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The development of the bronchial veins with special reference to anomalies of the pulmonary veins.

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The Development of the Bronchial Veins, with Special
Reference to Anomalies of the Pulmonary Veins
Department of Anatomy, University of Alberta, Edmonton, Alberta, Canada
This communication reports a restudy
of the venous drainage of the lungs and
bronchi, aimed to match the greatly increased knowledge of anomalies of the pulmonary veins brought about by modern
thoracic surgery. Nearly all workers on
pulmonary vein anomalies have depended
upon the early work of Brown (’13) and
have manipulated his schema to explain
the anomaly they are concerned with. For
this purpose Brown’s schema is inadequate; it lacks important additions found
in older embryos, and especially the venae
.cornitantes of the vagus nerves. Butler
(’50, ’52a, b ) has recently emphasized the
significance of these vessels in the development of pulmonary drainage. Neither
worker, however, says anything about the
development of the bronchial veins, vessels which must be involved in some of the
graver pulmonary vein abnormalities.
My work is an extension of Butler’s careful study, using the same methods. I first
studied the veins of 60 pig embryos ranging in length from 9 to 70 mm. The veins
of each embryo were injected with drawing ink through a no. 28 cannula into the
primary vein of the head, or into the heart,
or into the mesonephros. Each embryo
was fixed in fonnalin and cut into serial
sections. Its veins could then be reconstructed by the graphic method. Next, I
made a similar study of a corresponding
group of human embryos. These could
not be injected. However, if one chooses
embryos with veins dilated with blood, it
is possible to follow the vessels already
found in the pig, and to reconstruct them
graphically. With the results of the two
parallel studies before me, I surveyed the
chief recorded anomalies of the pulmonary veins in an attempt to make them
more understandable.
Normal development in the pig
One may start with the schema of
Brown (’13), reproduced here as figure 1.
It is a reconstruction of the vessels of a
4.5-mm cat embryo. At this stage the foregut is undivided and the lung buds faintly
indicated. All are enclosed in a tight
fitting splanchnic plexus. The plexus is
drained laterally through several taps into
the cardinal veins, and ventrally into the
heart by the primitive pulmonary vein and
a second caudal tap.
Each component of Brown’s schema:
the splanchnic plexus, the cardinal vein
taps, the pulmonary vein, and the caudal
tap-can be identified in a 12-mm pig embryo, whose veins are graphically reconstructed in figures 2 to 5.
A portion of the splanchnic plexus of
the 12-mm pig embryo is shown separately
in figure 3. As compared to Brown’s
earlier schema, the pig’s plexus has been
modified by the division of the foregut
into trachea and esophagus, and still more
by the growth of the vagus nerves. The
plexus around the esophagus and trachea
remains plexiform, but the lateral part of
the plexus around the vagus nerve and
its recurrent branch has been made over
into venae comitantes. The full extent of
these venae comitantes is shown in figure
2; they can be traced more or less continuously down to the stomach.
The second feature of Brown’s schema,
the venous taps into the cardinal veins,
also appears in the 12-mm pig. The taps
arise, not from the general splanchnic
plexus but from the venae comitantes of
the vagus nerves (fig. 2). The number of
taps vanes from embryo to embryo, but the
taps that face the origins of the recurrent
vagi are invariably the largest and most
constant. Their constancy and size foreshadows their later significance as origins
of the bronchial veins.
The third feature of Brown's schema,
the primitive pulmonary vein, drains the
growing lung buds of the 12-mm pig (figs.
2 and 4). The lung buds are clothed with
a portion of the early splanchnic pIexus
(fig. 4) with which the terminal branches
of the pulmonary vein interosculate. In
addition, the primitive pulmonary vein receives a constant branch that descends
along the esophagus to join the vena comitans of the left vagus (fig. 2). This is the
caudal tap of Brown's schema and the
vitello-umbilical tap of Butler ('52a). A
better name would be esophageal tap. The
esophageal tap communicates through the
left vagus vein with the gastric plexus,
which in turn communicates with the duc-
LEVEL flG.5.
Fig. 1 Schema of venous drainage of foregut of a 4.5-mm cat embryo. After Brown
('13). X 65.
Fig. 2 Graphic reconsbction of the veins of a 12-mm pig embryo. Splanchnic plexus
omitted. X 25.
Fig. 3 Schema of the splanchnic plexus of a 12-mm pig embryo.
