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Three-dimensional structure of the bronchial microcirculation in sheep.

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THE ANATOMICAL RECORD 243:357-366 (1995)
Three-Dimensional Structure of the Bronchial
Microcirculation in Sheep
DEAN E. SCHRAUFNAGEL, DAVID B. PEARSE, WAYNE A. MITZNER, AND
ELIZABETH M. WAGNER
Departments of Medicine and Physiology, The Johns Hopkins Medical Institutions,
Baltimore, Maryland (D.P., W.M.,E.M.); Departments of Medicine and Pathology,
University of Illinois at Chicago, Chicago, Illinois (D.S.)
ABSTRACT
BACKGROUND: The bronchial circulation affects both
pulmonary vascular and airway activity. Fundamental to understanding
the role of the bronchial microcirculation in health and disease is understanding its anatomy. This study sought to identify specific structural elements that might contribute to the drop that occurs between the systemic
blood pressure of the bronchial artery and the low pressure of the pulmonary bed into which the bronchial circulation flows and to better describe
the connections of the bronchial and pulmonary circulations. METHODS:
To do this, the lungs of five sheep were cast by injecting a resin through
bronchial and pulmonary arteries. After taking samples for light microscopy, the tissue was digested and the casts were viewed with a scanning
electron microscope. RESULTS: Casts of extrapulmonary bronchial arteries were structurally similar to other systemic arteries. Tortuous ones spiraled around bronchi and large blood vessels. Intrapulmonary bronchial
arteries, about 100300 pm in diameter, had sharp branching and deep
focal constrictions with great rugosity that completely shut off the flow of
the resin. These vessels correspond to the Sperrurterien described by von
Hayek (and could cause the resistance associated with the pressure drop).
Vasa vasorum ran in the walls of intrapulmonary pulmonary arteries for a
variable distance before they entered the lumens of the pulmonary arteries.
The smallest blood vessel found that was supplied with vasa vasorum was
a bronchial artery 42 pm in diameter. Capillary-like networks with large
luminal diameters were found on the pleural surface. CONCLUSIONS:
Scanning electron microscopy of microvascular casts provides a fresh description of the bronchial circulation, further delineates the communications of these two circulations, and may structurally account for some pressure drop between the bronchial and pulmonary circulations.
0 1995 Wiley-Liss, Inc.
Key words: Bronchial circulation, Corrosion casting, Pulmonary artery,
Pulmonary circulation,Microscopy, scanning, electron, Sheep
Fundamental to understanding the role of the bronchial microcirculation in health and disease is understanding its anatomy. Although the anatomy has been
studied for centuries (Mitzner and Wagner, 1992), several specific structural questions that directly bear on
physiologic function have not been resolved. Bronchial
to pulmonary vascular connections have been ascribed
and denied (Von Hayek, 1960) a t the arterial (Kuttner,
1878), capillary, and venous levels (Miller, 1947) for
many years. Several investigators (Kuttner, 1878; Verloop, 1948; Marchand et al., 1950) found bronchial artery to pulmonary artery anastomoses, but others (Wagenvoort et al., 1964; Robertson, 1967)found them only
occasionally after the age of two in humans without
cardiac and pulmonary disease. Generally, the connections have been shown by injecting tracers and finding
0 1995 WILEY-LISS, INC.
the dye in the other circulation (Miller, 1947).Although
tracer studies show that anastomoses exist, the intersections of these two vascular systems have not been
well visualized. It is difficult to appreciate the threedimensional structure of this site with sectioning histologic techniques because large areas of fine vascular
detail are not readily visible. The bronchial circulation
is unique because it normally has a low flow but can
ReceGedFebruary 23, 1995; accepted July 5, 1995.
Address reprint requests to Dean Schraufnagel, M.D., Section of
Respiratory and Critical Care Medicine, Department of Medicine M/C
787, University of Illinois at Chicago, 840 S. Wood St. Chicago, IL
60612-7323.
D.E. SCHRAUFNAGEL ET AL.
