[ 224 ]
SOME OBSERVATIONS ON DIAPHRAGMATIC
BLOOD SUPPLY
By F. BECK AND J. S. BAXTER
Department of Anatomy, University College, Cardiff
Much detailed work has been done on the nerve supply of the diaphragm in man and
animals, and the results obtained have resulted in important conclusions concerning
the development of the diaphragmatic musculature. The blood supply of the diaphragm in mammals is less well known, and indeed Green (1955) in her monograph
on the anatomy of that commonly used laboratory animal, the rat, gives little
detail of the arterial supply and does not mention the venous drainage at all. We
have studied the vascular pattern of the diaphragm, chiefly in the rat, preliminary
to an investigation of its development.
MATERIAL AND METHODS
Preparations of the blood vessels of the diaphragm were made in twenty-eight adult
and four new-born rats in several ways. (1) Coloured neoprene latex was injected into
either the arterial or venous system or in some cases into both. In two new-born
rats indian ink was the injection medium. (2) Intravascular haemoglobin was stained
by Pickworth's method (as modified by Pfaff & Williams, 1940) in four adult specimens. Blood vessels were stained by Grant's (1929) technique in three adults. We
found the latter method gave good results when certain modifications were made,
namely, the injection of acetylcholine and sodium citrate into the circulation
immediately on death of the animal and continuance of the perfusion, after this,
with well-filtered Ehrlich's haematoxylin in 10 % formalin at a pressure of 120 mm.
of mercury for 3 hr. (3) Histological sections at various key areas of the diaphragm
in five adult rats were stained with haematoxylin and eosin and by van Gieson's
method.
We have also made injection preparations of the diaphragm from an adult dog,
an adult cat and two adult specimens of the fruit bat (Pteropus).
RESULTS
The vascular pattern of the diaphragm in the rat
(A) The arterial supply of the rat's diaphragm is shown in Plate 1, fig. 1, in which
the preparation is viewed from the abdominal aspect.
The arterial vessels in the rat diaphragm are these:
(1) Inferior phrenic vessels (left and right).
(2) Superior phrenic or pericardiaco-phrenic vessels.
(3) Intercostal rami.
(4) Musculo-phrenic arteries.
(5) Twigs from the internal mammary arteries.
Some observations on diaphragrnatic blood supply
225
There are some further points about these vessels which should be mentioned.
(a) The inferior phrenics, arising from the abdominal aorta, are the chief supply
of the crura and the central area of the pars costalis; they are often supplemented
by accessory inferior phrenic arteries.
(b) The peripheral part of the muscular diaphragm is vascularized by twigs from
the 7th to 12th posterior intercostal arteries, by radicles from the loop anastomoses
between the 6th anterior and 6th posterior intercostal arteries (the musculo-phrenic
artery) and by terminal branches of the internal mammary arteries.
(c) The superior phrenic or pericardiaco-phrenic arteries are small vessels
accompanying their respective phrenic nerves to the diaphragm and are of small
importance.
(B) The venous drainage of the diaphragm presents a remarkably constant pattern
which is shown in Plate 1, fig. 2, the position of these veins being of significance when
considered in terms of the function of this structure.
The venous drainage is mediated by four main channels on each side. They
are:
(1) Anterior phrenic vein.
(2) Middle phrenic vein.
(3) Posterior phrenic vein.
(4) Accessory posterior phrenic vein (a composite venous channel).
Small diaphragmatic tributaries of the musculo-phrenic and intercostal veins
drain the periphery of the diaphragm and anastomose with tributaries of the anterior
middle and posterior phrenic veins (P1. 2, fig. 1). A cross-anastomosis between the
veins of the right and left sides of the diaphragm called the transverse phrenic vein
completes the symmetrical pattern.
Certain features of these veins have now to be detailed.
