AUTHOR’S ABSTRACT O F T H I S PAPER ISSUED
B Y T H E BIBLIOGRAPHIC SERVICE, J A N U A R Y 14
ON THE VARIATIONS O F WALL THICKNESS I N
EMBRYONIC ARTERIES
J O H N LEWIS BREMER
Harvard Medical School, Boston, Massachusetts
SIX FIGURES
The relative thickness of arterial walls in embryos has
not, to my knowledge, been the subject of special study, yet
on looking at any number of embryos of different ages and
of different species with this in view one cannot but be
impressed by the great variety of appearances. One expects
the larger, main vessels to be more heavily coated than their
smaller branches, the arteries near the heart, on which the
full force of the pulse beat comes, to have thicker walls than
those more distally placed. It is known that in young
embryos the arteriez I r e relatively enormous and the walls
a simple endothelium. Large caliber and thin walls seem to
go together, and to indicate that with the slow stream and
low pressure suggested by the large caliber mesenchymal
differentiation to strengthen the walls is not necessary.
Mesenchymal differentiation appears at widely different
periods in different types of embryos and in different
arteries, and is usually accompanied by a relative or actual
narrowing of the vessels, as the circulation becomes more
definite. But in addition to this there may be, even in certain
arteries of individual embryos, great variation in the thickness of the wall in different regions.
The thinner o r thicker areas in the wall of an artery may
be very local and readily understandable, if the probable
cause for the presence of a coat is kept in mind. The walls
develop in response to pressure within the vessel, and, as a
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THE ANATOMICAL BIGCORD, VOL. 27, NO.
J A h U S R Y , 1924
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J O H N LEWIS BREMER
corollary to this, the greater the pressure the stronger the
walls. In the embryo, before the mesenchyma is much differentiated, the term stronger can probably be interchanged
with thicker, though it is by no means certain that this woulc!
hold true later. One instance of inequality in the arterial
wall is shown in figure 1. This is of a carotid branch cut
lengthwise at a rather sharp bend, in the region of a probably swift current, and the wall on the outer curvature, where
Fig. 1 Branches of the carotid artery. The blood flows in the direction of
the arrow into the three branches, all of which, but especially that to the left,
show a thickening of the wall on the outer curvature, as the stream is deflected.
A group of corpuscles lies in the lumen near the thin wall. Chick, 14 d. 5 h.,
€1. E. C. No. 1968, sect. 741, transverse.
Fig. 2 Ductus arteriosus entering the dorsal aorta. The walls are thin,
where they are supported by the vagus and recurrent laryngeal nerves, thicker
where not so supported. Man, 18.8 mm., H. E. C. no. 2246, sect. 582, transverse.
Fig. 4 Ductus arteriosus of turtle entering the dorsal aorta. The walls a r e
thin far beyond the area of contact with the vagus and recurrent laryngeal
nerves, which are shown in black on either side. The dorsal aorta shows thick
walls. Chrysemys marginata, 32 mm., H. E. C. no. 1127, sect. 947, transverse.
Fig. 6 Arteries of chick. The large thin-walled aorta is shown giving off
its branch, the vitelline artery, smaller but with thicker walls. Another branch
from a higher level, the coeliac artery, is shown below, of much smaller caliber
but with thicker walls. Chick, 14 d. 5 h., H. E. C. no. 1968, sect. 2184,
transverse.
WALL T H I C ~ N E S S IN THE EMBRYONIC ARTERIES
3
the pressure of the blood would be the greatest, is much
thicker than that on the inner curvature. Similar conditions
can be met with frequently, where arteries curve; but in
noting them one must be careful to eliminate the possibility
that the supposed thickening is in fact only due to oblique
sectioning of the wall. A familiar instance in sagittal sections is the inequality in the ventral and dorsal walls of the
aorta; the dorsal wall, on the outer curvature, receives its
coat earlier and is usually somewhat thicker than the ventral.
Another type of local inequality in wall thickness is that
in which s m e outside structure sufficiently supports the
vessel wall, rendering further efforts to withstand the pressure from within unnecessary, at least temporarily. I n these
instances the mesenchyma does not differentiate locally, as is
shown in figure 2. Here it is a nerve, the vagus and its branch
the recurrent laryngeal, against which the vessel, the ductus
arteriosus, is resting and which makes the strength of the.
wall in that particular region. I have also noticed vessels
where veins, other arteries, even the angularly set branch
of the same vessel served to relieve the pressure and allow a
thin place in the wall. Nature seems to add the coat only in
order to withstand the internal pressure, and to make use of
any other available means to attain the desired result. The
effect is purely local, as the mesenchymal layers are interrupted only f o r the nerve or other support, which thus
becomes imbedded in a wall otherwise of even thickness.