358
Fig.1. The casts of extrapulmonary bronchial arteries were similar
to other systemic arteries. The straight bronchial artery (B) lies in the
connective tissue at the entrance to a lobe. Thick walls are inferred by
the void between the artery and adjacent capillaries (arrow). The
capillaries in the artery wall (vasa vasorum) and bronchial wall are
often lost in preparing the tissue and leave an empty space. Elongated
impressions (small arrow) produced by endothelial cell nuclei run
with the long axis of the artery. A small bronchial vein (V) leads away
from nonalveolar capillaries ( C ) . Only the bronchial artery was injected in this sheep. Bar = 100 km.
immediately increase its blood flow to prevent pulmonary infarction if the pulmonary artery is obstructed
(Virchow, 1847). Furthermore, it is at a much higher
pressure that the pulmonary circuit into which it
drains. It must, therefore, be equipped to brake its blood
flow and pressure. Studying vascular casts with the
scanning electron microscope has expanded our knowledge of many vascular beds (Aharinejad and Lametschwandtner, 1992; Motta et al., 1992; Schraufnagel,
1992). With this three-dimensional technique, we also
sought to identify specific structural components that
could contribute to the large pressure drop between the
systemic arterial pressure of the bronchial artery and
the low pressure pulmonary bed. We also sought to
document the types of bronchial-pulmonary connections that occur in sheep. We injected the bronchial and
pulmonary circulations in sheep and studied the microscopic pathways of the bronchial circulation with scanning electron microscopy.
oral artery was cannulated and the animal was given
10,000 U of heparin and exsanguinated. The thorax
was opened with an incision through the fifth intercostal space on the left side. The bronchoesophageal artery
was isolated and the esophageal and intrathoracic tracheal branches were ligated. The artery was then cannulated with a 16-gauge catheter (Wagner et al., 1987).
A midsternotomy was made to cannulate the pulmonary artery and left atrium. The pulmonary vasculature was flushed with 1.5 L of 3% dextran in normal
saline and the bronchial vasculature was flushed with
100 mL of the same solution. All lobes of the lung were
tied off except the right middle and lower lobes to allow
adequate filling without wasting methacrylate. Sixty
milliliters of partially polymerized methyl methacrylate (Mercox, Ladd Research Industries, Burlington,
VT) was mixed with the benzoyl peroxide accelerator
and delivered by a hand-held syringe over 1 minute for
both the pulmonary artery and bronchial artery infusions (Schraufnagel, 1992). Two animals were cast
through the bronchial artery only (animals 1 and 4);
two were cast through both the bronchial artery and
pulmonary artery (animals 2 and 3) with different colored resins; and one was cast through the pulmonary
artery only (animal 5). The hydrostatic pressure of a
left atrial outflow reservoir was maintained at 0-5
mm Hg. The airway pressure was set to 10 mm Hg for
MATERIALS AND METHODS
Five male sheep, weighing 31.9 kg (SD 1.7 kg), were
anesthetized initially with ketamine, 1 g intravenously, and subsequently maintained with pentobarbital sodium as needed. They were ventilated with a
Harvard Ventilator at a rate of 12-15 breaths per
minute with a tidal volume of 10-12 ml/kg. The fem-
BRONCHIAL CIRCULATION
Fig. 2. This bronchovascular space of a sheep with only its bronchial
circulation injected has a bronchial artery (B) about 300 pm in diameter, a bronchial artery (b) about 83 pm in diameter, and several
straight arterioles (arrow), about 12 p m in diameter. The smallest
359
arteries may run long distances without branching. The void space
between the two larger arteries (B and b) was occupied by a n airway.
