Paper - The partitioning of the truncus and conus and the formation of the membranous portion of the interventricular septum in the human heart: Difference between revisions

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=The Partitioning Of The Truncus And Conus And The Formation Of The Membranous Portion Of The Interventricular Septum In The Human Heart=
 
Theodore C. Kramer
 
Department Of Anatomy, University Of Michigan Medical School, Ann Arbor
Nine Figures
 
A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy.
 
==I. Introduction==
This paper deals with the partitioning of the human embryonic heart at the region where the ventricles narrow into the arterial cones and the septum membranaceum completes the interventricular septum. This region has been of interest to many workers because of its importance in the development of the pattern of the circulation, and the frequency of its involvement in congenital defects of the heart, but there are still gaps in our knowledge that invite further investigation.
 
==II. Historical Summary==
The earliest study of the partitioning of the heart which can be considered of importance by present-day standards is that of His (1886). He published two papers on the development of the heart based on dissections of young embryos from which free-hand Wax models (not reconstructions) were made. These models, reproduced commercially by Zeigler of Berlin, show reasonably well the general external changes in cardiac form. The internal changes are suggested to a certain extent but the method was not sufliciently accurate for detailed analysis of the partitioning process.
 
 
 
In 1888 and 1889 Born published papers on a series of hearts from rabbit embryos and parts of two human fetal hearts. The models on which this work was based were made by the wax plate reconstruction method which is commonly known under his name. Our present knowledge of any phase of the detailed morphology of young embryos springs largely from the application of this "method of reconstruction, or modifications of it.
 
One of the early critical studies of the specific region of the human heart with which this paper is concerned was that of Hochstetter (1898). This work-, although not published in detail, was the foundation for the more extensive work of Tandler which followed later from the same laboratory.
 
Using the Born plate method of reconstruction, Tandler made careful studies’ of human embryonic hearts of younger stages than those covered by Born. His models of the hearts of 5.2—mm., 6.5—mm., 9—mm., and 14.5-mm. embryos are illustrated in his account of the development of the heart published in Bardeleben ’s Handbuch Der Anatomic des Menschens which
 
began to appear in installments in the early 1900 ’s. Much the same ground was covered in his chapter in Keibel and Mal1’s Textbook of Human Embryology published in 1912. This work gave us very. accurate information on some of the earlier phases of cardiac partitioning but it was not based on a sufliciently closely graded series of embryos to cover the course of events in the more rapidly changing structures. As
 
far as it goes this work has been confirmed by subsequent investigators and must still be used in laying the foundation of any discussion of cardiac partitioning.
 
° Working at about the same time Mall (’13) reconstructed the heart of an embryo of 11 mm. in connection with his study of the developing muscular architecture of the ventricles. This model shows conditions in the developing septa in accord with Tandler’s findings. Moreover, the age of the embryo fits nicely into the Tandler series and also with the stages described in this paper.
 
 
Frazer (’16) made a study, by the wax plate reconstruction method, of the development of the pars membranacea septi in the human heart. His illustrations, however, were free—hand schematizations, Which, while they may make for easier presentation, are difficult to compare satisfactorily with recontructions by other Workers. Certain phases of his conclusions Will be discussed later in this paper, in connection with my own findings.
 
Waterston (’18) made reconstructions of the hearts of human embryos of 3mm., 6mm., 8mm., 12.5 mm., 16 mm., 20 mm., 30 mm., and of the truncus arteriosus region of a 9-mm. embryo. The phases of his work of direct interest in connection with the present problem will be dealt with in the body of the paper.
 
0dger’s (’38) paper on “The Development of the Pars Membranacea Septi in the Human Heart” is, also, so directly in the field of this Work that discussion of it can best be postponed to be taken up in connection with our own findings.
 
It is evident from this brief survey that our knowledge of heart development depends on weaving together information which has been derived from a number of diiferent Workers, none of whom had available a really extensive series of stages. As is inevitable under such circumstances there are serious gaps and some apparent inconsistencies in the story.
 
The part_of the heart in which the partitioning process is most diflicult to interpret is that region in which_ the atriaventricular cushions, the conus (bulbar) ridges, and the crest of the interventricular septum all converge to a common meeting point in the formation of the septum membranaceum. At this point, moreover, the partition formed in the truncus arteriosus meets the cono—ventricu1ar portion of the septal complex in such a manner that the right ventricular output is routed into the pulmonary artery, and the left ventricular output into the aorta.
 
In the present paper an attempt is made to rescrutinize and bring together all the heretofore available information on this interesting region of the human embryonic heart and so to supplement it that a less-fragmentary and more understandable account may be made available.
 
==III. Materials and Method==
 
This study was based on the use of the Wax plate reconstruction method. Most of the models were made at a magnification
of 100 X or 150 X. This relatively high magnification was
used because it increased the accuracy with which details
could be Worked out. The plates Were made on the platerolling machine described by Huber in his English edition of
the Bohm, Davidoif, Histology, pages 55 to 57. Because of
the excessive amount of cutting necessitated by the delicate
trabeculation of the young ventricles it was not desirable to
embed the drawings in the Wax plates as is often done when
the plates are made by this method.
 
In constructing the models the plates Were stacked, using
a line drawn through the centers of the neural tube and the
notochord as a guide to the sagittal plane. The dorsal curvature was established by projecting a photograph of the entire
embryo to the scale to be used in the reconstruction. In the
cases in which such photographs had not been made before
the embryo was sectioned thephotograph of another embryo
of the same length Was substituted. By bending a brass rod
to fit the back curvature at the level of the body being reconstructed and fixing this rod in the model base,’ a guide was
afforded for determining, by measurements, the proper dorsoventral position for each plate as it was stacked.
 
