Download Direct Measurement of Bronchial Arterial Flow

Direct Measurement of Bronchial Arterial Flow
By BRUNO HORISBERGER, M.D.,
AND SIMON EODBARD, M.D.,
T
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in 30 dogs, found that the bronchial arteries
arise in all cases from the first to the fourth
right aortic intercostal arteries.
Miller13 showed that the bronchial arteries
supply the airways as far as the respiratory
bronchioles. Branches to the subpleural capillary network on the surface of the lung, to
the vasa vasoruin of the larger pulmonary
vessels, and to the mediastinal structures were
also demonstrated.
A curiosity of the true bronchial circulation is the fact that it has no veins of its
own. Liebow and his group14 studied the
venous drainage of the bronchial vascular
bed and pointed out that the intrapulmonary
drainage is via the pulmonary veins to the
left heart. The extrapulmonaiy part of the
bronchial vascular bed drains mainly via the
azygos vein and the superior vena eava into
the right heart. The "bronchial" arteries,
therefore, represent a vascular system which
supplies numerous mediastinal structures in
addition to the bronchial tree.
Many attempts utilizing both indirect and
direct methods have been made to measure
tlie flow through this system. Indirect measurements were made after ligation of the
pulmonary artery to one lung in dogs
(Bloomer, Harrison, Lindskog, and Liebow,"'
and Vidoue and Liebow15). The collateral flow
participating iu gas exchange ("effective"
flow) was computed by bronchospirometry
together with the Fick principle and was
found to be about 300 ml./min./M.2 of body
surface. Since the method cited appraises
only the part of the bronchial flow which
participates in gas exchange, the values reported are surprisingly high.
The Fick principle has been used to ineassure the "effective" pulmonary collateral
blood flow in man (Fishman et al. 8 ). In longstanding intrinsic lung disease with increased
pulmonary vascular resistance, the effective
collateral flow is known to be increased, but
even so it is less than 10 per cent of the
HE normal bronchial arterial blood flow
provides only a very small portion of
the blood flow through the lungs.1' 2 Since it
supplies oxygen and nutrients to the bronchial
musculature and mucosa, it may have importance for pulmonary mechanisms far beyond
that expected on the basis of its small flow.
After giving up its oxygen on passage through
the pulmonary parenchyma, this flow passes
into the pulmonary system where it may contribute oxygen-depleted blood to the pulmonary venous outflow. Precapillary anastomoses probably play a minimal role under
normal circumstances.3'4 Because of the great
potential for proliferation of the bronchial
vascular system in congenital anomalies and
inflammatory conditions, and after experimental obstruction of the pulmonary artery,5' ° the flow through this system may
also have relevance in the evaluation of circulatory mechanisms.
The normal anatomy of the nutrient arteries supplying the parenchyma of the lung
was studied long ago by Leonardo da Vinci,7
von Haller,8 and Kiittner.9 The great variability in the topographical origin was early
recognized. Cockett and Vass10 have reviewed
the pertinent literature.
Kiittner9 demonstrated that dye injections
into the aorta resulted in the staining of the
bronchial mucosa in man; he described the
posterior bronchial arteries in the dog and
showed that the branches to the right and
left lung often had a common trunk with a
medial intercostal artery, emerging from the
aorta at the sixth thoracic segment. Berry et
al.11 confirmed the arrangement desci'ibed by
Kiittner. Notkovich,12 in an extensive study
From the University of Buffalo Chronic Disease
Research Institute, Buffalo, N. T. Dr. Horisberger's
present address: University of Zurich, Switzerland.
Supported in part by the Now York State Department of Health and by Grant H-2271 (C3) from the
National Heart Institute of the U. S. Public Health
Service.
Received for publication May 12, 1960.
Circulation Research, Volume VIII, November 19t>0
PH.D.
1149
1150
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cardiac output. The collateral flow approaches
normal cardiac output values only in cases
of congenital absence of the pulmonary
artery.