Structures with characteristics of Sperrurterien arise from the largest
artery (B). Bar = 100 pm.
animals 1 and 2, to 3 mm Hg for animal 3, and atmo- monary veins do and pulmonary arteries often lie near
spheric pressure for animals 4 and 5.
airways. Large pulmonary arteries do not give rise to
After casting, the resin set for 1 hour before the capillaries but branch first into smaller (<lo0 pm) arlungs were removed and placed in water. They were teries. Capillaries are constant structures in caliber,
transferred to a sodium hydroxide solution that was branching frequency, and branching angle. Capillaries
changed regularly until corrosion was complete. The around alveoli, airways, and pleura each have a distinct
casts were studied grossly and with the dissecting mi- three-dimensional pattern, although the bronchial and
croscope and then cut with razor blades and scissors pleural patterns are similar (Ohtani, 1980; Guntheroth
into pieces about 1 mm thick. The pieces were fastened et al., 1982; Schraufnagel et al., 1986).The cast alveolar
to aluminum studs with double-sided tape, sputter- capillaries are arranged in basket-shaped structures
coated with palladium-gold, and reviewed with a JEOL that correspond to the alveoli. They have a central hole
JSM-35C scanning electron microscope at an acceler- and usually 5 radial spokes (Ohtani, 1980; Schraufnaating voltage of 15 kV.
gel et al., 1986).In rats about 91%ofthe alveolar surface
Arteries and veins were identified based on estab- contacts the vascular space in contrast to 73% of the
lished cast criteria previously described in the rat bronchial and 75%pleural surfaces (Schraufnagel et al.,
(Schraufnagel et al., 1994) and other species (Lame- 1995a). The branching frequency of alveolar capillaries
tschwandtner et al., 1990). Briefly, casts of both sys- is about 18 per 100 pm of length; of pleural capillaries,
temic and pulmonary veins have round impressions it is about 9 and, of bronchial capillaries, it is about 14
caused by the endothelial cell nuclei (Miodonski et al., (Schraufnagel et al., 1995a). No criterion has been re1976). Pulmonary veins have regular ring constrictions ported to distinguish bronchial and pulmonary, arterial
(Ohtani, 1980;Schraufnagel and Patel, 1990) and small and venous casts, probably because only a few ultrapulmonary veins do not course with the airways. Pul- structural casting studies have been carried out on the
monary veins usually have a narrow space between bronchial circulation (Magno and Fishman, 1982; Chatheir wall and adjacent capillaries. Casts of both sys- ran et al., 1984; Magno, 1990). Here, we identified the
temic and pulmonary arteries have oblong nuclei run- two circulations by injecting only one circulation in
ning in the long axis of the vessel and lack regular ring certain animals and by using different colored resins
indentations. Pulmonary arteries have a greater space when injecting both circulations. We traced the plastic
between their surface and adjacent capillaries than pul- casts down from the gross using a dissecting microscope.
D.E. SCHRAUFNAGEL ET AL.
360
Fig. 3.Several characteristic structures were found in these bronchial arteries that may be associated with pressure and flow braking.
A bronchial artery (B), about 135 km in diameter, with deep nuclear
impressions, gives off an 85” branch, measured from the middle of
their long axes as they taper. Note that the musculature is constricted
more of the side with the branch, as evidenced by the deeper nuclear
impressions (wavy arrow). This sheep had only the bronchial arteries
cast. Bar = 10 pm.
RESULTS
At the site of cannulation, the bronchoesophagel artery was 2-3 mm in diameter. In this sized sheep the
right and left main pulmonary arteries are about 1.5
cm in diameter as they enter the lung. The subgross
examination of the casts showed that the bronchial arteries resided on top of and in the walls of the bronchi
and pulmonary arteries. The bronchial arteries often
twisted in a helical structure around the cylindrical
structures they supplied. The bronchial arteries retained their diameter, tapering less than the pulmonary arteries they encircled. The circulations that were
injected filled well in all five animals. In animals with
only one circulation cast, the other circulation did not
fill well. The animal (1)with only the bronchial artery
injection and highest airway pressure filled least.
teries, shown as a void between the artery and adjacent
capillaries (Fig. 1) (Schraufnagel et al., 1983). The
casts of all arteries had oval impressions on their surface that ran with the long axis of the blood vessel, but
in systemic arteries they were deeper than in pulmonary arteries. The imprints are produced by the nuclei
of their endothelial cell, which are less compliant than
the cytoplasm to the distending pressure of the resin.