The models have been made dissectable at several levels so
that internal structures ‘can be observed. The proximal portions of the main vessels entering and leaving the heart were
usually included.
 
The series used for the reconstructions Were selected to
dovetail into the series reconstructed by previous Workers.
After a study of the younger embryos of the University of
Michigan Collection the heart of one of this group was selected
for reconstruction (E. H. 35). To Doctors Streeter and Corner
PARTITIONING OF THE HUMAN HEART 347
 
I am indebted for the loan of three other series from the extensive collection of the Carnegie Institute of Embryology.
 
The embryos from which reconstructions of the hearts were
made for this study are listed in the following table:
 
EMB. N0. 00I4IaE(7l'I0N C. B. LENGTH REIIIARKS
 
E. H. 35 U. of M. 8.8 mm. Entire heart, aortic arches
' and ducts of Cuvier modeled. Endocardial cushions
“inlayed” in white wax.
 
6521 Carnegie 12.0 mm. Truncus and top of ventricles only modeled. Endocardial cushion tissue in
white wax “inlay.”
 
841 Carnegie 13.0 mm. _ Entire heart a11d main vessels modeled.
 
5537 Carnegie 18.0 mm. _ Entire heartand main vessels modeled.
 
Embryo 841 of the Carnegie Collection Was listed in their
records as 15 mm. in crown-rump length. Only the body of
this embryo was available in this series, the head having been
used for other purposes. From a count ofthe sections in this
series we have estimated the length of this embryo in the fixed
condition as being about 13 mm. This undoubtedly means that
the Carnegie measurement of 15 mm. was made before the full
shrinkage effect of fixation had occurred. This amount of
shrinkage during preparation for sectioning is not at all unusual (Patten and Philpott, ’21). This interpretation, moreover, fits well with the fact that the model of this heart is
smaller than would have been expected from its degree of
development in comparison with the other models of the series
reconstructed to the same scale. In spite of the disadvantages
 
due to its shrinkage, this series was selected for study because
of the particularly valuable developmental phase exhibited
 
by the heart.
 
IV. THE PARTITIONING OF THE AORTIC TRUNK AND THE
VENTRICLE AS SHOWN BY RECONSTRUCTIONS
 
The ventral Views of the embryonic hearts shown in figure 1
were assembled from various sources and redrawn in com—
348 THEODORE c. KRAMER
 
parable orientation and magnification to show the early
changes in external configuration and the establishing of the
primary regional divisions of the heart. The relatively
straight condition of the young tubular heart is short—liVed.
An elongation of the cardiac tube, which is much more rapid
than the enlargement of the pericardial part of the coelom in
which it lies, causes the heart to bend first in a rather U—shaped
 
E 8_.8mrn
 
Fig. 1 Ventral views of reconstructions of the hearts of young embryos showing
the shift in the position of the truncus toward the mid-line and the reduction of
the cono-ventricular sulcns. Slight modifications in the redrawing have been made
in order to bring the various models into comparable orientation.
 
A 2.08—mm. embryo X 42 (Modified from Davis, '27, fig. 23).
 
B 3—mm. embryo X 42 (Modified from Tandler, ’12, fig. 374).
 
C 5.2-mm. embryo X 42 (Modified from Tandler, '12, fig. 378).
 
D 6.0-mm. embryo X 21 (Modified from Waterston, ’18, fig. 2).
 
E 8.8—mm. embryo X21 (Original figure from reconstruction of EH. 35, Uni
versity of Michigan Co11.).
 
 
 
 
fashion to the right (fig. LA), and shortly thereafter i11to a
compound S—shaped curve (fig. 1, B). By this time it is
possible to recognize the major cardiac regions, although the
lines of demarcation between them are still vague. It will be
most convenient to consider these regions in a sequence corresponding to the direction of the flow of blood.
 
The atrial region can be recognized as the transversely
dilated portion of the cardiac tube into which the great veins
converge. This part of the heart remains dorsally located,
being anchored to. the body wall by a persistent portion of
the dorsal mesocardium and the entering veins. The ventricular part of the cardiac tube, having early lost its dorsal
mesocardium, is free to bend laterally and then ventrally.
There is at this stage only a poorly marked constriction between the ventricle and the atrium. Cephalically there is a
gradual transition from the ventricle to the conus arteriosus
communis, or more briefly “the conus.” As its name implies,
the conus is the somewhat conically shaped part of the heart
which joins the ventricle with the truncus arteriosus. The
terms “bulbus eordis” and “bu1bo-conus arteriosus” are not
infrequently applied to the cardiac region here designated as
the ‘ ‘conus. ’ ’ Because there is a transitory (aortic) ‘ ‘bulb’ ’ at
the distal end of the young truncus arteriosus where it turns
abruptly‘ dorsad to give off the aortic arches, it seems less
confusing to avoid the use of “bu1bus” (cordis) in connection
with a neighboring structure. The term “bulbo—conus” is at
once cumbersome and confusing in that the term is inapplicable
to mammalian embryos after the transitory aortic bulb has
disappeared. Moreover both these terms have connotations in
comparative anatomy which are not readily transferable to
primate ontoge_ny. The term conus is aptly descriptive of conditions in the embryo and furthermore by its division gives
rise to that part of the right ventricle commonly known in
adult anatomy as the conus pulmonalis, and to the more modified corresponding portion of the left ventricular outlet into
the aorta. As the terms are here employed the transition from
conus to truncus arteriosus is arbitrarily regarded as taking
350 THEODORE C. KRAMER —
 
place at the level where the aortic and pulmonary valves are
formed. At this early stage the conus grades into the truncus
without any definite line of demarcation.
 