The bronchial artery flow in dogs was measured directly by Bruner and Schmidt16 who
supplied femoral arterial blood to a cannula
in the origin of the right bronchial artery at
the fifth intercostal space. A bubble flowmeter
showed a range of delivery of 0.6 to 27 ml./
min. with an average of 4 ml./min. Labeled
erythrocytes showed that the right lung rereived two-thirds of the bronchial arterial
blood while the remainder supplied the mediastinum. Stimulation of the vagus increased
flow to the bronchial vascular bed, while sympathetic stimulation reduced the flow.
"Williams and Towbin17 ligated the pulmonary artery and then estimated bronchial flow
as the backflow from the cut distal segment of
the vessel. They found this to be 4 to 9 ml./
min. More recently, State et al.1 and Cudkowicz et al.2 measured the left and right heart
output simultaneously in dogs and calculated
the difference, i.e., the collateral flow, to be
approximately 1 per cent of the total cardiac
output.
To obtain further insights into the regulation of the bronchial arterial circulation, we
have developed a method which registers flow
continuously in dogs. This technic permits
direct and continuous measurement of the
changes due to experimental procedures or
to the administration of drugs.
Methods
It is difficult to isolate the true bronchial arteries
from their widespread anastomoses with the
mediastinal and pericardial vessels. However, a
technic was developed in the course of the preliminary studies in a series of 12 dogs by means
of which the extrabronehial fraction of flow could
be minimized. This teehnic has since been used
with only slight variations in more than 20 experiments.
Ten dogs were anesthetized with intravenous
injection of pentobarbital sodium (about 30 mg./
Kg.). A large cannula was tied into the trachea
through a low incision. The cervical vagus nerves
were isolated. To abolish spontaneous respiratory
movements, a continuous infusion of diacetylcholine chloride (succinyleholine) (0.16 mg. in
HORISBERGER, RODBARD
2 ml. saline/min.) was administered intravenously.
Intermittent positive pressure breathing was maintained at a selected insufflation pressure, using
a Burns valve.18
After a left thoracotomy, the sixth rib was resected. The first 5 lateral and the first medial
intercostal arteries were then ligated at the aorta.
The descending aorta was retracted venkally and
the second, third, and fourth medial intercostal
arteries were then isolated. The posterior bronchial
arteries usually originated at the second and third
medial intercostal arteries at the fifth right intercostal space. Occasionally, the bronchial artery for
the left lung originated directly from the aorta.
After the bronchial vessels were isolated, the remaining medial intercostal arteries down to the
fifth branch were ligated. The esophageal branches
were ligated.
The segment of the aorta from the second to
the fourth intercostal artery, which contained the
vessels to the pleura, mediastinum, and bronchial
tree, i.e., the bronchial vessels, was then isolated
to produce a small vascular sac. The gap in the
descending aorta was bypassed by means of a
T-tube. One arm of the T-tube was connected to
a rotameter (Fisher and Porter Co., No. O2.F1/
8-20-5/36) and then to the isolated aortic segment
(%• 1).
Plastic cannulas, 1 mm. in diameter, were tied
into the pulmonary artery and into a left pulmonary vein. Simultaneous pressure recordings
taken from these vessels as well as from the
tracheal tubes were traced on a Sanborn direct
writing apparatus.
The bronchial vascular resistance (R) was
calculated as the pressure drop (AP) in mm. Hg
from aorta to pulmonary vein, divided by the
quantity (Q) of flow in ml. blood per minute
so that
AP
R =
Q
At the end of each experiment, 15
0.1 per cent solution of "fast green"
injected into the aortic sac to visualize
lar communications and the tissues it
ml. of a
dye were
its vascusupplied.