The deeper depressions in the systemic arteries may
reflect their greater muscularity and tone. Bronchial
arteries differed from pulmonary and other systemic
arteries by their more tortuous course and their anatomic relationships with other blood vessels and airways. The unusual forms that corresponded to Sperrarterzen, described by von Hayek (von Hayek, 1942),
appeared to be unique to bronchial arteries and are
described below.
Light Microscopy
The plastic was easily seen by light microscopy and
outlined the vessels that were cast. In the animals that
had bronchial artery injections, the capillaries beneath
the pleural and around bronchovascular structures
filled.
Scanning Microscopy of the Vascular Casts
Distinguishing bronchial and pulmonary arteries
The casts of extrapulmonary and large bronchial arteries were similar to other systemic arteries: they had
thick walls-thicker than equal-sized pulmonary ar-
Extrapulmonary bronchial arteries
The bronchial arteries entered the connective tissue
around the bronchi and gave off small branches that
joined other bronchial arterial trunks. They spiraled
around the bronchi and pulmonary blood vessels in a
corkscrew pattern. These small vessels (often about 12
pm in diameter) could be larger than pulmonary capillaries, which were about 7 pm in diameter. In contrast, the pulmonary arteries slowly tapered and
hardly branched until they reached the lobular segments. Pulmonary arteries branched most when they
BRONCHIAL CIRCULATION
361
Fig. 5. The vessels with deep transverse constrictions (Sperrurterien) branched further into smaller vessels with tortuosity. This had
deep longitudinal grooves from longitudinal smooth muscle and folds
many times. The extension of these “blockading”features into smaller
bronchial arteries suggests that Sperrurterien is more of a concept of
capability than a precise region in the artery. Bar = 50 pm.
entrance of lobes and in the bronchovascular bundle
(Figs. 1,2).
Sperrarterien
Fig. 4. a: Constrictions were so deep on certain bronchial arteries
that the flow of resin stopped at (or just after) branching points (short
arrow). b,c. Their luminal surfaces had great rugosity with both longitudinal and circular furrowing. These structures characterize casts
of certain bronchial arteries that correspond to Sperrarterien. This
sheep had only bronchial arteries cast. Bars = 100 pm.
On examining the lung with light microscopy, occasionally thick-walled muscular arteries with their lumens nearly occluded, Sperrarterien, were found. Because this German word used by von Hayek is not
easily explained, Krahl elected to retain it in his translation of von Hayek‘s book (von Hayek, 1960). The
term has gained acceptance in English writing as well
as German. Literally it means “blockading arteries”
referring t o their appearance that suggests a blockade
of flow to the blood vessels beyond it. We found arteries
about 100-300 pm in diameter could be considered
Sperrarterien because they had sharp branching, at
right and even acute angles. Their cast surfaces were
marked by both longitudinal and circular furrowing.
The surface irregularities and infoldings were associated with radial retractions that were greatest at
branch points (Figs. 3,4). The deepest furrowings occurred on the intrapulmonary bronchial arteries several divisions before the first capillaries, but even the
terminal arterioles were more rumpled than the pulmonary arteries of the same size. Last, several of these
arteries had branches that choked the flow of the resin,
contrast,the pulmonary
leaving only a cast stump.
arteries were completely
and had smooth cast
Surfaces. Smaller arteries coming from the Sperrarterien were tortuous and often folded on their way to the
capillaries but were not corkscrew (Figs. 5,6).