In 5—mm. embryos (fig. 1, C) the regional divisions of the
heart have become more definitely delimited. The ventricular
loop l1as been carried into a position caudal and ventral to the
atrium. There is a well marked external notch clearly indicating the location at which the interventricular septum is
making its appearance internally. The transition from the
conus to the truncus is still gradual, although relatively more
 
abrupt .than in earlier stages. Very striking is the deep groove
 
at this stage between the conus and that part of the primary
common ventricle which is destined to become the left ventricular chamber. Later we shall have occasion to consider
more carefully the internal flange arising opposite this groove.
 
In embryos of 6 mm. (fig. 1, D) and 8 to 9 mm. (fig.'1, E) a
marked growth of the auricular appendages of the atrium is
evident. These extensions from the common atrial chamber
swing ventrally, lying close against either side of the truncus
arteriosus. The atrioventricular groove marking the line of
demarcation between atrium and ventricle is by this time
clearly defined. The interventricular sulcus has become much
deeper, while in contrast the sulcus between the left ventricle
and the conus is less extensive than in the younger stages. The
changing position of the ventricle and diiferential growth in
the region of transition from ventricle to truncus have combined to shift the conus from the extreme right (fig. 1, B)
toward the mid—line (cf. fig. 1, C—E). This shift is of great
importance in bringing the partitions in the truncus arteriosus,
 
and in the conus, into line with the interventricular septum
Accompanying these changes in the external form of the
heart, correlated changes have been occurring' internally. At
the stage shown in figure 1, A, the paired endocardial
primordia characteristic of younger embryos have united
throughout the ventricular region to form a single endocardial tube. The fusion is pretty well completed also in the
atrial region but has not yet extended sufliciently far caudad
PARTITIONING OF THE HUMAN HEART 351
 
to establish the sinus venosus. In general the endocardial
tube follows the configuration of the outer (epi-myocardial)
portion of the heart. In very early stages the material between the endocardial and myocardial layers is almost
acellular. For this reason it was called by Davis (’27)
“cardiac jelly.” As development proceeds an increasing
number of mesenchymal cells invade the “cardiac jelly” and
start to differentiate into a primitive type of embryonic connective tissue. Because of its tendency to occur in local concentrations this tissue has been called “endocardial cushion
tissue.” It tends to appear most abundantly where valves
and parts of the septal complex are arising.
 
In embryos of about 5-6 mm. fusion of the paired primordia
has extended through the entire length of the cardiac tube,
and a definite sinus venosus has been formed where the great
veins become confluent as they enter the heart. VVhen first
established, the sinus venosus is situated medially on the
dorso—caudal side of the atrium, and communicates with it by
an oval opening. By the end of the first month of development
a thickening appears dorso—cephalically in the Wall of the
atrium, in its sagittal plane. This is the beginning of the interatrial septum primum. Almost as soon as this first part of the
interatrial septal complex is definitely formed the sinus
venosus shifts to the right from its primarily median position.
At the same time its originally oval orifice becomes slit—shaped,
and its margins become thickened and project into the right
atrial lumen as the valvulae venosae (Patten, ’38).
 
About this time, also, two sub—endothelial thickenings are
becoming evident in the narrowed part of the cardiac tube
between the atrium and the ventricle. One of these is dorsally
located, and the other lies directly opposite it in the ventral
wall. These are the so—called dorsal and ventral endocardial
cushions of the atrioventricular canal. They can be designated
more briefly as the dorsal, and ventral, A.—V. cushions. Meanwhile, at the caudal border of the ventricular loop, a thickening
is becoming evident which presages the formation of the inter~
ventricular septum.
352 THEODORE C. KRAMER
 
By this time, also, there is a concentration of the endocardial
cushion tissue into two longitudinal ridges extending in a
clockwise spiral path from the cephalic end of the truncus
arteriosus, through the conus, to the ventricle. Although these
ridges are by no means equally well developed at all levels
some endocardial cushion tissue is present throughout the
length of the truncus and the conus. It was undoubtedly the
unequal development at different levels which Tandler was
emphasizing in describing “proximal and distal bulbar
ridges ’ ’ as separate structures. Probably it was the continuity
of the endocardial cushion tissue Which led Waterson to say
that he was unable to find the discontinuity described by
Tandler. Thepresent work would seem to indicate the correctness of both observers and to show that the apparent
discrepancy is merely a matter of what phase of the conditions
each writer chose to emphasize. There seem to be quite
definitely three levels in which the ridge system of the truncus
and conus of young embryos are best developed. These three
regions, as seen in the reconstruction of an 8.8—mm. embryo,
are: (1) in the ventral aortic roots at the level where the
fourth and sixth arches arerbeing separated (fig. 2, A) ; (2) in
the truncus arteriosus, at the level where the aortic and
pulmonary valves are destined to be formed (fig. 2, C); and
 
Fig. 2 Photomicrographs (X 65) of different levels of the truncus and conus
of an 8.8—mm. embryo (U. of M. Coll. E.H. 35).
 
A At the level of the septum aorto-pulmonale between aortic arches 4 and 6.
B Truncu, between septum aorto-pulmonale and level of primordia of semi
lunar valves.
C Through the level at which the semilunar valves are formed.
D Through the conus immediately below the level of the valves.
E Through the conus ridges near the transition from ventricle to conus.
 
KEY TO ABBREVIATIONS
 
Ao.V, Ventral aorta. S.-v.C.R., Sinistro—ventral conus ridge.
ARCH 6, Aortic arch 6. S.—v.T.R., Sinistro—ventral truncus ridge.
D.—d.G.R., Dextro—dorsal conus ridge. Tr.Art., Truncus arteriosus.
 