Results
Characteristics of Flowmeter and Preparation
The flowmeter (capacity 0 to 60 ml./min.)
had a curvilinear characteristic for flows less
than 5 ml./min., and was quite linear in the
5 to 60 ml. range. The pressure drop across
the flowmeter between the aorta and the bronchial arterial system was less than 5 mm. Hg
and the phase of the pulse pressure curve
was practically unchanged (fig. 2). The perfusion pressure and phase relationships for
Circulation Research, Volume VIII, November 1960
BEONCHIAL ARTERIAL FLOW
1151
Cm Hf
Ai
AORTA
M00
UGATED
NTERCOSTAL
30
20
A
SEGMENT
OF AORTA
PA
10
S0C
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Figure 1
Essentials of the preparation. Respiratory gases
were supplied from commercial cylinders to a series of reduction valves (upper left) which lowered
the insufflation pressure to a selected value, usually 20 cm. water. The gas then passed through a
Burns valve to the trachea. The bronchial blood
supply is shown at the right. Aortic blood passes
through a flowmeter to the isolated aortic segment
from which the branches to the bronchial arteries
originate. The crossmarks on the lines to the esophagus and intercostals indicate that these vessels
have been ligated. The "bronchial" arteries supply
the bronchial tree and both lungs, as well as the
mediastinum.
the bronchial arterial system were therefore
practically identical with the central aortic
pressure. This could be achieved because the
orifices of the bronchial arteries were not
cannulated and no significant additional resistance was introduced by our preparation.
Flow Measurements
Initial Reduction
Blood flow measurements were recorded at
intervals of 10 to 30 seconds. The bronchial
blood flow was highest immediately after it
had been interrupted for several minutes during the preparation of the aortic sac and
the connection of the fiowmeter, and then
fell to a constant level within the course of
a few minutes (fig. 3).
Spontaneous Variations
Small spontaneous variations in bronchial
artery flow were sometimes seen in our experiments. One of our dogs showed larger variation for a prolonged period of time, but these
Circulation Research, Volume VIII, November 1960
Figure 2
Pressure contour and phase relationship of the
pulse loave in the Aorta (A,) aiid in the sac (At)
were not altered by the intervention of the flowmeter, and the pressure drop xuas negligible. Calibration marking are in mm. Hg; PA refers to
the pressure in the pulmonary artery.
were synchronous with marked fluctuations in
systemic blood pressure due to arrhythmias.
Effects of Air Pressure
An increase from 20 to 30 cm. water insufflation pressure was associated with an increase in the calculated bronchial vascular
resistance in 4 dogs (fig. 3). This was indicated by a fall in flow; a decrease in insufflation pressure to 20 cm. water was then accompanied by a return of the blood flow to
previous values. Further lowering of the insufflation air pressure did not produce a
further decrease in bronchial vascular resistance in our preparations.
Vagotomy
After the bronchial flow was stable for at
least 5 minutes, the previously isolated vagi
were cut bilaterally in dogs 4 to 8. The calculated bronchial vascular resistance increased
within a few seconds in all 5 animals, and
then persisted at the higher values (table 1).
l-epinephrine
When the systemic pressure increased after
intravenous injection of Z-epinephrine, the
flow through the bronchial vascular system increased proportionate!y. Injections of Z-epinephrine into the bronchial artery via the
1152
HORISBERGER, RODBARD
Table 1
Effect of Bilateral Vagotomy on Bronchial Vascular Resistance
Before vagotomy
After vagotomy
Resist.
PVP
Dog
4
5
G
7
8
Aortic BP
mm. Hg mm. Hg
135
120
125
80
100
Flow
ml./min.
4
8
6
9.0
25.3
4.0
O
3.0
35.0
s
PVP
Flowmm. Hg Aortic BP
mm. Hg mm. Hg mi./min.
ml./min.
14.6
4.4
29.8
26.0
2.6
200
135
130
90
100
7
9
6
10.0
15.5
3.0
3.0
30.5
O
8
Resist.
mm. Hg
ml./min.
19.3
8.1
41.3
29.3
3.0
Change in
vascular
resistance
(%)
+ 32.
+S4.
+39.
+13.
+12.
BP = Blood pressure.
