Cell Tiss. Res. 176, 553-564 (1977)
Cell and Tissue
Research
9 by Springer-Verlag 1977
A Scanning Electron Microscope Study
of the Microvasculature of the Avian Lung
Nigel H. West, Owen S. Bamford, and David R. Jones
Department of Zoology, University of British Columbia, Vancouver, British Columbia
Summary. 1. The microvasculature of the lung of the duck and pigeon was
studied by scanning electron microscopy of vascular casts and critical point
dried preparations of the gas exchange tissue.
2. The gas-exchange capillaries are discrete tubular vessels intimately associated with air capillaries in a three dimensional network.
3. The capillaries originate from arteries at the periphery of the parabronchus, and are collected by veins which run close to its luminal surface.
4. The capillary bed of 3-5 atria is drained by a single vein. It is suggested
that the vein and its associated capillaries may form a controllable subunit
of pulmonary perfusion.
Key words: Duck - Pigeon - Avian - Pulmonary microvasculature -Capillary bed - Lung circulation - Lung anatomy.
Introduction
The fine structure of the respiratory exchange surfaces of mammals (Weibel,
1963; Rosenquist et al., 1973) and fish (Hughes and Morgan, 1973; Morgan
and Tovell, 1973) has been extensively studied, and consequently their functional
morphology is well established. By contrast the gas exchange surface of the
avian lung has received comparatively little attention.
The gross anatomy of the lung and air-sac system of the bird was extensively
studied by early workers (Duncker, 1971, for exhaustive review) but many false
conclusions were reached, primarily because the observations were viewed in
a mammalian context. The historical conflicts have been largely resolved by
the recent anatomical work of Duncker (1971, 1972) and King (1966), King
Send offprint requests to: Dr. Owen S. Bamford, Department of Animal Physiology, P.O. Box
30197, Nairobi, Kenya, Africa
The authors wish to thank Mr. L. Veto for his advice on S.E.M. techniques, and Dr. D.G.
Smith for his criticism of the manuscript
554
N.H. West et al.
and Molony (1971). Unreliable anatomical data naturally led to many opposing
views on the ventilation of the lungs and associated air-sacs (Duncker, 1971)
although the gas flow pattern through the lung now appears to be conclusively
established (Piiper and Scheid, 1973). It is generally accepted that the flow
of respiratory gases is unidirectional through the parabronchi of the paleopulmo
in all birds, although higher birds possess a further system of parabronchi,
the neopulmo, in which the direction of gas flow changes with the phase of
the respiratory cycle (Duncker, 1972). The respiratory exchange tissue proper
surrounds the parabronchi. Air capillaries branch off from depressions in the
parabronchial wall, the atria, and there interdigitate with blood capillaries.
It is at this site, within the tissues of the wall, that gas exchange takes place.
The anatomy of the major pulmonary blood vessels has been described
for several species of birds by Radu and Radu (1971), but these authors did
not consider the courses of the smaller blood vessels within the gas exchange
areas of the lung. In particular the relationship between the blood capillaries
involved in gas exchange and the air capillaries has not been elucidated. This
task is very difficult in the bird, due to the complex three dimensional arrangement of the blood capillaries, which is in marked contrast to the flat sheet-like
arrangement of exchange capillaries in mammalian alveoli (Weibel, 1963 ; Fung,
1975) and the secondary lamellae of teleosts (Hughes and Morgan, 1973; Morgan
and Tovell, 1973). Duncker (1974), using histological techniques, was able to
present a reconstruction of the structure of the parabronchial exchange tissue,
while more recently Abdulla and King (1975) made a study of the pulmonary
vasculature of the fowl Gallus domesticus and were able to describe the courses
of the arterioles and venules within the exchange tissue itself. They both agree
that the blood capillaries of the parabronchial wall arise from short arterioles
at the exchange tissue periphery and are collected by venules which run for
a short distance beneath the luminal surface of the parabronchus before penetrating the exchange tissue once more to ultimately join inter-parabronchial veins.