D.I.V.S., Dorsal intercalated valve V.A.-v.Cu., Ventral atrioventricular
 
swelling. g canal cushion.
P.C., Pericardial cavity. V.I.V.S., Ventral intercalated valve
 
Sept.Ao.-Pul., Septum aorto—pulmonale. swelling.
PARTITIONING OF THE HUMAN HEART 353
354 THEODORE c. KRAMER
 
(3) in the conus, definitely on the ventricular side of the
location at which the semilunar valves appear (fig. 2, E).
Although, as indicated above, there is some endocardial
cushion tissue present at all levels (fig. 2, B and D). there is
at this stage a definite discontinuity of the ridges. The absence of ridges immediately caudal to the valves is particularly
striking (fig. 2, D).
 
Dorsal
ln Tcalated
 
   
 
 
 
 
Truncus
Ridge
 
 
 
Ar 5inistroventral Truncus ._
Ridge
 
Venfral Cusp of
Pulmonary Valve
 
Fig. 3 Schematic diagram to illustrate the origin of the semilunar valve primordia.
 
It is proposed in this study to designate that part of the
partition formed by the growth of the ridges appearing between the fourth and the sixth aortic arches as the septum
aorto-pulmonale, as suggested by Tandler. In line with the
regional distinctions here used for conus and truncus arteriosus, the elevations at the second of the levels of accelerated
growth will be called the truncus ridges. After the ridges have
united to divide the truncus lume11 into an aortic and a pulmonary portion the term truncus septum will be used (fig. 3).
 
 
 
 
What are here called truncus ridges would, as nearly as I can
determine, be the part of the complex which Tandler called
the distal bulbar ridges (“Wulste”). The ridges of endocardial cushion tissue in that part of the ventricle which is
narrowing as it approaches the outlet into the truncus, will
here be called co11us ridges, or after their fusion, the conus
septum. This undoubtedly is the part of the complex to which
Tandler applied the term “proximal bulbar ridges. ”
 
It has seemed necessary thus to analyze, and to have terms
for the accurate designation of, the different regions in which
accelerated growth is occurring. This rather cumbersome
terminology should not lead to overlooking the facts that all
these regions grade insensibly one into the other, and that
ultimately these regions of locally accelerated growth are
destined to coalesce into a continuous septal system. This
septal system divides the truncus arteriosus into aorta and
pulmonary arteries, and at the same time extends into the
conus level of the ventricle. There the conus part of the
complex meets both the interventricular septum and certain
local enlargements of the A. V. canal cushions to complete
the partitioning of the ventricles in such a manner that the
left ventricle discharges into the aorta, and the right into the
pulmonary arteries.
 
At the level where the semilunar valves are formed there
are some structural details which should receive attention
before we pass on to the consideration of the conus region
where the final steps in the ventriculo—cono—truncus partitioning occur. At the level of the developing valves two smaller
elevations arise between the main truncus ridges. These elevations are relatively local in cephalocaudal extent and are
destined to take part in the formation of the pulmonary and
aortic valves, rather than to play any role in the division of
the truncus channel. They have been rather unsatisfactorily
designated by various Workers, either by numbers, or by
letters. It would seem desirable to give them a descriptive
name such as intercalated valve swellings. The term is admittedly overlong, but it does suggest the position in which the structures in question arise between the main truncus
ridges, and designating them as swellings rather than as
ridges, suggests their more local character. Their positional
relations when they first arise are shown in the schematic
diagrams of figure 3. The way in which these two masses of
endocardial cushion tissue become moulded, respectively, into
the primordium of the dorsal cusp of the aortic valve, and the primordium of the ventral cusp of the pulmonary valve is
indicated in figure 3, D—E. Figure 3 shows also the expansion
of the margins of the fusing truncus ridges to form the right
and left cusps of the aortic and ‘the pulmonary semilunar
valves. Figure 4 shows photomicrographs of sections through
the developing valves in a 13—mm. embryo. The plane of cutting is such that the aortic and pulmonary valves appear in
different sections. The pulmonary valve lies farther cephalad in the series and the plane of sectioning passes through it
diagonally, so that the limited longitudinal extent of the valve
primordia is well shown (fig. 4, A). The aortic valve lies
farther caudad and is cut more nearly transversely, so that
the relations of the three cusps to each other are Well shown
(fig. 4, B, and cf. fig. 3, C, D).
 
 
 
 
 
 
 
Fig. 4 Photomicrographs (X 50) of sections of a 13-mm. human embryo
through the truncus arteriosus at semilunar valve levels.
 
A Pulmonary valves, cut diagonally because of the sharp bend at this point
in the truneus arteriosus.
 
B The aortic valves, from a slightly more caudal level in the same series where
the plane of sectioning cuts the outlet more nearly transversely.
 
 
 
 
In later stages of development there is a further rotation
of the heart, soethat the relative positions of the aortic and
pulmonary outlets are changed from the embryonic conditions
depicted in figure 3. This, unfortunately, has resulted in two
 
   
 
B Pulmonary Artery
 
Fig. 5 Schematic diagrams to illustrate the positional relations of the cusps
of the aortic and pulmonary semilunar valves. (Modified from figure 534 in
Buchanan’s Manual of Anatomy, ’27.) ’
 
A Shows'the embryonic positional relations (cf. fig. 3, E).
B Shows an intermediate rotational change toward
C the adult condition.
 
sets of names coming into use for the leaflets of the semilunar
Valves. The BNA designates the cusps on the basis of their
position when the heart, removed from the body, is so held
that the septal system is the axis of right—left orientation. On
this basis the aortic leaflets are dorsal (posterior), right, and
left; and the pulmonary leaflets are ventral (anterior), right,
and left as in the fetal heart (cf. fig. 3, E and fig. 5, A). The
INA terminology is based on the position of the valve cusps
as seen in sections of the adult thorax with the heart in situ.
On thisbasis (fig. 5, C) the aortic cusps are right, left, and
ventral (anterior), and the pulmonary leaflets are right, left,
and dorsal (posterior).
 