PVP = Pulmonary venous pressure.
BP-PVP = Pressure gradient (BP) across the pulmonary vascular system.
Resistance is calculated as /\P/flo\v.
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Table 2
Effect of Serotonin on Bronchial Vasiular Resistance
Dog
4 (vagotomized)
"i (vagotomized)
S
9
10
Paor.
150
160
130
135
100
90
90
105
110
Flow before serotonin
Q
*Vv
7
G
S
9
3
O
9
9
9.0
10.0
14.5
13.5
3.0
3.0
3.0
4.0
4.5
Peak flow
R
15.8
15.4
8.4
9.3
32.3
29.3
29.3
25.8
24.0
p
* aor.
P,.,
Q
R
AR%
150
160
120
120
95
90
90
100
105
7
6
13.0
12.0
29.0
24.0
5.5
4.0
3.5
5.5
8.S
11.0
12.8
3.9
4.7
16.7
22.0
25.1
17.8
11.7
-30
—17
—54
—50
-48
—25
—14
—31
—51
-36*
8
S
3
o
o
o
2
*Jloati change in vascular resistance.
P.or. = Aortic pressure in mm. Hg.
Pi.v = Pulmonary vein pressure in mm. Hg.
Q = Bronchial arterial flow in ml./min.
Resistance (R) is calculated as P n o r .—PIT/Q.
/ \ B is the change in resistance.
sac system sharply decreased the bronchial
flow. Since the systemic blood pressure was
unaffected in the latter case, it must be concluded that a marked increase in bronchial
vascular resistance was induced (fig. 4).
Serotonin
Responses of the bronchial vascular resistance to serotonin (5-hydroxytryptamine) in
doses of 1 ^g./Kg. into the bronchial artery
were compared with the responses to injection of 5 ,u,g./Kg. into the pulmonary artery
or vein (table 2).
Bronchial Arterial, Injection. The systemic
pressure remained unchanged after the injection of 1 /xg. of serotonin into the bronchial
arterial system. The bronchial vascular resistance first showed a transitory increase
followed in about 30 seconds by a decrease
in resistance which persisted for approximately 2 minutes (fig. 5).
Pulmonary Artery or Vein. The administration of 5 /xg./Kg. of serotonin into the
pulmonary artery in 5 trials and .10 injections into the pulmonary veins resulted in a
decrease in bronchial vascular resistance
within about 10 seconds and reached a maximum in about 30 seconds and then returned
to control values in about 2 minutes.
The difference in response after injections
into the bronehial artery and into the pulCirculation Research, Volume VIII, November 1960
BRONCHIAL ARTERIAL FLOW
monary artery or vein are significant (p
< 0.05, as calculated with the t test).
1153
FLOW
Anatomic Control
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At the end of each experiment, the injection of 15 ml. of an 0.1 per cent solution of
"fast green" dye into the aortic sac was used
to demonstrate the vessels and tissues supplied by the bronchial artery. In the majority
of the preparations, the bronchial vessels in
both lungs were clearly outlined and the
bronchial mucosa showed fair to very good
staining. The bronchial arteries could be
traced to the dorsal region of the bifurcation
of the trachea. An annular vascular distribution of the dye could be seen between the
tracheal rings for an inch or so of the
trachea above the bifurcation. The major
supply passed along the bronchi to the intrapulmonary tissues. The branches of the bronchial tree were clearly delineated. The va.sa
vasorum of the pulmonary veins near the
left atrium and of the pulmonary arteries
near the heart were also filled. The connective tissue layer around the vagi was green
in all preparations. With one exception, the
pericardial vessels were also filled in all the
cases where the dye had entered the bronchial
vascular system. The wall of the esophagus
was stained near the origin of the bronchial
vessels around the aortic sac, despite the fact
that all visible esophageal vessels had been
li gated. Most of the cases also showed a
slight filling of the right intercostal artery
in the fourth or fifth interspace.