(a) The anterior phrenic veins run antero-posteriorly at the boundary between the
pars costalis and the anterior leaf of the central tendon (PI. 2, fig. 3). Straight
radicles pass from the muscular part of the diaphragm into the anterior phrenic
veins. These are vessels which are parallel to the longitudinal direction of the
muscle fibres and drain the pars costalis. Peripherally they anastomose with the
lower intercostal, internal mammary and musculo-phrenic veins. The right anterior
phrenic vein terminates, as a rule, in the middle phrenic vein near the caval orifice
and thus forms an arc around a part of the circumference of this opening. The left
anterior phrenic vein ends in the transverse phrenic vein within the boundary of the
central tendon. The very anterior part of the anterior phrenic vein is occasionally
found to run within the muscle of pars costalis for a short distance before it reaches
the boundary between muscle and tendon. In these cases another vein joining
the anterior phrenic vein where the latter reaches the boundary is found between the
muscle and tendon further anteriorly (PI. 2, fig. 2).
(b) Middle phrenic veins. The right vein opens directly into the inferior vena cava
as this passes through the diaphragm, while the left joins the posterior phrenic vein
at the junction of muscle and central tendon to form the transverse phrenic vein.
The middle phrenic veins again run parallel to the long axis of the muscle fibres and
their tributaries show a 'stepped' appearance as if made up of centripetally running
vessels connected by cross-anastomoses (PI. 2, fig. 2). They are responsible for the
15
Anat. 94
226
F. Beck and J. S. Baxter
drainage of a large part of the pars costalis and have peripheral connexions with tne
7th to 9th intercostal veins.
(c) Posterior phrenic veins. The termination of the right vein is in the inferior
vena cava while the left uniting with the left middle phrenic vein forms the transverse phrenic vein. Traced backwards, each vessel runs just within the boundary of
the central tendon to the apex of the dorso-lateral leaf and then lateral to the
lumbo-costal trigone. Each vein receives numerous straight tributaries on the lateral
side parallel to the muscle fibres and these connect peripherally with the lower intercostal veins. There are some medial tributaries, the most important being two on the
right side (Plate 1, fig. 2) related to the right inferior phrenic artery and coming from
the pars lumbalis of the diaphragm. They communicate with the right accessory
posterior phrenic vein.
(d) Accessory posterior phrenic veins. These veins arise by a number of small
radicles in the crura where they have anastomoses with the azygos system and the
1st lumbar veins. They then run towards and cross the dorso-lateral leaf of the central
tendon, first communicating with each other along its medial margin and ending,
after having traversed the tendon, in the inferior vena cava, the right posterior
phrenic vein, the transverse phrenic vein and the left posterior phrenic vein. They
thus form a venous cross-connexion in the medial margin of the dorso-lateral leaf of
the central tendon-the accessory posterior phrenic vein.
(e) Transverse phrenic vein. This is an important large vein connecting the left
side of the diaphragmatic venous drainage with the inferior vena cava. It receives
all the major veins of the left half of the diaphragm and begins at the boundary
between the central and left dorso-lateral leaves of the central tendon. It passes to
the right just within the central tendon near to the two fused crura. The vein has a
few small tributaries from the anterior leaf of the central tendon and others which
have already been mentioned.
(f) Diaphragmatic tributaries of the musculo-phrenic and intercostal veins were
clearly demonstrated in animals where the azygos system had been injected, and
also in preparations of the blood vessels made by Grant's method (P1. 2, fig. 1). They
drain the peripheral part of the diaphragm and anastomose in series with the anterior
phrenic, middle phrenic and posterior phrenic veins (P1. 2, fig. 1).
Small veins draining the crura appear to run to the lumbar veins or to the azygos
vein as this pierces the diaphragm.
The superior phrenic vein (P1. 2, fig. 1) running with the phrenic nerve has a small
and inconstant area of drainage.
Brief additional notes on the diaphragm of the bat, cat and dog
The arterial supply in the bat is very similar to that found in the rat except
that the inferior phrenic arteries arise by a common stem from the abdominal aorta
(P1. 3, fig. 1). The venous drainage again is remarkably like that in the rat with the
familiar pattern of anterior, middle, posterior and accessory posterior phrenic veins
'framing' the central tendon on each side and connected by the transverse phrenic
vein (P1. 3, fig. 2). The commencement of both posterior phrenic veins and a part of
the right anterior phrenic vein run within the muscle at right angles to its fibres, but
this does not appear to be a significant difference, since the muscle on the central
Some ob8ervatione on diaphragmatic blood eUpply
227
tendon side of the veins is much attenuated in comparison with the main portion of
the pars costalis on their lateral side.
