via the atrio-ventricular canal and the inlet
segment directs all blood to the distal outlet segment
via the primary foramen. Therefore, in this stage of
development the inlet segment is probably the main
contraction compartment to supply the embryo with
blood. From 13 days onwards the cushions of the atrio16
17
ventricular canal direct also a part of the bloodflow
into the proximal outlet segment through a developing
groove from the atrio-ventricular canal into the proxi8
mal outlet segment (Wenink et al., 1994). From that
time the proximal outlet segment, too, starts to function like a contraction compartment which directs the
bloodflow to the distal outlet segment. This might explain our observation (Fig. 10) that the proximal outlet
segment is steadily increasing its proportional volume.
In later stages of development the embryo gradually
requires a greater blood volume to supply all the tissues of the embryo as well as an increase in blood pressure (Van Mierop and Bertuch, 1967). The suggestion
that the atrium functions as the collecting compartment whereas inlet and proximal outlet segment act as
the contraction compartments is supported by the fact
that inlet and proximal outlet segment show higher
and longer action potentials than the atrium does (Paff
and Boucek, 1962; Agata et al., 1993). The rate of the
action potentials increases gradually as more myocarI
dium becomes contractile (GOSS,1938).
16
17
Apparently, the functional changes of the heart tube
are as follows. The straight heart tube shows peristal9
toid contractions. The venous part has then the greatest contractility (Hall, 1954). After looping, a more synchronous contraction pattern develops which is
reflected by changes in myosin heavy chain expression
patterns (de Jong et al., 1987). As we have shown, the
ventricular inlet segment has the greatest relative
myocardial volume in these stages. Gradually, the
Fig. 8. The myocardial volumes of the atrium and both ventricles,
(i.e., inlet and proximal outlet) and the primary fold on a logarithmic
scale in relation to the developmental stages from 11-day to 17-day
rat embryos.
EL-
10
5
0
10
11
12
13
14
15
16
Age in days
-SV
*SA
O A T R B A V *INL
Figs. 8-10.
+PF
17
10
*PO
*DO
Fig. 9. The myocardial volumes of atrium, inlet segment including
the myocardial volume of the primary fold (IP), and proximal outlet
segment during the period studied on a logarithmic scale in relation
to the developmental stages from 11-day to 17-day rat embryos.
Fig. 10. The ratio of the individual cardiac segments and intersegmental junctions to the total myocardial volume in the period from
11-day to 17-day post coitum. SV, sinus venosus; SA, sinu-atrialjunctions; Atr, atrium; AV, atrio-ventricular canal; Inl, inlet segment; PF,
primary fold; PO, proximal outlet segment; DO, distal outlet segment.
MYOCARDIAL GROWTH
99
which squeeze the endocardial cushions together, so as
to avoid backward flow (Goerttler, 1955; Jaffee, 1965).
Indeed, the myocardial walls of the atrio-ventricular
canal and distal outlet segment have been reported to
show a slow conduction velocity and slow contraction
Primary Fold
(de Jong et al., 1992).
The primary fold is a special junction because it gives
By day 13, septation has proceeded to create two
rise to the main part of the ventricular septum. There- blood streams (Rogers and Morse, 1986; Wenink, 1987).
fore, in relevant stages, we have included the ventric- From that time onwards the formation of valves at the
ular septum in our counts of the primary fold. The atrio-ventricular and ventriculo-arterial junctions bebasal portion of the fold, in the inner curvature of the comes more important in avoiding backward flow of
heart, is not supposed to grow significantly, but our the blood when the pressures in both ventricles start to
data fail to show this because all of the fold was increase (Van Mierop and Bertuch, 1967; Clark et al.,
counted as one single structure. The growth curve of 1986).In the human embryo, the atrioventricular cushthe primary fold shows a remarkable increase of the ion tissue has been reported to grow only for a limited
volume from day 11to day 17.