The data of 2 preparations were not included in the present series because the
bronchial vessels remained unstained.
Discussion
With the present preparation (fig. 1), the
bronchial vascular resistance and blood flow
can be studied in dogs under nearly normal
hemodynamic conditions (fig. 2). The normal
relations between the blood pressures and
flows in the pulmonary and bronchial vascular systems are maintained. The preparation
differs from normal in that the lungs are
insufflated with positive pressure. The exact
role of this factor has not yet been evaluated.
Circulation Research, Volume VIII, November i960
20
10
0
MINUTES2
4
*
*
9
Figure 3
Bronchial blood flow immediately after connection
of flowmeter between aorta and vascular sac. The
vertical width of the bar represents the oscillations
of the float of the rotametcr. Prior to the establishment of the connection, the bronchial arterial
flow had been disconnected for several minutes.
The low resistance at this time is a characteristic
response to the transitory occlusion, as in other
vascular beds. After stabilization at S minutes, the
insufflation pressure (1PPB) was raised from 20
to 30 cm. neater; this was accompanied by a fail
in bronchial blood flow and a marked rise in bronchial vascular resistance.
However, lowering of the insufflation pressure from 20 to 10 cm. water had no effect
on the bronchial vascular resistance or blood
flow. Since we used an insufflation pressure
of 20 em. water for all of our studies, we
assume that the bronchial vascular system was
not significally affected by the use of our
ventilatory device.
The bronchial vascular resistance increased
when the insufflation pressure was raised
from 20 to 30 cm. water (fig. 3). It would
thus appear that high intrapulmonary air
pressures can affect the bronchial vessels,
or perhaps the effect is by collapse of the
pulmonary capillary bed into which some
of the bronchial arterial flow passes.
It would appear that the communication
between the vascular beds of the bronchial
and pulmonary arterial systems is not completely open for flow in both directions. This
is suggested by the fact that a transitory
HORISBERGER, RODBARD
1154
INJECTION INTO PA.(») OR PV.(e)
£
mL/mln.
30 T
I-OT
•
1
O 0.8-•
UJ
"0.620
HI
ADRENALIN INTO
BRONCHIAL ART.
INJECTION INTO BRONCHIAL ART.
10
1.0-
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uo.e
o
8 0.61
ml/min.
30TS
CONTROL 10 20 30 SECONDS 60
Figure 5
VASC.
RESIST.
T2
20
-I
ESIST.
ADRENALIN
INTO
THORACIC
. AORTA
10
-I
,
0 MINUTES I
2
3
Figure 4
(Above) Effect of adrenalin (l-epinephrine) on
bronchial arterial blood flow (shaded area) and
'bronchial vascular resistance. After administration
at 0- minutes, the resistance increased sharply at
first; this was folloxoed by a transitory increase
in flow as the resistance returned to normal. (Below) A reduction in calculated bronchial vascular
resistance occurred on administration of adrenalin
into the thoracic aorta as the systemic blood pressure increased; this ivas follotoed by a return to
control values. Discussed in text.
obstruction of the bronchial artery is followed by an increased flow. This may be interpreted as a reactive reduction in bronchial
vascular resistance (hyperemia), a phenomenon which follows obstruction of the blood
flow to tissues supplied by end-arteries. It is
presumed that the accumulation of metabolic
end-products generates a localized bronchial
90
Effect of serotonin. Changes from the normal
calculated bronchial vascular resistance are indicated by the vertical axis. After injection into the
bronchial artery (lower set of data), the resistance
increased for about 15 seconds and then fell to
normal or less than normal values. Injection into
the pulmonary artery or vein produced a fall in
bronchial vascular resistance which ivas maximal
about 30 seconds after administration; the resistance values then returned to normal.
arteriolar vasodilatation. The occurrence of
such a vasodilatation may be interpreted as
indicating that the blood passing through the
pulmonary circulation does not eliminate these
materials and the "reactive hyperemia."