 
While the semilunar valves have thus been taking shape,
the septum:aorto—pulmonale and the growing truncus ridges
have coalesced to dividepthe truncus into the aorta and the
pulmonary artery. The mannerin which this-part of the partitioning process ispaccomplished is already so well known
that it need not concern us further in this paper. With the
aortic and pulmonary outlets established in nearly their adult
relationships, and their valves clearly differentiated, we can
now confine our attention to conditions on the ventricular side
of the developing semilunar valves.
 
The most elusive phases of heart development are those
changes which bring the partitioning of the truncus above
the semilunar valves into line with the partitioning of the
ventricles below the valves. Sir Arthur Keith clearly recognized the importance of this region of the developing heart.
His study of an extensive series of anomalous human hearts
led him to compare the heart of a human embryo of 3 weeks
with the heart of a shark. He published (Keith, ’09, fig. 10)
two very interesting diagrams indicating the part of the
human embryonic heart which he believed to be homologous
with the bulbus cordis of the Elasmobranch heart. This theory
he used to explain, “a great number of abnormal conditions
hitherto inexplicable” (loc. cit. p. 363). In spite of the incompleteness of the morphological evidence on which his conclusions were based, these particular diagrams of his have
been reproduced in many textbooks of embryology and many
papers on congenital cardiac defects. They-certainly embody
a very intriguing portrayal of the supposed ontogenetic recapitulation of a remote phylogenetic phase of heart structure,
but it has been diflicult for me to satisfy myself that I could
see in my own reconstructions the landmarks that these diagrams capitalize.
 
There is one relationship suggested by Keith ’s diagrams
which, regardless of what one may feel as to its possible phylogenetic implications, seems of considerable importance in
connection with the partitioning of the conus. This is the
position of the extensive flange found internally at the concventricular sulcus. The location of this flange makes it necessary for the blood from the left ventricle to negotiate a sharp
reverse turn through the interventricular foramen into the
right ventricle, before it can leave the heart by way of the
truncus (fig. 6, A). It is quite possible that under the static
conditions depicted by a model, the sharpness of this turn
in the blood channel is exaggerated. In a beating heart it may
well be less abrupt. Certainly in observing the living chick
heart the turns around which blood currents are driven can
be seen to change markedly in different phases of contraction
 
 
 
 
Fig. 6 Semischematic drawings to show the early relations of the conus and
ventricle and early stages in the partitioning processes leading toward the establishment of the aortic and pulmonary outlets.
 
 
 
A Heart of an embryo about 4-5 mm. based in part on figure 532 in Buchanan’s
Manual of Anatomy (’27).
 
13 From a reconstruction of the heart of an 8.8—1nm. embryo (U. of M. Coll.
EH. 35).
 
(Patten and Kramer, ’33). Nevertheless, with all due allowances made for such possible differences between living and
fixed hearts, this flange certainly lies across the most direct
route for the outlet which must eventually be established from
the left ventricle into the aortic part of the truncus. It becomes, therefore, a matter of some theoretical interest whether
this flange is reduced entirely by differential growth in its
Vicinity, or whether there may be some actual resorption of
360 THEODORE C. KRAMER
 
its tissues. Keith’s diagrams would lead one to think that
resorption was the main factor. With this interpretation I
would be inclined to disagree, although admittedly this sort
of problem is exceedingly difiicult to answer with any certainty. The changing relations of the flange with reference
to a landmark such as the atrial opening into the ventricle do,
perhaps, suggest that there may be some resorption (cf. figs. 6,
A and B). But when one considers also the rapidly increasing
size of the ventricles and the atria, and their radical changes
in shape and position, it seems inescapable that differential
growth is an exceedingly important factor, probably the main
factor, in the reduction of the flange. Figure 1, B—D shows
how the ventricular loop shifts from the right side to a more
median and ventral position, and also how in this same shift
the cono-ventricular sulcus comes to lie nearer the sagittal
plane. Coincidently, the cephalic end of the cono-ventricular
sulcus opens out, and the medial shoulder of the left auricular
appendage crowds into it (fig. 1, D and E). The shoulder of
the left ventricle also appears to have moved more caudad,
thereby helping to lessen the depth of the cono-ventricular
sulcus. Along with these changes the internal flange is reshaped into a broad thickened mass of tissue, so located that
it no longer interferes with the establishing of a fairly direct
path from the left ventricle, through the conus, into the aortic
outlet in the truncus (fig. 6, B). It seems pertinent to emphasize that the changes thus accomplished do not accord with
the simple resorption or retraction process depicted in Keith's
figures.
 
The mesial shift of the conus and the reduction of the
cono-ventricular flange, together with the coincident shortening, widening, and straightening of the exit from the ventricles,
all combine in paving the way for the final steps in the
partitioning process. The septum in the truncus and the conus
ridges are now beginning to approach alignment with the
interventricular septum (cf. fig. 6, A and B). There remains
only the final closure in the region where the conus springs
from the ventricle. This is accomplished by the merging of
PARTITIONING OF THE HUMAN HEART
 
plastic endocardial cushion tissue masses derived from the
conus ridges, the crest of the interventricular septum, and
tubercles which develop from the endocardial cushions of the
atrioventricular canal. '
 
Before discussing the final steps in the closure of the conoventricular septal system it is desirable to add certain details
to what has already been said about the structures involved.
 