A rarer and more extensive change of caliber and of wall
thickness in continuous vessels is shown in the older stages
of the turtle, Chrysemys marginata. At 29 mm. the whole
arterial system of these embryos is formed of thick-walled,
massive vessels, except for the two ductus arteriosi, right and
left, which are greatly expanded, thin-walled sacs, in striking
contrast t o the neighboring arteries, as is shown in figures
3 and 4. The whole extent of these dorsal portions of the
pulmonary arches, from the points of origin of the pulmonary
arteries to the dorsal aorta, is of the same character, the
thin wall merging at each end into the adjacent thick ones by
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JOHN LEWIS BREMEB
rapidly tapering zones, wedge-shaped in longitudinal sectiori.
From the heart the blood must pass through the thick-walled
proximal portions of tho pulmonary arches either to the.
pulmonary arteries, also thick-walled but of much smaller
caliber, o r into these expanded sacs on its way to the dorsal
aortae. There must be an abrupt lessening of pressure and
rate of flow during this passage.
Fig. 3 Reconstruction from sagittal sections of the right aortic and pulmonary arches of a turtle embryo, as seen from the right side. The vessels a r e
f o r the most p a r t represented as bisected longitudinally to show the relative
thickness of their walls. The dorsal aorta lies at the left of the figure, the
heart would be to the right. The pulmonary arch gives off the pulmonary
artery a n d continues as a thin-walled, curved, bulging ductus arteriosus, which
joins the aorta. Chrysemys marginata, 31.7 mm., I€. E. C. no. 1101.
This condition is first noticeable in Chrysemys embryos of
about 11mm., where a distinct relation with the vagus nerve
can be observed, for the large vagus indents deeply the lateral
side of the vessel. From then on the ductus grows in caliber
and length, but the wall remains thin far beyond the limit of
the nerve. Even earlier than this the pulmonary and aortic
arches differ from each other, the pulmonary being much
WALL THICKNESS I N THE EMBRYONIC ARTERIES
5
the larger throughout its extent. Ultimately the dilated ductus comes in contact with the overlying fourth arch, around
which it bulges both mesially and laterally, as shown in
the figure, and which may thus lend support to the thin walls ;
but the sides and floor of the ductus are not so supported,
and yet remain thin.
The interpolation of these flaccid, sac-like segments along
the course of the pulmonary stream may remind one of the
similar thin-walled enlargements seen frequently in the early
embryonic conus arteriosus, and called the ‘aortic sac’ by
Congdon (’23); and the purpose may be the same in both
cases, namely, to reduce the full force of the pulse beat and
insure a more regular flow of blood along the distal vessels.
Yet in the turtle of this age there is no such thin-walled segment on the conus nor on any of the other arteries leaving the
heart, which seem able of themselves to regulate the blood
stream, as do adult arteries ; and it would seem unnecessary
t o have the pulmonary arch alone provided with such a safety
valve. Another thought might occur, that the thin walls in
this particular place represent merely an attempt at economy
of effort on nature’s part, in refusing to provide muscular
walls of any great thickness for a vessel so soon to become
obliterated. If this were the case, one would expect to find
somewhat similar appearances in other members of the reptile group. I n the snake, Eutaenia radix, however, where
only one ductus persists till hatching, the channel of the
arch is of the same caliber throughout, and the walls of the
same thickness as those of neighboring arteries. (It is
curious that in this form, whereas the left lung and left pulmonary artery are absent, it is nevertheless the left ductus
arteriosus that is used, the right disappearing some time
before hatching. Thus, as there is no left pulmonary artery,
the whole arch becomes ductus arteriosus, and is obliterated
in toto.) The other reptiles examined show also no marked
difference in thickness in different parts of the pulmonary
arch. The peculiarity is certainly not a reptilian characteristic.