Clearly, detailed knowledge of parabronchial microvascular structure is
needed in order to provide a firm structural basis for the demonstrated function
of the parabronchus as a cross-current gas exchanger (Piiper and Scheid, 1973).
To this end we have attempted in the present study to directly view parabronchial
fine structure by means of the scanning electron microscope with the aim of
relating observed structure to known function.
Methods
Lungs for S.E.M. examination were obtained from young adult Khaki Campbell Ducks (Anas
platyrhynchos), and homing pigeons (Columba livia) of a local stock. Six birds of each species
were used for the preparations. The birds were prepared by cannulating the right brachial vein
under local anaesthesia (Xylocaine, Astra-Hewlett Ltd.) and injecting with 500 i.u. heparin/k.g.,
followed by an overdose of sodium pentabarbitone (Nembutal, Abbott). After death the sternum
was cut and the thorax was opened to expose the heart and central blood vessels. The pericardium
was opened, the heart removed and suction applied in order to partially exsanguinate the bird.
The left pulmonary artery was then cannulated with polyethylene tubing (P.E. 240) and the left
lung perfused with saline at the appropriate mean physiological pressure levels (20 mm Hg, duck,
16 mm Hg pigeon) until saline returning in the pulmonary vein ran clear.
Avian Pulmonary Microvasculature
555
Critical Point Dried Preparations
10 ml of Karnovsky's glutaraldehyde-formaldehyde fixative was introduced into the left bronchus
via the trachea in order to fix the left lung. The lung was then carefully dissected from the
thoracic cavity and 1-2 m m sections cut parallel to the parabronchi with a razor blade. The sections
were immersed in fresh 5~ Karnovsky fixative for 5 h and subsequently stored in 0.2 M cacodylate
buffer at 5~ They were then prepared for the S.E.M. by the technique of critical point drying
(Anderson, 1951). The dried specimens were trimmed, m o u n t e d on specimen stubs with Silver
D a g and their suitability for S.E.M. examination was checked with a binocular microscope.
Vascular Casting
Those casts to be observed in the S.E.M. were prepared with Batson's methacrylate c o m p o u n d
made up as a slowly polymerising mixture. This was perfused through the pulmonary artery after
a preliminary saline infusion with a constant pressure head of 20 m m H g (duck) or 16 m m Hg
(pigeon). When the perfusion of Batson's c o m p o u n d was complete, as judged by the flow of
the c o m p o u n d from the left pulmonary vein, the c o m p o u n d was hardened by immersing the bird
in warm water for 3 h. The left lung was then dissected free, removed from the thoracic cavity,
and placed in 20% K O H solution at room temperature in order to remove the soft tissues. After
rinsing in water and alcohol the resulting cast was allowed to dry in a dessicator before 1 2 m m
sections were razor cut and m o u n t e d for S.E.M. examination. In two birds a pigment was added
to the Batson's compound. The particle size was such that pigment particles could not pass through
the exchange capillaries of the lung, enabling arteries and veins to be positively identified.
Both critical point dried specimens and casts were carbon/gold coated in a Mikros VE 10
evaporator and subsequently examined with a Cambridge Stereoscan S.E.M. using beam potentials
from 2-20 kV. The stage was tilted 3-6 ~ depending on magnification, between the pairs of a
micrograph (Boyde, 1973).
Preliminary studies showed paleo- and neopulmo to be indistinguishable at the level of the
gas exchange tissue. Because the paleopulmo was more amenable to sectioning due to the regular
arrangement of its parabronchi, most of the material examined was taken from this region.
The terminology of the International Committee on Avian Anatomical Nomenclature (1975)
is used throughout this paper.