Fig. 4 Section through the lung buds of a 12-mm pig embryo. X 25.
Fig. 5 Section through the stomach and liver of a 12-mm pig embryo. x 25.
tus venosus (figs. 2 and 5). This collateral
pathway has potential significance.
Of the later development of the main
pulmonary vein nothing can be added to
the usual text-book description. I will deal
henceforth with the venae comitantes of
the vagi and their recurrent branches, the
cardinal taps, and their bronchial derivatives.
The venae comitantes of the vagus
nerves of a 22.5-mm pig embryo are reconstructed in figure 6. Well injected
veins parallel the recurrent vagi, and follow the main vagi as far as the stomach.
Fig. 6 Graphic reconstruction of the veins of a 22.5-mm pig embryo. x 8.
Fig. 7 Graphic reconstruction of the veins of a 37-mm pig embryo. x 13.
Fig. 8 Graphic reconstruction of the veins of a 15-mm human embryo. x 25.
Fig. 9 Graphic reconstruction of the veins of a 29-mm human embryo. x 12.
Both nerves and veins have been affected
by the downward shift of the heart and
great arteries. The cardinal taps draining
the vagus veins are mostly restricted to a
narrow zone below the origin of the recurrent nerves. As before, the taps that
follow the hook of each recurrent vagus
are far better developed than the rest and
form the chief outlets of the venae comitantes of the recurrent vagi.
At the same time the cardinal veins are
undergoing their complex metamorphosis.
The azygos and hemiazygos veins have
formed along the sympathetic trunks; they
drain into the terminations of the posterior
cardinal veins. The terminations of the
azygos and hemiazygos veins into the cardinal system lie opposite the recurrent
vagus taps.
The 37-mm pig embryo (fig. 7) is characterized by the appearance of the bronchial veins and a general breakup of the
cardinal system of veins.
The left bronchial vein appears as a
leash of small veins that arise from the
termination of the left recurrent vagusi
vein. The leash uses the part of the recurrent vagus vein that hooks beneath
the ductus arteriosus to enter the posterior cardinal vein. The right bronchial
vein appears as a similar leash of vessels
from the right vagus vein. This leash uses
a cardinal tap to enter the termination of
the azygos vein. The bronchial veins are,
therefore, outgrowths from the venae comitantes of the vagus nerves.
The human anatomist, expecting the
left bronchial vein to enter the hemiazygos
and the right bronchial to end in the
azygos, may be confused by the pig’s arrangement. The pig’s arrangement is
really the same as in man, only it is
masked by a different development of
the azygos and hemiazygos veins. In the
pig the hemiazygos is the larger vein
(Reagan, ’19); it uses the end of the left
posterior cardinal to enter the coronary
sinus, and retains this outlet in the adult.
Hence the left bronchial of the pig seems
to enter the coronary sinus. On the right
side the pig’s azygos disappears save for
a terminal fragment, which persists as
the cervico-thoracic vein of Reagan. The
pig’s right bronchial drains into this termi-
nal part of the azygos-just as the right
bronchial vein does in man.
Normal development in man
After one has followed the injected
veins o i pig embryos, one can trace similar vessels in human embryos, provided
the vessels are well dilated with blood.
The veins of a 15-mm human embryo
(fig. 8) are a fair copy of those of a 12mm pig (fig. 2). A well defined vena
comitans follows each recurrent vagus
nerve and the main vagus nerve below.
Each vein drains through several taps into
the cardinal veins. The largest taps face
the origin of the recurrent nerves. The
pulmonary vein is a short vessel, with a
well developed esophageal branch which
mingles caudally with the vessels around
the vagi and esophagus. Farther caudad
a fragment of the gastric plexus can be
traced; it has connections across the lesser
omentum with the ductus venosus.
The human bronchial veins appear in a
29-mm embryo (fig. 9). The left bronchial arises as a leash of vessels from the
left recurrent vagus vein, where the latter
hooks beneath the ductus arteriosus. In
man, as in the pig, the left bronchid vein
uses the recurrent vein tap to drain into
the cardinal system. In man, however,
the left cardinal system is broken into a
lower fragment which becomes the coronary sinus, and an upper remnant that
connects the accessory hemiazygos to the
left innominate. Through the upper remnant the left bronchial vein enters the accessory hemiazygos.