period (Mandarim-de-Lacerda, 1991; Wenink, 1992),
Before day 14 of development the volume shows the whereas the distal outlet segment may become thicker,
greatest increase. This period corresponds with the but without changing its length (Thurkow and
time when the atrio-ventricular canal starts to direct Wenink, 1993). All these data point a t a diminishing
the blood into both the inlet and proximal outlet seg- role of the atrio-ventricular canal and the distal outlet
ments (Lamers et al., 1992; Wenink et al., 1994). As is segment as temporary sphincters. Our present findshown in Figures 8 and 10, the primary fold differs in ings, in particular the steep decrease of the relative
growth rate from the growth rate of the inlet segment myocardial volumes between day 12 and day 14 (Fig. 6)
as well as the proximal outlet segment and the growth support the notion of a changing function in this develrate of the total myocardial volume. It is important to opmental period.
note that the growth rates of inlet segment and proxiCONCLUSIONS
mal outlet segment are also different from the total
myocardial volume and from each other. We have deSeveral important conclusions can be extracted from
liberately considered inlet segment, primary fold and the growth curves. 1)The sinus venosus and sinu-atrial
proximal outlet segment as three separate entities. junction grow proportional to the total myocardial volThus, the volume increase of the primary fold at 14 ume. They remain relatively small components, but
days is supposed to reflect ventricular septation. Goor there is no change in proportion during development.
(1970) has suggested that ventricular septation takes 2) A similar exponential growth is seen in atrium, inlet
place by expansion of the two neighbouring ventricular segment, and proximal outlet segment. These are the
cavities. This would mean an equal contribution from components that do most of the work of the heart. In
both the inlet segment and the proximal outlet seg- the youngest stages, the inlet segment is the most imment. However, the different growth curves of the en- portant segment to propel the blood into the distal outtities allow still another hypothesis. If the volumes of let segment. 3) The atrio-ventricular canal and distal
primary fold and inlet segment are added and consid- outlet segment show conspicuously less growth than all
ered as one entity, then this new entity no longer has a other components. However, their percentage of the todifferent growth curve from either that of the proximal tal volume is relatively high at day l l , indicating their
outlet segment or that of the total myocardial volume importance in squeezing the endocardial cushions to(Fig. 9). This suggestion that the ventricular septum gether to avoid backward flow in a heart yet without
would belong more to the left ventricle than to the valves. 4) The primary fold, although being a juncright is also supported by the myofiber architecture in tional structure, does not have the same constricting
the mature heart (Anderson and Becker, 1980).
function as the atrio-ventricular canal and distal outlet
segment a t day 11. It can be considered as part of the
Atrio- Ventricular Canal and Distal Outlet Segment
wall of the inlet segment and gives rise to the main
The slow growth of the atrio-ventricular canal and part of the ventricular septum.
distal outlet segment, i.e., the decrease of a high relaACKNOWLEDGMENTS
tive volume at day 11to a lower proportion at day 17,
indicates that their function may be important only
This study was supported by grant 90288 from the
during a limited period of cardiac development. These Netherlands Heart Foundation. The authors gratefully
are the regions in the developing heart which contain acknowledge the help of Dr E.A. van der Velde, Deendocardial cushion tissue. Before valve formation partment of Medical Statistics, who reviewed the stathey must have a particular contraction pattern. The tistical part of this study.
ventricular segments contract faster than the atrium
does, and in addition the repolarization phenomenon of
LITERATURE CITED
the atrium occurs simultaneously with depolarization Agata, N., H. Tanaka, and K. Shigenobu 1993 Developmental
of the ventricle (Paff and Boucek, 1962). Also the
changes in action potential properties of the guinea-pig myocardium. Acta Physiol. Scand., 149:331-337.
atrium has a lower blood pressure than the ventricular
part (Faber, 1968). Thus, in a heart which does not yet Anderson, R.H., and A.E. Becker 1980 Cardiac Anatomy. Churchill
Livingstone, Edinburgh London New York, 5.14-5.26.
possess atrio-ventricular valves and ventriculo-arterial Clark,
E.B., N. Hu, J.L. Dummett, G.K. Vandekieft, C. Olson, and R.
valves the myocardial walls of atrio-ventricular canal
Tomanek 1986 Ventricular function and morphology in chick embryo from stages 18 to 29. Am. J. Physiol., 250:H407-H413.
and distal outlet segment function like sphincters
atrial and ventricular segments develop their own specific myosin isoform expression pattern (de Jong et al.,
1987), and we believe that this functional evolution is
also illustrated by the present data.
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