Bronchial capillaries
were less than 100 pm in diameter. At this level pulmonary arteries formed short branches, often only a
few pm in length, before giving rise to many capillaries. The bronchial arteries started smaller, tapered
less, and branched earlier, as one might expect because
they supply the hilar structures of the lobes and segments. Straight bronchial arteries were found at the
The bronchial capillaries that supplied hilar structures were shorter and had fewer branches than did
pulmonary capillaries. Some bronchial arteries ended
in tufts of capillaries that lacked the characteristic appearance of alveolar capillaries, but attached t o pulmonary veins. In the bronchovascular bundle, the main
bronchial artery was often about 300 pm in diameter
362
D.E. SCHRAUFNAGEL ET AL.
Fig. 6. a: This constricted bronchial artery (B) ends in a tuft of
bronchial capillaries (C) probably at the entry into a secondary lobule.
These capillaries may join alveolar capillaries (top left) or converge
directly into a pulmonary vein (V). We found no bronchial artery
directly supplying alveolar capillaries. Bar = 100 km. b A more
magnified view, shows the larger bronchial artery (B) giving rise to a
burst of capillaries (C), after going a considerable distance without
producing any. Bars = 10 pm.
363
BRONCHIAL CIRCULATION
of microns without branching. The latter was common
for the pulmonary arteries about 100-200 pm in diameter. The vasa vasorum in the walls of pulmonary arteries appeared to disappear into the artery itself (Fig.
71, but the smaller ones appeared to be hugged by a
bronchial artery, which then went into its own capillaries. The bronchial arteries also had their own vasa
vasorum.
Deep into the lobule, bronchial arteries only slightly
larger than capillaries ran around and between structures of the bronchovascular bundle (Figs. 8,9). Small
bronchial arteries anastomosed with themselves in the
walls of large structures and around the small vessels
at the end of the bronchovascular bundle. We did not
find bronchial capillaries leaving and reentering larger
bronchial arteries, although small vessels (from about
7 to 12 pm in diameter) would split and re-anastomose
(Fig. 8). The smallest vessel with its own vasa vasorum
was a bronchial artery 42 pm in diameter. A single
bronchial artery could supply both a bronchiole and
artery.
Giant capillaries
Fig. 7. The cast of this pulmonary artery (PA) is more than 3 mm in
diameter and has small capillaries on its surface (diamond arrowhead). The distance between the vessel lumen (the cast surface) and
the capillaries indicates the capillaries are within the arterial wall.
These capillaries were only found in the animals where both the bronchial and pulmonary arteries were injected. The capillaries extended
a variable distance and often disappeared into the pulmonary artery
itself. Bar = 10 km.
Animal 3 that was filled with both pulmonary and
bronchial injections had giant capillaries-vascular
structures that had the shape and pattern of capillaries
but were up to 600 pm in diameter (Fig. 10). They
appeared to connect the pulmonary and bronchial circulations on the pleural surface of this animal and were
extensive, occupying several square centimeters of surface area. They had no irregularities to suggest a pathologic process but had folds that corresponded to the folds
seen in the normal pleural a t low lung volumes.
DISCUSSION
and several others were usually less than 100 pm in
diameter. These gave off small straight and tortuous
vessels that were generally larger than typical pulmonary capillaries, about 12 pm in diameter. These small
bronchial arteries often penetrated nonalveolar areas
of the lung and gave off tufts of capillaries (Fig. 6).
These tufts could be traced directly into the alveolar
capillaries. Alternatively, the small bronchial arteries
and their capillaries could continue for long distances
and eventually end in a vein or a tuft of capillaries.
Unlike pulmonary capillaries these small arteries
could run long distances without branching. We never
found bronchial arteries directly supplying alveoli, although the capillaries that lined the bronchioles were
extensively connected with the alveolar capillaries,
and the capillary tufts at the end of the bronchial arteries often joined alveolar capillaries. The bronchial
capillary casts were easily distinguishable from alveolar capillaries by the lack of the characteristic appearance of alveolar capillaries described above.