Since a portion of the bronchial arterial
distribution is extrapulmonary, this part of
the circulation obviously could not benefit
by the intrapulmonary circulation, and part
of the reactive hyperemia following release
of occlusion of the bronchial vessels may be
accounted for by vasodilatation in this extrapulmonary portion. An increase in insufflation air pressure would be expected to affect
only the intrapulmonary portion of the bronchial vascular bed and not compress the
extrapulmonary, mediastinal part in the open
chest animal. Since the increase in airway
pressure to 30 cm. water resulted in a substantial increase in bronchial vascular resistance (fig. 3), we can conclude that the intraCirculation Research, Volume VIII, November 1900
BEONCHIAL ARTERIAL PLOW
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pulmonary bronchial flow is responsible in
a considerable part for these results. However, the injection of dye at the end of each
experiment demonstrated a marked staining
of the bronchial structures while only a small
amount of the dye stained the extrapulmonary
tissues in the mediastinum. Therefore, the
flow to the mediastinal tissues probably accounts for only a small portion of the bronehial arterial flow.
The effects seen after vagotomy (table 2)
or after injection of Z-epinephrine directly
into the bronchial artery (fig. 4) support the
observations of Brunei- and Schmidt16 that
the adrenergic fibers are vasoconstrictors to
the bronehial vascular bed.
One of the advantages of the present preparation is that it is possible to test the effect
of drugs on the bronchial vascular system
without interference with the systemic effects
of these agents. This was demonstrated by a
comparison of the effects of systemic injection
of Z-epinephrine with those after injection
into the bronchial vascular system (fig. 4).
An immediate bronchial vasoconstrietion,
shown by a reduction in flow, follows direct
injection into the bronchial vascular system.
After systemic injection of Z-epinephrine, the
vasoconstrictor effects on the bronchial arterial system are delayed in accord with the
time required for transit of the agent through
the bypass and the flowmeter. It is of interest
that an increased flow through the bronchial
arterial system results prior to the arrival
of the agent in the bronchial system. The
slight decrease in calculated bronehial vascular resistance may be accounted for by a
passive distention of the bronchial arteries
and arterioles by the increased transmural
pressure or by a reflex dilatation.
Serotonin is considered to be a potent constrictor of the pulmonary vascular system.19
However, State et al.1 indicated an increase
in collateral flow to the lungs after injection
of large doses (1 to 10 mg.) of serotonin into
the pulmonary artery. Some of this effect
in their preparation may have reflected the
considerable and prolonged coronary vasodilatation demonstrated by Maxwell et al.20 after
Circulation Research, Volume VIII, November 1980
1155
the injection of serotonin in amounts of 20
/xg./Kg./min. It was, therefore, of interest
to test the effect of serotonin in the bronchial
artery; after injection of 1 /xg./Kg., a transient increase in resistance was followed by
a decrease in resistance (table 2). Since'these
small doses of serotonin did not significantly
affect either the systemic or the pulmonary,
arterial pressures, the demonstrated increase
in bronchial flow can be explained only by
vasodilatation of the bronchial arteries and
arterioles. The response after injection into
the pulmonary artery or vein shows that the
bronchial vascular resistance fell sharply after
a lag of about 10 seconds. Other data suggest
that this effect may be a response to changes
in pulmonary vascular resistance.
Summary
A method is described for the measurement
of the collateral pulmonary blood flow in the
thoracotomized dog by utilization of a flowmeter which measures flow into an aortic sac
from which the bronehial arteries arise. This
preparation maintains the normal perfusing
pressures and diminishes phase changes in
the-arterial pulse waves. The bronchial vascular'resistance is increased by an increase
in the insufflation air pressure, by bilateral
vasrotomy, or by the administration of lepinephrine into the bronchial arterial circulation. The bronchial vascular • resistance
was decreased after a tratisitory interruption
of the bronchial arterial blood flow (reactive
hyperemia). After administration of serotonin
in the bronchial artery, a transient increase
in resistance was followed by a marked decrease. Intrapulmonary vascular injections
produced on"y a decrease in resistance. The
present data demonstrate the sensitivity of
the preparation described.