Results
a) Critical Point Dried Preparations
Parabronchi. The parabronchial walls of both the duck and the pigeon possess
a well developed inner lattice-like network of smooth-muscle bundles which
ring the parabronchial lumen. The muscle bundles are connected to the parabronchial wall by elastic tissue septa running more or less perpendicularly to
the plane of the wall (Figs. 2, 3). The luminal surface of the atrial wall thus
is divided into a series of compartments with depressed floors, the atria, which
are surrounded and delineated by the tissue septa and muscle bands (Figs. l, 2).
The major bands of smooth muscle are arranged in a circular fashion, or
as a helix of shallow pitch running down the parabronchus. However at quite
regular intervals, minor muscle bands divide and run to the neighboring band,
so that the impression is gained of two shallow intersecting tissue helices of
opposite pitch running the length of the parabronchus. The resulting atrial
boundaries formed by the intersection of the helices therefore usually approximate a rhomboid in shape, with the long axis of the rhomboid often lying
556
N.H. West et al.
All figures except 7 and II are stereo pairs
Fig. 1. Pigeon paleopulmo. Critical point dried preparation. Longitudinal section of parabronchus
showing atria on the parabronchial wall and a cut surface of exchange tissue, at atrium; by interparabronchial blood vessel; e exchange tissue; i infundibulum; m atrial muscle, x 158
Fig. 2. Duck paleopulmo. Critical point dried preparation. Surface view of an atrium and the
associated infundibular openings, at atrium; i infundibulum;m atrial smooth muscle, x 410
a l o n g the circumference of the p a r a b r o n c h i a l wall (Fig. 1). Typical atrial dimensions are in the range 60 100 Ix • 120-300 g in both pigeon a n d duck, while
the sheets of elastic tissue in our fixed p r e p a r a t i o n extend some 40-60 g into
the p a r a b r o n c h i a l l u m e n (Fig. 3).
A t r i a . The atrial floor is perforated by openings, the i n f u n d i b u l a , which lead
into the area of exchange tissue s u r r o u n d i n g the p a r a b r o n c h i a l lumen. Typically
groups of 3-6 i n f u n d i b u l a some 2 5 4 0 g in diameter perforate the floor of
Avian Pulmonary Microvasculature
557
Fig. 3. Pigeon paleopulmo. Critical point dried preparation. Oblique view of longitudinal section
illustrating the depth of the bands of atrial smooth muscle, a t atrium; e exchange tissue; m atrial
muscle. • 86
Fig. 4. Duck neopulmo. Critical point dried preparation. Longitudinal sections through infundibulure penetrating exchange tissue. Blood capillaries can be seen under the epithelium of the infundibulum. a t atrium; e exchange tissue; i infundibulum; m atrial smooth muscle, x 450
a single atrium (Figs. 1, 2), and they penetrate the pulmonary exchange tissue
for some 100-150 ~t giving off air capillaries before they finally appear to merge
with the air capillary network (Fig. 4). Tangential sections of the exchange
tissue of the parabronchial wall show a dense, apparently random, three-dimensional " s p o n g e " of blood capillaries and air capillaries, penetrated by the lumina
of the infundibulum in sections taken close to the atrial surface (Fig. 5). The
entrances to air capillaries, approximately 8 la in diameter, are visible in the
walls of the infundibula, while the positions of blood capillaries can be seen
558
N.H. West et al.
Fig. 5. Duck paleopulmo. Critical point dried preparation. Tangential section of exchange tissue
at the level of the infundibula, ac opening of air capillary into infundibulum; c blood capillary
beneath respiratory epithelium; i lumen of infundibulum; r red cell. The broken red cell to the
right of the picture is still within a blood capillary, x 750
beneath the thin respiratory epithelium of the infundibulum (Fig. 5). At least
in the region near the atrial floor most of these capillaries appear to be arranged
circumferentially around the infundibular wall (Figs. 4, 5) although this arrangement does not appear to persist far into the exchange tissue. The interstices
of the blood capillary network, the air capillaries, are therefore a series of
minute interconnected air spaces separated from the seemingly randomly
arranged blood capillaries by a thin epithelium, and connecting to the parabronchial lumen via air capillary entrances in the walls of the infundibula.