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J O H N LEWIS BREMER
The fate of these enlarged sacs in the turtle may point
toward the explanation of their presence. Shortly after
hatching1 changes take place leading toward the final closure
of the vessel. At one stage the walls are folded irregularly
inward, until the passage is almost occluded ; within three or
four days the closure is complete. The procedure differs
from that in other vertebrates, however, in that it is the distal
end of the tube which clo~esfirst, and in that the ductus
becomes longer and straighter than before. The closure is
initiated by the contraction of the muscles of the narrow
tapering zone, near the aorta. The result is a relatively
capacious caecum or blind branch appended to the pulmonary
artery, in its course to the lung. The sac thus formed is
broader than the aortic arch, and capable of holding a considerable quantity of blood. If one blows into a canula whose
point is inserted in the pulmonary trunk of a turtle a few
days old the flaccid ductus can be seen to expand and become
tense. No air leaks into the aorta. When the pressure is
released, the ductus is immediately much reduced in size, as
though its walls contained elastic elements, and finally
resumes its collapsed condition. The force of the pulse beat
is not, however, sufficient to dilate the vessel to a noticeable
extent, as observation with the hand lens while the heart
is still beating shows no variation in caliber in the ductus
synchronizing with the pulse. At fifteen or twenty days after
hatching the ductus has become shrunken and obliterated
for fully half its length, and the proximal, remaining half
has been reduced in caliber by a rearrangement of the tissue
of its walls, which are now nearly as thick as in the ventral
portion of the arch. The obliteration of the lumen proceeds
from near the dorsal aorta toward the pulmonary artery,
and soon is completed for the whole ductus. The two vessels,
right and left, progress together at every step.
The presence of an expansile sac of considerable capacity
on each of the pulmonary arteries in the young turtle, a sac,
'I wish t o express my thanks t o Dr. Pauline Kimball and Dr. Frank A.
Stromsten, who have kindly supplied me with these older stages.
WALL THICKNESS IW THE EMBRYONIC ARTERIES
7
which gradually diminishes in size and finally disappears
entirely, leads one to speculate as to the probable usefulness
of these structures and the necessity for them in these special
reptiles.2 They could serve either as reservoirs for blood o r
as reducers of the pulse beat, or in both of these capacities.
Tbere should be some peculiarity of the turtle, among vertebrates, which might call for these special functions. The
lungs are, of course, indicated as the site of this peculiarity,
as the organs to which the arteries in question pass.
The turtle lung has long been recognized as one in which
the phylogenetic step has just been made from the primitive
saccular form to the higher lobular type with branching
bronchioles leading to independent air sacs. The branching
is only slight, however, as was shown by Miller ('04), since
the air sacs number only seven in each lung. The branching
of the pulmonary artery is also slight, and the resulting
arterioles break up almost immediately into thin-walled capillaries. This rapid change from thick-walled artery to thinwalled capillary might readily result in excessive pressure
within the smaller vessels, especially in those of the lung
which must already withstand the shock of rapid expansion
with breathing. To lessen this danger the distal end of the
pulmonary artery proper is found t o be, in turtles fifteen to
twenty days old, of large caliber and with thin walls, as
opposed to the smaller caliber and thicker walls found at its
union with the pulmonary arch, so that the pressure diminishes as the vessel is traversed by the blood. This is not the
case in turtles just before hatching, in which the artery is of
a uniform small caliber throughout. It occurs to me that,
as the young normally enter a hibernating period almost
immediately on hatching, the small artery may be sufficient
in that state to supply the necessary blood t o the lungs; but
that when the turtles are prevented from hibernating and
'A. Brenner noted a slight rounded swelling a t the junction of the pulmonary
artery and the obliterated ductus botali in Test,udo graeca, and figures the pulmonary arch as of greater caliber than the branch t o the lung. Arch. f. Anat.
u. Entwick., 1883.
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J O H N LEWIS BREMER
forced to lead an active life, as in the case of those examined
and described here, the artery becomes enlarged distally as
a means of protection. The expansile sac of the ductus
arteriosus may act as an additional safety valve. With more
mature adjustment the lung arteries become better able to
regulate the blood stream. I n the adult turtle the entire
ductus has been reduced t b the usual fibrous cord, and the
adult pulmonary artery, from heart to lung, is of even large
caliber.
The crocodile is classed with the turtle by Wiedersheim
(in his Lehrbuch) in respect to the phylogenetic position of
the lung. I have not the necessary older stages of crocodile
embryos to learn of the later condition of the ductus arteriosus in this form, whether o r not it shows the characteristics
described for the turtle as possibly corresponding to the lung
structure. In the young alligator embryos available, however, the pulmonary arches are much larger than the others,
and it will be remembered that this was characteristic
also of the younger turtle embryos. The coincidence
is suggestive.