By casting the bronchial and pulmonary circulations
and examining the blood vessels under the scanning
electron microscope we found that their communications were more extensive than is generally taught. In
these normal animals the bronchial circulation joined
the pulmonary circulation at the precapillary, capillary, and postcapillary levels. The precapillary connections occurred in the vasa vasorum of the pulmonary
artery that appear to empty into the pulmonary artery
itself. The capillary connections occurred in the extensively shared capillaries at the end of the bronchial
arteries in the small airways and in the lobular hila.
Postcapillary connections appeared to be represented
by the giant capillaries on the pleural surface. Other
investigators have shown that mediastinal vessels may
flow into pulmonary veins in different species, especially in disease conditions (Khaliq et al., 1972; Harris
and Heath, 1986), but these structures were not studied here. Large capillary structures have been reported
in humans (Zuckerkandl, 1883; Tobin and Zariquiey,
1950) and animals (Prinzmetal et al., 19481, but scanVasa vasorum
ning microscopy of their casts has not been shown beLarger pulmonary arteries could have several bron- fore.
The bronchial capillaries lined bronchi and bronchichial arteries and tangles of capillaries in their walls,
but smaller pulmonary arteries often had only capil- oles, but the capillaries of the lower membranous bronlaries in their walls. The light microscopy showed that chioles and respiratory bronchioles were so extensively
the bronchial vessels penetrated and coursed within connected with alveolar capillaries that it was imposthe media and adventitia of the pulmonary arteries. sible to identify which circulation supplied them. A
The bronchial capillaries of the large pulmonary arter- prevailing concept is that the bronchial circulation
ies could branch and rejoin themselves or go hundreds ends with its capillaries joining alveolar capillaries as
364
D.E. SCHRAUFNAGEL ET AL.
Fig. 8.The vasa vasorum (arrowhead) of a bronchial artery (B) were
often larger than pulmonary capillaries (0.Vasa vasorum slightly
larger than alveolar capillaries may branch and rejoin around blood
vessels. Bar = 100 pm.
Fig. 9.The figure shows a bronchial artery (B) (about 90 pm in
diameter) with several bronchial capillaries (wavy arrow) coursing
with it. On bronchial arteries, capillaries may continue for long distances and eventually find a vein. Bar = 100 pm.
BRONCHIAL CIRCULATION
Fig. 10. Giant capillaries up to 600 Fm in diameter were found
joining the pulmonary and bronchial circulations on the pleural surface in an animal (3) that had both the pulmonary and bronchial
circulations injected. A wrinkle that rose about 1 mm (bent arrow)
could reflect a normal fold in the pleural surface at low lung volumes.
Bar = 1 mm.
the respiratory bronchioles are approached. For larger
airways the bronchial capillaries empty into bronchial
veins (von Hayek, 1960; Miller, 1947; Nagaishi, 1972).
Capillaries are definable by their regular network pattern with multiple branching and re-entry sites. Casts
of the capillary beds of most organs are characteristic
in their pattern and density. The structural patterns of
the capillaries of the bronchioles and alveoli are distinct and the term bronchial capillaries has been applied to the capillary casts that line airways and have
the bronchial pattern even though blood could fill them
from the pulmonary artery (Schraufnagel, 1987). Indeed, casting either circulation filled the capillaries at
the intersection of the two networks. It is not difficult
to speculate that larger anastomoses could arise if an
inflammatory or neoplastic stimulus were present. The
only postcapillary connections we found in this study
were on the pleura in an animal injected from both the
pulmonary and bronchial arteries. To find out the frequency and extent of this finding, a separate study
with additional animals and conditions needs to be carried out.
In addition to evaluating the junctures of these circulations we sought to learn if discrete structures
might be associated with the large pressure drop between the bronchial and the pulmonary circulations.