In some of our preparations washing failed to remove all the adhering
red blood cells and these survived the critical point drying process without
distortion, while occasionally capillaries containing red cells were sectioned
(Fig. 5). In these cases the red cells appear to closely conform to the internal
dimensions of the respiratory capillary, contacting the capillary wall around
the internal circumference.
b) Corrosion Cast Preparations
Arterioles. The blood capillaries of the respiratory exchange tissue originate
from short intra-parabronchial arterioles which, after branching from interparabronchial arteries lying in the exchange tissue between adjacent parabronchi,
penetrate the exchange tissue towards the parabronchial lumen and give off
capillaries (Fig. 6). Some arterioles are very short, and the apparent origin
of exchange capillaries directly from an interparabronchial artery was observed
in a few cases. Three examples were found of a dilatation of the lumen at
the root of an intraparabronchial arteriole with a ring-like constriction distal
to the dilatation (Fig. 7). These structures are suggestive of the arteriolar sphincters tentatively identified by Abdulla and King (1975) and may represent sites
at which precapillary resistance may be adjusted. Typically the intraparabron-
Avian Pulmonary Microvasculature
559
Fig. 6. Duck paleopulmo. Vascular cast. View of part of longitudinal section of parabronchus
showing the blood vessels of the parabronchial wall and exchange tissue, a intraparabronchial
artery breaking up into gas exchange capillaries; a t position of atrium; v atrial veins collecting
exchange capillaries, x 165
Fig. 7. Duck paleopulmo. Vascular cast. Ifiterparabronchial artery and vein, formed by the union
of intraparabronchial veins from adjacent parabronchi, showing sphincter-like region at the junction
of the inter- and intra-parabronchial arteries, a interparabronchial artery; a t region of atria; e
area of exchange capillaries; s septal space, produced by the KOH removal of the interparabronchial
septum; sp sphincter, x 117
560
N.H. West et al.
Fig. 8. Duck paleopulmo. Vascular cast. View of an atrial region similar to that illustrated in
Figure 2. Note the orderly arrangement of blood capillaries within the atrium, at adjacent atrial
region; c blood capillaries; v atrial vein, which in life would run beneath the smooth muscle
and elastic tissue septum surrounding the atrium, x 410
chial arterioles give off clusters of 5 g capillaries that immediately fan out
and interdigitate to form the exchange tissue (Figs. 6, 7). The only regularly
arranged exchange capillaries were found near the openings of the infundibula
into the atria, In this region capillaries often run circumferentially around the
atrial floor and infundibular openings (Fig. 8), although this ordered arrangement does not appear to persist deep into the infundibula, but is replaced
by a m o r e random appearance, previously seen in the critical point dried preparations, as the mass of blood capillaries is increasingly penetrated by air capillaries
(Fig. 9).
Veins. The veins draining the respiratory exchange capillaries lie on the surface
of the parabronchial walls in the corrosion preparations, running between atria
in such a position that they lie at the base of the interatrial septa in life (compare
Figs. 1 and 10). Typically the capillaries underlying a group of 3-5 atria are
drained by a single atrial vein (Fig. 10), although there is some overlap between
the drainage areas of adjacent atrial veins, so that a single atrium may be
partially drained by two veins. As observed by Abdulla and King (1975), the
atrial veins receive some capillaries directly from the exchange tissue, while
others drain into short tributary veins, which then join the larger atrial veins.
After running under an interatrial septum for some 45 11 the large atrial veins
penetrate the exchange tissue radially to join an interparabronchial vein running
between adjacent parabronchi (Fig. 7).