The whole stream from the right ventricle does not pass
t o the lungs in the turtle, as the left fourth arch, as is well
known, also arises from this chamber of the heart t o join the
dorsal aorta, after giving off branches to the stomach, liver,
and intestine. Also from the left pulmonary arch a small
branch passes mesially and ventrally to a parathyroid gland
and to the wall of the trachea. The lack of a complete interventricular septum probably allows a mixture of venous and
arterial blood, so that these various organs are not so poorly
served as one would at first imagine. The whole force of
the pulse beat is not, however, directed toward the lungs.
In the chick the ductus arteriosus also exhibits thin walls,
in contrast to the more massive pulmonary artery. Here
again, just before hatching, the two pulmonary arches are
complete, though only the right fourth arch persists, the left
having long before degenerated and disappeared. From each
pulmonary arch branches a pulmonary artery, of much
W A L L THICKNESS I N THE EMBRYONIC ARTERIES
9
smaller caliber but with a continuation of relatively thick
walls. From this point to the dorsal aorta on each side
extends the ductus arteriosus, slightly larger than the proximal segment of the arch, but with thinner walls. The striking
effect made in the turtle b:r the sudden changes in caliber and
thickness of wall is lost, however, in the chick, because the
ductus is straight and tubular, instead of saccular, and because it joins a thin-walled dorsal aorta. I n fact, examination
of all the main arteries of an older chick embryo shows that
the thinness of wall of the ductus is only one example of numerous similar differences in wall thickness throughout the
arterial system.
As can be seen in figure 5, of a chick of nineteen days’
incubation, the aortic arch is massive, but is continued into
a dorsal aorta of much larger caliber but with much thinner
walls. The t,ransition is abrupt. I n the pulmonary arches
the transition, as has been mentioned, occurs at the proximal
end of the ductus. The carotid, or brachiocephalic arteries,
though of small caliber, are provided near the heart with
coats equaling in thickness those of the arch of the aorta,
the diameter of which is several times as great. If the vessels
are traced further, beyond the limits of reconstruction, the
descending aorta remains thin-walled and of large caliber,
but its first branch, the coeliac artery, is again small and
provided with a coat actually thicker than that of the parent
stem, proportionately much thicker, as is shown in figure 6.
The vitelline and allantoic arteries are also thick-walled. I n
the head region the external carotid artery is a thin-walled,
flaccid continuation of the massive brachiocephalic trunk,
and as such extends throughout the long neck into the head.
There, near its terminal branches to the face and the eye, it
abruptly assumes massive walls and a small caliber, which
are continued along the branches. The transition here is on
the artery itself, not, as in the coeliac artery, definitely on
the branch. It will be seen that in both directions, cranially
and caudally, the blood from the heart passes first through
relatively narrow, thick-walled arteries, then through long
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J O H N LEWIS BRGIMER
stretches with larger caliber and thinner walls, then again
through smaller thick-walled vessels. Not in every case,
however, for the brachial branch of the brachiocephalic
artery shows no such expanded area and no thinning of the
walls beyond what is usual with lessening size after repeated
branching; and, on the other hand, the smaller branches of
the dorsal aorta to the back and to the mesoiiephros show no
return to the thick-walled condition.
Several suggestions can be made in explanation of these
facts, but only, I think, to be discarded. Congdon mentions
Streeter 's view that the early proliferation of endothelium
entailed in vessels of great size may serve as a reserve for
the future rapid differentiation of the vascular system.
While this suggestion may explain the relatively enormous
vessels of young embryos, in which connection it was put
forth by Streeter, it would not so readily apply t o the established arteries of chicks or turtles about to hatch, nor t o the
ductus arteriosus, which is soon to become obliterated. On
the other hand, the supposition that muscular and elastic
tissue had not been supplied to the ductus arteriosus of these
two forms because nature had foreknowledge of their future
obliteration and declined to expend unnecessary energy on
tissue building, is denied by the numerous instances of purely
embryonic vessels which are provided with thick coats, and
would fail to explain the thin walls found in many permanent arteries,
The possibility that vessels of different embryological
origin may retain, in certain forms, characteristic rates of
wall development, though already united and used as a continuous channel, might be considered. Thus the aortic arches
might conceivably develop walls thicker than those of the
dorsal aorta. This might explain the sudden change in character of the aorta shown in figure 5, as the area of rapid
reduction of wall thickness may very probably mark the
junction of fourth arch and dorsal aorta, as is seen by studying younger chick embryos in which the dorsal aorta, between
the third and fourth arches, is still present. The massive
WALL THICKNESS I N T E E EMBRYONIC ARTERIES
11
portion may represent arch, the thin portion aorta. Carrying this idea to the pulmonary arch, one might consider that
the thin-walled ductus arteriosus represents that portion of
the arch which has developed as an outgrowth of the dorsal
aorta, and therefore inherited its characteristics, though in
Fig. 5 Reconstruction from tzransverse sections of the right aortic and pulmonary arches of a chick embryo of nineteen days’ incubation, as seen from
the left or medial side. The heart, therefore, would lie t o the left of the drawing. The left pulmonary arch and ductus arteriosus, though present in the
embryo, are not shown in the reconstruction. The two brachioeephalic arteries,
pointing upward toward the head, have small caliber and thick walls. The
dorsal aorta shows a sudden increase in caliber and reduction in wall thickness,
as does also the ductus arteriosus.