The diaphragmatic venous drainage in the dog (P1. 3, fig. 3) shows the same pattern
as in the rat. Where the beginning of both anterior phrenic veins appears to be
embedded in muscle and the course to be at right angles to the direction of the
muscle fibres the thickness of the diaphragmatic muscle on the medial and lateral
sides of the vein is precisely the same as in the bat. Furthermore, a small vein is
found on the left side at the junction of muscle and tendon in addition to the main
anterior phrenic vein when the latter is running in the muscle.
The veins of the diaphragm in the cat (PI. 3, fig. 4) show, as it were, a standard
pattern, except that the dorso-lateral leaf of the central tendon is very narrow and
accessory posterior phrenic veins are absent.
DISCUSSION
The foregoing, strictly morphological, account of the vascular supply of the diaphragm provides a necessary basis for further work in this field. From it the following points emerge.
(1) The venous drainage of the diaphragm is very constant in all the specimens
examined, and furthermore a remarkable bilateral symmetry is immediately
apparent. The diaphragmatic veins are the only tributaries of that component of
the adult inferior vena cava which is developed from the hepatocardiac channel and
this segment is itself the right member of the originally bilateral vitelline veins
(Streeter, 1942).
The problem now arises as to whether the drainage of the left half of the diaphragm
is into tributaries of the left vitelline vein which has become secondarily connected
with the right vitelline vein by means of the transverse phrenic vein; in the same way,
for example, that the intersubcardinal anastomosis connecting the two primitive
subeardinal veins, persists in the adult as the left renal vein and allows the cephalic
part of the left subcardinal vein to regress as a consequence.
Blair (1922) described in the human a perforating vein present fairly constantly
at a point on the left side corresponding to the position of the caval orifice. This he
considered to represent a continuation of the left vitelline vein above the diaphragm.
The perforating vein he described eventually joined the inferior vena cava by means
of a transverse vein running on the superior surface of the diaphragm. No evidence
of such perforating or transverse vein was seen macroscopically in the specimens
studied here. Of course this finding does not exclude its occasional presence but
even if it were never present, the transverse phrenic vein could still represent the
foetal connecting channel between the right and left vitelline veins running on the
abdominal surface of the diaphragm.
Work is at present being done by injection methods on rat foetuses to elucidate the
origin of the diaphragmatic veins.
(2) The second point of interest concerning the venous drainage of the diaphragm
is the constant position of the main venous channels just within the central tendon
of the diaphragm. These veins run at right angles to the direction taken by the diaphragmatic muscle fibres, they lie on the abdominal surface of the diaphragm and
15-2
228
F. Beck and J. S. Baxter
their centrifugal tributaries run parallel to the direction of the muscle fibres and are
buried within the substance of the muscle.
Clark (1918) enlarging on the work of Thoma (1898) dealt with the development
of blood vessels in tadpoles; he considered that a certain degree of development of
blood vessels is genetically determined but that beyond a certain point mechanical
and functional factors cause the final pattern. Two of these factors are that:
(i) The amount of blood flow through a vessel regulates its diameter.
(ii) Increase in the length of a vessel is due to surrounding tissue tension.
Anrep (1934 a, b) has studied the effect of muscular contraction upon blood flow
and concludes that the blood flow through the diaphragm is diminished during
its normal spontaneous contractions. This diminution in the amount of blood flow
presumably affects the muscular veins most severely, particularly those which run
across the direction of the muscle fibres. It therefore seems reasonable to assume
that such transversely (in relation to the muscle fibres) running veins would not
develop in the embryo from the pre-existing capillaries-which form a network
from which the adult arteries and veins will differentiate-until the region of the
central tendon is reached where muscular contraction cannot further affect blood
flow through the veins. This is found to be the case in the diaphragms studied. One
might consider its part in venous drainage to be one of the functions of the central
tendon. Furthermore, the second of Clark's mechanical factors quoted above would
ensure that the centrifugal tributaries of the central veins would run parallel to the
direction of the muscle fibres, as indeed they do.