The sight bronchial vein of man is
somewhat irregular. The human right recurrent vagus vein is too high up in the
chest to serve as an origin for a bronchial
vein. Some lower cardinal taps or other
adventitious veins drain the bronchi into
the arch of the azygos. The right bronchial vein resembles the renal veins, which
are also formed in a haphazard fashion
from 16cal adventitious vessels.
I add figure 10, a reconstruction of a
50-mm abnormal human embryo, because
it confirms the preceding embryo and suggests some normal variations of the bronchial vessels. This 50-mm embryo has a
blind coronary sinus, which drains backward into a persisting left common car-
plexus by a bronchial vein. The development of the bronchial veins enables one
to explain some of the aberrant pulmonary venous patterns.
According to 4 recent studies (Healey,
’52; Parson et al., ‘52; Keith et al., ’54;
and Darling et al., ’57) total bilateral abnormal pulmonary drainage is more often
diverted into a persisting left superior
vena cava and the coronary sinus. Partial
anomalous drainage, on the other hand,
is found more commonly on the right side.
Now the left bronchial vein is established
quite early and is preserved intact. It is
in an ideal position to capture the entire
Zuckerhandl (1884) long ago demon- pulmonary plexus. The right bronchial
strated the surprising number of routes vein is a more haphazard vessel, and
by which blood may be returned from the would be unable to capture more than
lungs and bronchi in the adult. From the the adjacent parts of the pulmonary
standpoint of the embryo these can be plexus.
summarized by a diagram (fig. 11). The
According to Hickie et al. (‘56): “Anomproblem set is the drainage of a plexus alous veins from the right lung often occovering the bronchi and lungs. The cur without associated anomalous veins
plexus around the lungs proliferates enor- from the left lung, but the reverse is unmously; it is drained by the pulmonary usual and left-sided anomalous pulmonary
vein into the left atrium. The early pul- veins generally occur with complete transmonary vein is for a time connected by position of all pulmonary veins and an
an esophageal tap with the gastric plexus atrial septal defect.” Such graver disorders
and through it with the liver. The lesser must begin early in embryonic life and
plexus around the bronchi, on the other would be more likely to involve the early
hand, are drained by more circuitous well established left bronchial vein.
routes made up of the venae comitantes
There is in addition another kind of
of the vagus nerves, the taps from the anomalous drainage of the pulmonary
cardinal veins, and the body veins.
veins which does not involve the bronchial
The pattern of the left bronchial vein vessels. About a dozen cases are known
is laid down early and is preserved. It where the lungs drain through a vein that
begins with a leash of vessels from the descends through the esophageal hiatus
left recurrent vagus vein, which uses that of the diaphram, follows the left vagus
vein and its cardinal tap to enter the left nerve and lesser curvature of the stomach
common cardinal vein. When the cardi- and ends in the ductus venosus or portal
nal system breaks up, the left bronchial vein. Details of this anomaly are often
enters the accessory hemiazygos, or the vague, but the accounts of Druepple (’57),
left innominate. Should the left common Edwards and DuShane (’50) and Butler
cardinal be preserved as a left superior (’52b) are explicit enough. Such an abvena cava, the left bronchial drains into dominal pulmonary vein is a combination
the coronary sinus. The right bronchial of several normal embryonic vessels shown
vein uses some of the lower cardinal taps in figure 11. The first part is a persisting
to enter the azygos vein. The right bron- early common pulmonary vein. The secchial vein is more haphazard in its consti- ond part is its esophageal branch. The
tution and course.
third part is a fragment of the left vagus
vein and the gastric plexus. The outlet is
Anomalous drainage o f t h e lungs
a communication of the gastric plexus
It has long been thought that many ab- with the ductus venosus. This outlet is
normal pulmonary veins are the result of near the outlet of the portal and may shift
a capture of all or parts of the pulmonary to it.
dinal vein. A retroesophageal right subclavian artery is also present.
The bronchial veins of both sides run as
in the previous embryo. But, where the left
bronchial ends, the common cardinal is
degenerating into a swamp. The left bronchial vein could end in the hemiazygos,
or move upward to the left innominatea common variation. Or it could empty
downward into a persisting left superior
vena cava and the coronary sinus. The
right bronchial vein again shows its haphazard origin from adventitious vessels.
The ending of all pulmonary veins in
the coronary sinus, without the mediation
of a persisting left superior vena cava,
has caused much discussion. In the well
known case of Brody ('42) 4 separate
veins enter an enlarged coronary sinus.