 
Fig. 7 Drawings of ventral views of reconstructions of hearts of human e1n«
bryos at various stages to show the changes in the conus and ventricles which
lead to their partitioning and to the formation of the membranous portion of the
interventricular septum.
 
A 8.8—mm. embryo (U. of M. Coll. EH. 35). .
 
B 11-min. embryo (Modified from Mall, ’13, fig. 11).
 
C 13—mm. embryo (Carnegie Emb. 0011., no. 841).
 
D 14.5—mm. embryo (Modified from Tandler, in Keibel and Mall, ’12, fig. 386).
 
After they first become recognizable, at about the 4—mm. stage,
the dorsal and ventral atrioventricular canal cushion masses
rapidly increase in thickness and width, until by the 8- to 9—mm.
stage they project well into the atrio—ventricular canal (figs. 6,
B, and 7, A). They are quite broad, and each cushion exhibits a raised area at each of its lateral borders. These local elevations are the so—called right and left tubercles of the dorsal
and ventral endocardial cushions. The tubercles remain conspicuous even after the main part of the cushion masses
become apposed to each other, and then fuse, dividing the
common atrioventricular channel into a right and a left channel (fig. 7, A and B). The orifices of these channels are at
this stage more or less slit—like. Eventually they become the
atrioventricular ostia, guarded on the right by the tricuspid
valves, and on the left by the mitral valves. For a short time
after the fusion of the dorsal and ventral A.-V. canal cushions
has taken place, there remains a groove marking the point at
which they originally made contact with each other. This
groove, although it ultimately disappears entirely, is for a
time a valuable landmark indicating the origin of structures
which have otherwise lost their identity by fusing. When
heart models are opened so that one can look up from below
toward the ventricular inlets and outlets, either end of the
groove is marked by the notch appearing on the mesial border
of each atrioventricula.r canal (fig. 7, B and C). When the
lateral wall of a heart model is removed to give a side view
of the septal complex, one looks along this groove, from one
ventricle to the other. It is situated in the atrioventricular
canal partition, which at this stage forms what might be called
the roof of the interventricular foramen (fig. 8, B).
 
What is called the interventricular septum in the embryo is
essentially a muscular ridge which is the primordium of the
muscular part of the septum of the adult heart, in distinction
to the interventricular septum membranaceum. For brevity,
in the following description the term interventricular septum
will be used for the primary muscular portion of the septum.
When it is wished to refer to the fibrous portion of the adult
interventricular septum, the term septum membranaceum will
be employed. It is necessary to be thus explicit, for the adult
interventricular septum is a composite structure and formed
only in part from the embryonic “interventricular septum.”
Moreover, the embryonic septum as such, is not destined to
PARTITIONING on THE HUMAN HEART 363
 
close. The original interventricular foramen above the broad
primary muscular septum is remoulded into the aortic cone,
and the final steps in the partitioning of the ventricle and
conus take place where this foramen opens out into the right
ventricle, definitely to the right of the plane of the primary
interventricular septum. It is necessary clearly to understand
these relations to appreciate the important role played by the
right tubercles of the A.-V. canal cushions in the formation
of the septum membranaceum.
 
 
Fig. 8 Semischematic drawings to show the relations of the various parts of
the septal system in lateral aspect (Collaboration with Bradley M. Patten).
 
A Based on reconstructions of the hearts of embryos 8-10 mm.
B Based on reconstructions of the hearts of embryos 12-14 mm.
 
The tubercles grow very rapidly and extend toward the
conus septum and the right side of the gap above the interventricular septum. The right tubercle of the Ventral cushion
becomes somewhat conical in shape with its tip projecting into
the narrowing outlet of the interventricular foramen (fig. 7, C,
and 8, B). Its location is to the right of the primary muscular
portion of the interventricular septum, and in approximately
the same parasagittal plane as the place where the sinistro-ventral conus ridge merges with the crest of the interventricular septum (fig. 8, B). At the same time the right tubercle of
the dorsal cushion grows considerably in size and becomes
merged with the interventricular septum dorsally, on the right
364 THEODORE c. KRAMER
 
side of its crescentic margin. This tubercle also bulges into
the interventricular foramen at its outlet into the right
ventricle.
 
While these changes have been going on in the region of
the interventricular septum, the conus ridges have been developing rapidly. At valve level the conus ridges come into
alignment with the truncus ridges in an interesting manner.
Following from the distal end of the truncus toward the
ventricle, the sinistro—ventral truncus ridge can be seen to
spiral from the left, around toward the ventral aspect of the
truncus (fig. 6, B). Caudal to the valve primordia the same
spiral course is continued by the dextro—dorsal conus ridge,
which starts from the ventral aspect of the upper part of the
conus, and then swings around onto its right side and finally
to the dorsal wall of the conus where it joins the ventricle
(fig. 7, B). In like manner the spiral started by the dextrodorsal truncus ridge is continued by the sinistro—ventral conus
ridge. Thus, of the approximately 180° turn in the trunco—
conal septal system, the half above valve level is executed by
the truncus ridges, and the half below valve level by the conus
ridges. If one thinks of this spiral as a whole (see dotted lines
in fig. 6, B) the significance of the meeting of sinistro—ventral
truncus ridge with dextro—dorsal conus ridge, and of dextrodorsal truncus ridge with sinistro—ventral conus ridge, will be
self—evident.
 