Our findings confirm and amplify the observations of
von Hayek. He believed that the thick muscular arteries with abundant longitudinal smooth muscle were
associated with bronchial to pulmonary anastomosis
(von Hayek, 1942). The multiple longitudinal and circumferential foldings and sharp-angled branching of
these Sperrarterien that we found make it is easy to see
how the resistance could quickly change by relaxation
of the arterial smooth muscle. Relaxation could allow
bronchial blood flow to increase t o prevent pulmonary
infarction if the pulmonary artery was occluded (Virchow, 1847). It is also easy to imagine how a fault in
this control could lead to a localized increase in pulmonary blood pressure or flow, which could result in
bleeding into the airspace. The “blockading effect” that
365
could occur in these vessels affirms the term used by
von Hayek, although it may be better expressed as a
concept rather than an exact segment because their
beginnings and endings are often subtle. The casts
show that the muscle is not strictly longitudinal, a fact
that von Hayek also noted (von Hayek, 1960). Although von Hayek was uncertain if the Sperrarterien
communicated directly with pulmonary arteries or capillaries, we found that they branched into capillaries
supplying the interstitium and nonalveolar lung as
well as alveolar capillaries through bronchial capillaries.
Although the folding, branching, and wall rugosity
may be unique to the Sperrarterien and is greater than
other systemic arteries studied so far, the helical twisting of the bronchial arteries is also found in arteries of
skeletal muscle (Schraufnagel et al., 1983) whose corkscrew pattern no doubt relates to contraction. Part of
the tortuosity of the bronchial blood vessels could be an
adaptation to the shortening and lengthening of the
bronchi as the lung undergoes its respiratory motion.
Although casting and studying the fine structure of
the blood vessels has added considerably to how we
look at these circulations, this technique is best used
with light microscopy and physiological evaluation. In
this study we did not characterize the pattern of capillaries around larger airways, which has already been
shown (Magno and Fishman, 1982; Charan et al.,
1984). Also, we did not study the vasa vasorum of the
pulmonary veins, which have been shown by Ohtani in
the rat (Ohtani, 1980). He filled the pulmonary veins
and their vasa vasorum and found they had one to
three layers of capillaries with longitudinal connections, whereas the capillaries of the pulmonary artery
were mostly in the adventitia. He found the vasa vasorum outside the lungs collected into bronchial veins
and inside the lungs into pulmonary veins. Others
have shown that bronchial veins empty into pulmonary
veins in humans (Tobin, 1952; Pump, 1972; Murata et
al., 1986). Using silicone injections of the bronchial circulation, Sobin described a spiral structure of the vasa
vasorum (Sobin et al., 19621, which is similar to what
we found. There has been no study of vascular casts
that described the vasa vasorum ending in the pulmonary artery itself, but our finding of this should not be
unexpected. The vasa vasorum of pulmonary arteries
are well known to enter pulmonary arteries to recanalize vessels that have become occluded with thrombus
(Heath and Thompson, 1969).
The sheep with their thick pleura may be different
from other species with thin pleural, such as the rat
(McLaughlin, 1983). The rat, which is the most studied
species by scanning electron microscopy of vascular
casts, has its pleura supplied by the pulmonary arteries
(McLaughlin, 1983; Aharinejad et al., 1991). Injecting
the pulmonary artery in the sheep did not fill the pleural capillaries, which also occurs in the human
(Schraufnagel et al., 199513). In the sheep, with both
circulations injected, it was often difficult to determine
which circulation supplied a particular capillary bed
because of the lack of color in scanning electron microscopy and the difficulty in tracing fine structures. Furthermore, filling a capillary bed with a bronchial artery injection does not necessarily signify the bed is
filled that way in vivo. The direction of flow in these
366
D.E. SCHRAUFNAGEL ET AL.
vessels may change in life depending on the pressure in
the vascular circuit (Harris and Heath, 1986).
ACKNOWLEDGMENTS
This work was supported in part by the National
Institutes of Heath, Heart, Lung, and Blood Institute
grant HL10342 and the James Liston Fund at the University of Illinois for research on the Acute Respiratory
Distress Syndrome. Dr. Wagner is a n established investigator of the American Heart Association. We
thank Teresa Privett and John Irwin for their technical
support and the Electron Microscopy Facility of the
Research Resources Center, University of Illinois a t
Chicago, €or their assistance and use of equipment.
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