The best explanation seems to be that of
Auer ('48). Auer found in very young
human embryos a second pulmonary vein
orifice just caudal to the standard one.
The second vein enters the area of the
future coronary sinus. He thought the
second tap might supplant the usual one
and lead the pulmonary veins into the
coronary sinus.
I have seen Auer's accessory pulmonary
outlet in a 4.7-mm human embryo; it is
apparently a constant vessel. What seems
to be a later stage of the same vessel
turned up in an 18-rnrn pig embryo with
an abnormal heart. A section through this
heart (fig. 12) shows the early common
Fig. 10 Graphic reconstruction of the veins of an abnormal 50-mm human embryo,
with occluded coronary sinus and retroesophageal left subclavian artery. x 12.
Fig. 11 Schema of the venous drainage of the bronchi and lungs in the human embryo.
Fig. 12 Section from an abnormal 18-mm pig embryo heart. Pulmonary vein is transferred from its normal inlet to an accessory one into the coronary sinus. x 12.
Fig. 13 Section from an abnormal 23-mm pig embryo heart. Pulmonary vein opens into
right atrium. x 12.
pulmonary vein bypassing its normal outlet to enter the adjacent coronary sinus.
With the subsequent absorption of the
common stem, the 4 separate veins could
enter the coronary sinus.
The diversion of all the pulmonary veins
into the right atrium is a more complex
affair, involving heart anomalies. The
early common pulmonary vein enters the
common atrium just above the atrio-ventricular canal. When the atrial septum I
descends, it just grazes the right side of
the pulmonary o s c e (Davies and MacConaill, '37). It would seem a matter of
chance into which atrium the vessel would
go. In the rare case of Graham ('44) in
which a common pulmonary vein enters
the right atrium, the vein must have been
diverted into the right atrium by a slight
shift of the pulmonary orifice or of the
descending atrial septum I. Figure 13 is
a section through the heart of a 23-mm
abnormal pig embryo that duplicates Graham's anomaly. The common pulmonary
vein enters the right atrium about 6 sections above the free edge of atrial septum I.
The normal development of the pulmonary and bronchial veins is followed by
means of injected pig embryos and corresponding stages of human ones. The early
pulmonary vein has a constant esophageal
branch which communicates through the
gastric plexus with the ductus venosus.
The bronchial veins are derived from the
venae comitantes of the vagus nerves and
their cardinal vein taps. The left vein is
a constant derivative of the left recurrent
vagus vein. The right bronchial is a more
haphazard branch of some other cardinal
vein tap.
The normal findings are used to explain the nature and frequency of abnormal forms of pulmonary drainage, some
of which are also illustrated by abnormal
embryonic cases.
This paper is a report of work done
while the author held a Research Fellowship of the National Heart Foundation of
Canada. The cost of technical assistance
was met by the Alberta Heart Foundation.
For material the author is indebted to
Swift Canadian Company. To all the
author gives his thanks.
Auer, J. 1948 The development of the human
pulmonary vein and its major variations. Anat.
Rec., 101: 581-584.
Brody, H. 1942 Drainage of the pulmonary
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Brown, A. J. 1913 The development of the
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Butler, H. 1950 The development of the azygos
veins in the albino rat. J. Anat., 84: 83-94.
1952a Some derivatives of the foregut
venous plexus of the albino rat, with reference
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1952b An abnormal disposition of the
pulmonary veins. Thorax, 7: 249-254.
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the right side of the heart: report of 17 autopsied cases not associated with other major
cardiovascular anomalies, Lab. Invest., 6: 4464.
Davies, F., and M. A. MacConaill 1937 Cor
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Druepple, L. G. 1957 Complete pulmonary venous drainage into the portal vein with multiple congenital anomalies. Am. Heart J., 53:
Edwards, J. E., and J. W. DuShane 1950 Thoracic venous anomalies. Arch. Path., 49: 517537.
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C. P. Bailey 1957 Partial anomalous venous
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Hickie, J. B., T. M. D. Gimlette and A. P. Bacon
1956 Anomalous pulmonary venous drainage.
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Keith, J. D., R. D. Rowe, P. Vlad and J. H.
O'Hanley 1954 Complete anomalous p b o nary drainage. Am. J. Med., 16: 23-38.
Parsons, H. G., A. Purdy and B. Jessup 1952
Anomalies of the pulmonary veins and their
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Reagan, F. P. 1919 On the later development
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Zuckerhandl, E. 1884 Vber die Anastomosen
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