Following this line of argument it is unnecessary to postulate the existence of a
left vitelline venous system to account for the symmetry of the diaphragmatic
venous drainage; nevertheless, such a basic genetic system is not disproved by the
finding that reinforcing mechanical factors exist. In fact the existence of some veins
running in the muscle and yet transversely to the long axis of the muscle fibres, such
as the anterior part of the anterior phrenic veins in the dog, suggests an hereditary
basis since mechanical factors cannot have operated in the production of these
particular vessels.
(3) The specimens studied clearly demonstrate an anastomosis between the caval
and azygos venous systems involving the diaphragmatic veins. The normal and
potential functioning of this anastomosis was not investigated, though its existence
in the cat has previously been stated by Sudzilovskii (1958).
(4) As a corollary to the above it is of interest to note that blood enters the pars
costalis from the periphery and leaves it centrally, in other words the common
arrangement of arteries entering and veins leaving a muscle at the same hilum does
not exist here. The relationship of this arrangement to muscular contraction may be
worthy of investigation.
(5) Belou (1934) in his work 'Revision anatomica del sistema arterial' shows an
arteriograph of the arterial supply of the human diaphragm. The similarity with
the above descriptions is striking.
Some observation on diaphragmatic blood supply
229
SUMMARY
The distribution of the arteries and veins in the diaphragm of the rat has been
studied by: (1) injection methods; (2) the staining of gross specimens (methods of
Pickworth and Grant) and (3) the examination of microscopic sections. Comparison
is made with the vessels in the fruit bat (Pteropus), the cat and the dog.
The arterial supply is derived from: (1) inferior phrenic vessels; (2) superior
phrenic or pericardiaco-phrenic vessels; (3) intercostal vessels; (4) musculo-phrenic
vessels; and (5) internal mammary vessels. The courses of these vessels and the
areas supplied are described.
The venous drainage by anterior, middle, posterior and accessory posterior phrenic
veins is found to be remarkably constant in its main features. The major veins lie
just within the confines of the central tendon and show a bilateral symmetry. They
represent the only tributaries of the embryonic hepato-cardiac channel (Streeter,
1942) to be found in the adult. Two hypotheses, one genetic and the other mechanical,
regarding the formation of these veins are advanced and discussed.
The presence of an anastomatic system of diaphragmatic veins connecting the
inferior vena cava and azygos veins first noted in the cat by Sudzilovskii is confirmed
in the rat.
We should like to thank Messrs A. Welch and L. Jones for taking the photographs
for us and Miss M. White for her painstaking production of the illustrations.
REFERENCES
ANREP, G. V., BLALCOCK, A. & SAMAAN, A. (1934a). The effect of muscular contraction upon blood
flow. Proc. roy. Soc. B, 114, 223-244.
ANREP, G., CERQUE, S. & SAMAAN, A. (1934b). The effect of muscular contraction upon the blood
flow in the skeletal muscle, in the diaphragm and in the small intestine. Proc. roy. Soc. B,
114, 245-257.
BELOU, P. (1934). Revision anatomical del sistema arterial. Representation: Libreria y Editorial
'El Ateno', Buenos Aires. Vol. 3, 90-91.
BLAIR, D. M. (1922). A study of the central tendon of the diaphragm. J. Anat., Lond., 57,203-215.
CLARK, E. R. (1918). Studies on the growth of blood-vessels in the tail of frog larva by observations
and experiment on the living animal. Amer. J. Anat. 23, 87-88.
GRANT, R. T. (1929). Observations on direct communications between arteries and veins in the
rabbit's ear. Heart, 15, 281-300.
GREEN, E. (1955). The anatomy of the rat. New York: Hafner Publishing Co.
PFAFF, R. A. & WiuLLAms, W. L. (1940). The use of the benzidine method on thick specimens.
Stain Tech. 15-17, Index 11-15, 165-169.
STREETER, G. L. (1942). Developmental horizons in human embryos; age group XI, 13-20 somites
and age group X1I, 21-29 somites. Contr. Embryol. Carneg. Instn, 30, 211-245.
SUDZILOVSKII, F. V. (1958). The collateral blood circulation in the vena cava system of the cat.