Summario in Interlingua
Es deseribite un methodo pro le mesuration del
collateral fluxo de sanguine pulmonar in le thoracotomisate can per medio de un fluxometro que mesura le
fluxo entrante in un sacco aortic in le qual le arteriaa
bronchial prende lor origine. Iste preparato mantene
le normal pression de perfusion e reduce le alterationes
de phase in le undas de pulso arterial. Le resistentia
bronchio-vascular es augmentate per un augmento ia
HORISBERGER, RODBARD
1156
le prcssion del aere insufflate, per vagotomia bilateral,
o per le administration de (-epinephrina a in le circulation bronchio-arterial. Le resistentia broncho-vascular esseva reducitc post un interruption transiente del
fluxo de sanguine bronchio-arterial (hyperemia reactive). Post le administration de serotonina a in le
arteria bronchial, un transiente augmento del resistentia esseva scquite per un reduction de marcate
magnitudes. Tnjeetiones vascular intrapulinonar produceva solmeiite un reduction del resistentia. Le
presento dittos demonstra le sensibilitate del prepanito describite.
Eeferences
1. STATE, D., SALISBURT,
P. F., AND WEIL,
P.:
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Physiologic and pharmacologic studies of collateral pulmonary flow. J. Thoracic Surg. 14:
599, 1957.
8. VON HALLER, A.: Icones anatom. fasc. I l l , p.
35-37, and Tab. art. bronchialis. Gottingen,
1756 (cf. reference 9).
9. KUTTNER: Beitrag zur Kenntniss der Kreislaufverhaltnisse der Saugethierlunge. Arch. path.
Anat. 73: 476, 1878.
10.
circulation to the lungs. Brit. J. Surg. 38:
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11. BERRY, J. L., BRAILSFORD, F. J., AND DALY, I.
DEB.: Bronchial vascular system in the dog.
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12. NOTKOVICH, H.: Anatomy of the bronchial arteries
of the dog. J. Thoracic Surg. 33: 242, 1957.
13. MILLER, W. S.: The Lung. Springfield, III.,
Charles C Thomas, 1937.
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2. CUDKOWICZ, L., CALABBESI, M., NIMS, R. G., AND
GRAY, F. D.: Simultaneous estimation of right
and left ventricular outputs applied to a study
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J. 58: 732, 1959.
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16. BRUNER, H. D., AND SCHMIDT, C. F . : Blood flow
in the bronchial artery of the anesthetized
dog. Am. J. Physiol. 148: 648, 1947.
17. WILLIAMS,
(). FlSHMAN, A . P . , TURINO, G. M., BRANDFONBRENER,
M., AND HIMMELSTEIN, A.: "Effective" pul-
monary collateral blood flow in man. J. Clin.
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Editors: Leonardo da Vinci on the Human
Body: Anatomical Physiological, and Embryological Drawings of Leonardo da Vinci, with
Translations, Emendations, and Biographical
Introduction. New York, Henry Schuman, 1952,
p. 394.
M. H., JR., AND TOWBIN,
E.
J.:
Magnitude and time of development of the
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5. BLOOMER, W. E., HARRISON, W., LINDSKOO, G. E.,
AND LIEBOW, A. A.: Respiratory function and
blood flow in the bronchial artery after ligation of the pulmonary artery. Am. J. Physiol.
157: 317, 1949.
VIDONE, R. A., AND LIEHOW, A. A.: Anatomical
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great vessels. Am. J. Path. 33: 539, 1957.
of the relation of pulmonary and bronchial
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Circulation Research, Volume VIII. November I960
Direct Measurement of Bronchial Arterial Flow
BRUNO HORISBERGER and SIMON RODBARD
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Circ Res. 1960;8:1149-1156
doi: 10.1161/01.RES.8.6.1149
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