The conus ridges bulge into the lumen, grow toward each
other, and become fused progressively from the valve region
toward the ventricle, thus forming the conus septum (figs. 7
and 8). As the conus septum grows caudad it extends toward
the right border of the interventricular septum (figs. 8, B,
and 9). Toward the ventricle from the point where the conus
ridges are fused to form the conus septum, they diverge
sharply from each other (fig. 8, B). The dextro—dorsal ridge
swings toward the orifice of the right atrioventricular canal.
Its medial border reaches the right tubercle of the ventral
atrioventricular canal cushion and merges with it. Its lateral
border merges with the lateral cushion of the right A.-V. canal (fig. 7, B and C). There is thus something of the effect
of the base of the dextro-dorsal conus ridge straddling the
right A.-V. canal orifice. By the fusion of this basal portion
of the deXtro—dorsal conus ridge with the right tubercle of the
Ventral cushion of the A.-V. canal, the communication between the right atrium and common ventricle, through the cep11aloventral part of the atrioventricular canal is occluded. Thus
is formed the part of the septal complex between the right
atrium and the aortic conus of the left ventricle. It will be
recalled that this part of the septum lies cephalic to the
attachment, on the right, of the septal cusp of the tricuspid valve, and that it is known anatomically as the pars atrioventriculare of the septum membranaceum.
 
 
 
 
Fig. 9 Ventral view of a reconstruction of the heart of a. 13-mm. embryo
(Carnegie Emb. 0011. no. 841, X 42$). Ventral wall has been removed to show the
relations of the right tubercles of the dorsal and ventral atrioventricular canal
cushions with the conus ridges.
 
 
 
The sinistro—ventral conus ridge is somewhat more narrow
and shorter than the dextro-dorsal conus ridge. It becomes
continuous with the right border of the interventricular
septum as shown in figure 8, B and figure 9. The progressive
fusion of the conus ridges to form the conus septum continues
to reduce the interventricular foramen. The closure is finally
completed by a ring of endocardial cushion tissue contributed
to by the right and left conus ridges, the endocardial cushion
tissue at the crest of the interventricular septum, the right
tubercle of the dorsal, and the right tubercle of the ventral
atrioventricular canal cushi0n._ Thus is formed a thick composite mass of plastic young connective tissue occluding the
opening from the aortic conus into the right ventricle, and
accomplishing the final step in the separation of the aortic and
pulmonary channels with the establishment of the septum
membranaceum. Although the fusion of all of the component
parts is not complete in the 13-mm. stage, they are in such
close juxtaposition that there is no doubt about the direction
in which the process is progressing. The final closure of the
endocardial ring ordinarily occurs in embryos of from 15 to
17 mm. In a particularly well preserved 18—mm. embryo which
was reconstructed, closure had occurred so recently that most
of the component parts could still be identified. After this age
the linesof demarcation between the fusing structures rapidly
disappear, and the plastic endocardial cushion type of tissue
by which the closure is first effected gradually becomes differentiated into the densely woven fibro-elastic connective
tissue characteristic of the adult septum membranaceum.
 
 
==V. Discussion==
 
It is clear from the foregoing study that the formation of
the septal system of the truncus and conus is more complex
than is usually recognized. A redefinition of the terms used in describing the structures involved has proved urgently necessary, both because of the discrepant usages employed by
previous workers, and also because of the rapidly changing
shapes and locations in which the structures themselves are
found at different stages of development. It should be emphasized at the outset, however, that the mechanism of the formation of the septum membranaceum as here described in nowisc
invalidates the foundational work of such early investigators
in the field as Born (1888, 1889) and Tandler (’12, ’13); nor
is it radically at variance with the careful studies of such
workers as Robertson (’13), Frazer (’16 and ’31), VVaterston
( ’18), and Odgers (’38). It does, however, fill in certain gaps
in the story and serves to bring into line, observations which
in their early fragmentary form appeared contradictory.
There do remain certain points on which I would have to take
issue with previous workers. For example, as already stated,
I could not subscribe to the conception of the resorption of the
cono-ventricular flange, as first postulated by Keith (’O6 and
’09) and later accepted by Frazer (’16). Neither am I able to
agree with Odgers’ statement that the conus (bulbar) septum
“does not contribute anything to the occlusion of the interventricular foramen or to the formation of the pars membranacea septi” (’38, p. 258). But these are on the whole
matters of detail and one ’s conclusions as to them depend, to
a certain extent, on questions of definition. A similar situation
appears to exist with regard to the fact that Odgers does not
agree with Frazer’s (’16) account on how much of the fused
atrioventricular canal cushions go into the formation of the
pars membranacea septi. It seems to me undesirable to dwell
on these minor differences. It would appear much more pertinent to emphasize, as has been done in the body of this paper,
major points in the complicated developmental history on
which there can be agreement. It is for this reason, also, that
I have attempted to utilize, in connection with drawings of my’
own reconstructions, some figures which capitalize and bring
into line the work of previous investigators.
 
 
 
==VI. Acknowledgment==
 
The study was undertaken at the suggestion of Dr. Bradley
M. Patten. It is a pleasure to acknowledge his many helpful
suggestions in the planning of the work of his constructive
criticisms in the final preparation of the text and figures.
 
 
==VII. Summary==
 
1. This paper presents a restudy, with the aid of wax plate
reconstructions, of the formation of the septal systems of the
truncus and conus arteriosus and their union with the primary
interventricular septum.
 
2. The varying terms used by previous investigators have
been reviewed and an attempt has been made to bring them
into line with each other and, where necessary, to supplement
or alter them.
 
3. Analysis of the partitioning processes involved shows
them to be more complex than is generally realized. The following septal components must be recognized:
 
(a) Septum aorto-pulmonale at the level of the fourth and
sixth aortic arches.
 