Arkh. Anat. Gist. Embr. 33, 4S-48. (Abstracted in Excerpta med. 12, 1279.)
THOMA, R. (1893). Untersuchungen uber die histogenese und histomechanik des geftissystems.
Stuttgart (quoted by Clark, E. R. 1918).
230
F. Beck and J. S. Baxter
EXPLANATION OF PLATES
PLATE 1
Fig. 1. Arterial supply to the diaphragm of the rat. a, accessory right inferior phrenic artery;
b, 12th rib; c, right inferior phrenic artery; d, its oesophageal branch; e, branches of posterior
intercostal artery; f, caval orifice; g, branches of musculo-phrenic artery; h, branches of
internal mammary artery; i, oesophageal orifice; j, oesophageal branches of left inferior phrenic
artery; k, origin of lateral branch; 1, left inferior phrenic artery; m, aortic orifice.
Fig. 2. Venous drainage of the diaphragm of the rat (viewed from the abdominal aspect).
a, lumbo-costal trigone; b, caval orifice; c, transverse phrenic vein; d, left anterior phrenic
vein; e, left middle phrenic vein; f, left posterior phrenic vein; g, right and left accessory
posterior phrenic veins.
PLATE 2
Fig. 1. Rat diaphragm stained by Grant's method demonstrating the anastomoses between the
azgyos and caval venous systems. Note the left superior phrenic vein indicated by arrow. x 2k.
Fig. 2. Rat diaphragm with the veins injected with neoprene latex. Note the anterior part of the
right anterior phrenic vein running within the pars muscularis, a smaller tributary indicated
by an arrow marks the boundary between muscle and central tendon in this region. x 2k.
Fig. 3. Section through the right anterior phrenic vein to show its relation to the muscle (M) and
central tendon (C.T.) of the diaphragm. The vein (V) (filled with neoprene) lies on the thoracic
surface of the diaphragm at this point and is overlapped on the abdominal surface by a tonguelike process of tendon which is continuous with the looser connective tissue of the central
tendon. x 100.
PLATE 3
Fig. 1. Diaphragm of fruit bat injected with neoprene latex to display inferior phrenic arteries.
Note division of common trunk (at arrow) giving rise to right and left inferior phrenic arteries
which in their further course accompany branches of the middle phrenic vein. x.
Fig. 2. Diaphragm of fruit bat injected with neoprene into arterial and venous systems. Note
similarity of venous drainage to that described in rat (see text). x j.
Fig. 3. Diaphragm of dog injected with neoprene to show venous system. Note similarity of
venous drainage to that of rat, cat and bat (see text). A small vein (a) marks the boundary
between the anterior leaf of the central tendon and the muscle beyond the point where the
main stem of the left anterior phrenic vein can be traced peripherally into muscle. The vessel
seen medial to this (b), within the central tendon, is an artery. x i.
Fig. 4. Diaphragm of a cat injected with neoprene latex to display the diaphragmatic veins. The
anterior and posterior phrenic veins lying just within the central tendon are clearly seen. Here
the posterior leaves of the central tendon are narrow and consequently there is no accessory
posterior phrenic vein. x j.
Journal
~ ahe\ sijEv:g. ~
of Anatomy,
Vol. 94, Part 2
Plate 1
I'/'~ ~ ~ ~ ~ ~ ~ I
k
Fig. 1
L^,.§C
Fig. 2
BECK & BAXTER
SoME
OBSERlVATIO(NS
ON
DIAPHRAGMATIC
BLOOD SUPPLY
(Facing p. 230)
Journal of Anatomy, Vol. 94, Part 2
_.
Plate 2
_
.--I
3W.
I
I
Ir
11
---
IC
Fig. 1
Fig. 3
a
.'~l~
.:
Fig. 2
BECK
AND
BAXTER-SOmE
OBSERVATIONS ON DIAPHRAGMATIC BLOOD SUPPLY
Journal of Anatomy, Vol. 94, Part 2
BECK AND BAXTER-SomIE OBSERVATIONS ON THE DIAPHRAGMIATIC BLOOD SUPPLY
Plate 3