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J O H N LEWIS BREMER
that case one would expect this influence to be shown on the
fourth arch as well, and also on the branches of the dorsal
aorta, which have been shown, on the other hand, to be in
general thicker than the parent vessel. And if one traces the
vessels cranially no such differentiation into thick arch and
thin dorsal aorta appears. No part of the internal carotid
artery, which should represent the third arch and cranial
dorsal aorta, shows the expected differentiation. On the
other hand, the sudden thickening of the walls of the external
carotid artery in the head, already referred to, falls into no
scheme based on the aortic arches. It would be difficult
indeed in the chick t o correlate all the facts with the known
embryological development of the vessels.
The arterial walls of the older chicks are much thicker as
a whole near the heart, and appropriate stains reveal a large
amount of elastic tissue in the arch of the aorta and in the
proximal parts of the carotid arteries and pulmonary arches,
in contrast t o the absolute lack of it in the heart proper and
to the small amount found in the more distal parts of these
vessels. This looks like, and probably is, a special arrangement connected with the heart beat, but proximity to the
heart and the necessity to withstand and lessen the force of
the pulse cannot be given in explanation of the thickness of
wall of distal branches, like the coeliac artery. The possibility that the thick-walled segments of small caliber are
merely the results of greater contraction in these areas
merely carries the question one step further, f o r it suggests
differences in structure or arrangement of the muscles to
account for the differences in contraction, without offering
any explanation of the varying types of wall.
While, therefore, plausible explanations can be given for
the short, localized variations in the thickness of arterial
walls, and even f o r the peculiarities of the ductus arteriosus
in the turtle, I fail to find any reasoaable explanation f o r
the abrupt changes in caliber and character of the arteries
of the older chick embryos. That the implied variations in
rate and pressure of the blood stream must have some
WALL T H I C K N E S S I N T H E EMBRYONIC ARTERIES
13
advantageous relation, past, present, or future, to the development of the embryo, I do not doubt. The passage OP
blood from the large thin-walled aorta or carotid arteries,
where most of the force of the pulse beat must be lost and
the rate of flow must be slow, into narrower channels with
much more muscular walls would seem to imply a peristahic
action or autonomous pulsation in these distal arteries, capable of increasing the rate until it conforms with the type
of vessel. Such independent arterial pulsation has been
recognized in invertebrates, notably in the squid, but is
usually denied f o r vertebrates.
SUMMARY
The walls of embryonic arteries, of various vertebrate
types and different ages, occasionally show marked variation
in the thickness of the muscular coat, The cause f o r the
particular thinning o r thickening may be easily understood
in some cases, as when the outer curvature of a bend is
especially strengthened t o withstand the pressure of the
stream or when the vessel is supported by some other structure, as for instance a nerve, and remains locally thin-walled.
Photographs of these two conditions are shown. More
extensive thinning is seen in the ductus arteriosus of the
older turtle embryos, which is reduced to a flaccid expanded
sac. The changes in this sac after hatching are followed,
and its probable service in protecting the pulmonary capillaries from excessive blood pressure is suggested. In the
older chick embryos the whole dorsal aorta is thin-walled and
of large caliber, though continuous with massive aortic
arches and with many thick-walled branches. No cause but
that of a supposed physiological advantage can be given f o r
this curious variation in thickness of arterial walls.
BIBLIOGRAPHY
CONGDON,E. D. 1923 Transformation of the aortic-arch system during the
development of the human embryo. Contrib. t o Emb., no. 68.
MILLER, W. S . 1904 Development of the lupg in Chryseniys picta. Am. Jour.
Anat., 1701. 3, no. 1, pp. 15-16.
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