(b) Truncus ridges above the level of the semilunar valves.
 
(c) Intercalated valve swellings at the level of the semi
lunar valves.
(d) Conus ridges.
(e) The tubercles of the atrioventricular canal cushions.
4. Although arising as more or less separate structures with
 
locally accelerated growth rates, the truncus and conus ridges’
 
become moulded into a continuous spiral septum. In this
process the sinistro-ventral truncus ridge becomes aligned
with the dextro-dorsal conus ridge, while the dextro-dorsal
truncus ridge is aligned with the sinistro-ventral conus ridge.
 
5. The trunco-conal septal system is brought into line with
the interventricular septum at what'is destined to be the interventricular septum membranaceum. This part of the process
is brought about by the apposition and fusion of the parts of
a ring of enclocardial cushion tissue contributed to by the
PARTITIONING OF THE HUMAN HEART 369
 
right and left conus ridges, the endocardial cushion tissue at
the crest of the interventricular septum, and the right
tubercles of the atrioventricular canal cushions to form the
interventricular septum membranaceum.
 
6. The interventricular septum membranaceum is closed between the 15- and 17—mm. stages. It is, at first, a thick composite mass of endocardial cushion tissue occluding the
foramcn from the aortic conus into'the right ventricle. It is
much later in development that this mass of endocardial
cushion tissue gradually becomes differentiated into a relatively thin sheet of densely woven fibroelastic connective tissue
forming the septum membranaceum in its adult form.
 
 
 
==Literature Cited==
 
Bonn, A. A., M. DAVIDOFF AND G. CARL HUBER 1919 Textbook of Histology.
2nd Ed., Section on microscopic technic, pp. 17-57. W. "B. Saunders
Co., Philadelphia.
 
BUCHANAN’S MANUAL or ANATOMY 1927 Chapt. 12, vol. 2, pp. 986-1114. 0. V.
Mosby Co., St. Louis.
 
BORN, G. 1888 fiber die Bildung der Klappen, Ostien und Scheidewiinde im
Siiugetierherzen. Anat. Anz., Bd. 3, S. 606-612.
 
~—————* 1889 Beitréigc zur Entwickelungsgeschichtc der Séiugethierherzens.
Arch. Mikr. Anat., Bd. 33, S. 284-378.
 
DAVIS, CARL L. 1927 Development of the human heart from its first appearance
to the stage found i11 embryos of twenty paired somites. Carnegie Inst.
Contrib. to Embryol., vol. 19, no. 107, pp. 245-284.
 
FRAZER, J. E. 1916 The formation of the pars membranacea septi. J. Anat. &
 
Physiol., vol. 51, pp. 19-29.
:—-~ 1931 A Manual of Embryology. Bailliere, Tindall and Cox, Lon
don, viii & 486 pp.
Hrs, W. 1886a fiber die Entwickelung der Form und der Abtheilungen des
I-Ierzens. Congre period. inter. de Sc. Med. 0. R. 1884. Copenhagen
 
1886 I. Section d’Anat., pp. 32-34.
— 1886b Beitrlige zur Anatomie des Menschlichen I-Ierzens. F. C. W.
 
Vogel, Leipzig., 20 pp., 3 pl.
 
I-Iocnsawrrsx, F. 1898 ‘Uber die pars membranacea septi. Wiener Klin. Wsehi-.,
Bd. 11, S. 247-248. Vortrag gehalten in d. Wiss. Aerztegesellschaft
zu Innsbruck.
 
KEIBEL, F., AND F. P. MALL 1912 Manual of Human Embryology. J. B. Lippi}!cott Co., Philadelphia, vol. I, xviii & 548 pp.; vol. II, viii & 1032 pp.
370 THEODORE c. KRAMER
 
KEITH, A. 1906 Malformations of the Bulbus Cordis. Studies in Pathology,
Edited by William Bullock. Aberdeen University Studies, no. 21,
pp. 57-74.
1909 The Hunterian Lectures on Malformations of the Heart.
Lancet, 2nd vol. for 1909, pp. 359-363, 433-435, 519-523.
 
MALL, F. P. 1918 On the development of the human heart. Am. J. Anat.,
vol. 13, pp. 249-298.
 
ODGERS, P. N. B. 1938 The development of the pars membranacea septi in the
human heart. J. Anat. & Physiol., vol. 72, pp. 247-259.
 
PA'1"l‘EN‘, B. M. 1938 Developmental defects at the fornmen ovale. Am. J. Path.,
vol. 14, pp. 135-161.
 
PATTEN, B. M., AND T. C. KRAMER 1933 The initiation of contraction in the
embryonic chick heart. Am. J. Anat., vol. 53, pp. 349-375.
 
PATTEN, B. M., AND R. PHlLPO’I"1‘ 1921 The shrinkage of embryos in the processes prcparatory to sectioning. Anat. Rec., vol. 20, pp. 393-413.
 
ROBERTSON, J. I. 1913 Comparative anatomy of the bulbus cordis, with special
reference to abnormal positions of the great vessels in the human heart.
J. Path., vol. 18, pp. 191-210.
 
TANDLER, J. 1912 The Development of the Heart. Sect. II, chapt. 18, vol. 2,
in Keibel and Mall, Manual of Human Embryology, pp. 534-570.
1913 Anatomie des Herzens. In Bardeleben’s Handb. der Anatomie
des Menschen, Bd. 3, S. 1-292. Gustav. Fischer, Jena.
 
WATERSTON, D. 1918 The development of the heart in man. Trans. Roy. Soc.
Edin., vol. 52, Part 2, pp. 257-301.

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