Suprisingly, no evidence was found in the vascular casts of pigeon or duck
lungs for the existence of septal venules (Abdulla and King, 1975), which in
the chicken are described as arising from the exchange capillaries and forming
a network of small anastomosing vessels within the interatrial septa. In the
duck and pigeon at least it appears that the interatrial septa may be poorly
Avian Pulmonary Microvasculature
Fig. 9. Duck paleopulmo. Vascular cast. Region around the entrance to air capillaries,
of air capillary ; c blood capillary; i lumen of infundibulum, x 825
561
ac
position
Fig. 10. Pigeon paleopulmo. Vascular cast. View of the parabronchial wall demonstrating the arrangement of atrial veins around the atria. Each venule collects capillaries from more than one
atrial region, a t atrial region; v septal venule, x 180
vascularized, a l t h o u g h it is possible that p e r f u s i o n with B a t s o n ' s s o l u t i o n caused
these vessels to constrict thus p r e v e n t i n g their filling.
Discussion
S.E.M. e x a m i n a t i o n o f the r e s p i r a t o r y gas-exchange tissue in the d u c k a n d
pigeon has revealed a high degree o f s t r u c t u r a l c o m p l e x i t y , i m p l y i n g c o n s i d e r a b l e
f u n c t i o n a l flexibility, in the a r r a n g e m e n t o f the p u l m o n a r y m i c r o v a s c u l a t u r e .
M o s t o f the e x c h a n g e tissue consists o f discrete t u b u l a r b l o o d capillaries
s e p a r a t e d b y a thin r e s p i r a t o r y e p i t h e l i u m f r o m small interstitial air spaces,
the air capillaries. A recently p r o p o s e d sheet-flow c o n c e p t has been used to
562
N.H. West et al.
develop models of alveolar blood volume and transit time in the mammalian
(cat) lung. Predictions made using the model closely approximate experimental
results. The concept is based on the morphological evidence that in the mammal
the alveolar vascular space may be considered as a continuous sheet with endothelial boundaries held apart by cellular posts, possessing a high vascular space]
tissue volume ratio (Fung, 1975; Sobin, Tremer and Fung, 1970). These conditions do not obtain in the avian lung, and it seems clear that the sheet-flow
model is less applicable to the parabronchial microvasculature than the alternative tube-flow model of blood flow in which the pulmonary capillaries are
geometrically analysed as a network of interconnected tubes (Weibel, 1963).
Anatomical arterio-venous shunts were not observed in the lungs of Anas
platyrhynchos or Columba livia, and they also appear to be absent in the lungs
of Gallus domesticus (Abdulla and King, 1975). Such shunts are not present
in the normal human lung or the lung of Bufo marinus, although they appear
to exist in the lung of Xenopus laevis (Nagaishi, 1972; Smith and Campbell,
1976; Smith, 1976). Recently, however, a bronchial shunt pathway has been
demonstrated in the fowl lung. The bronchial artery derives from the right
common carotid artery and supplies the extrapulmonary bronchus with an arterial network before joining the pulmonary artery. Venous drainage of the caudal
region of the extrapulmonary bronchus is by veins which empty into the pulmonary veins by-passing the gas exchange area of the lung (Abdulla and King,
1976).
In the pulmonary circulation deoxygenated blood flows from short arterioles
which branch from septal arteries, into the capillaries which form the exchange
tissue (Figs. 7, 11). Capillary blood flows from the interparabronchial septum
perpendicularly towards the parabronchial lumen. Thus the flow of blood in
the capillaries is essentially at right angles to the flow of gas in the parabronchi.
The anatomical requirements for functional cross-current gas exchange appear
to be fulfilled in that venous blood is supplied to the whole length of a parabronchus (Piiper and Scheid, 1973; Duncker, 1974; Abdulla and King, 1975).
Duncker (1974) and Abdulla and King (1975) further consider, on morphological
grounds, that there may be an auxiliary counter-current mechanism operation
in the exchange tissue, as blood passing down an exchange capillary from the
interparabronchial septum to the parabronchial lumen would meet air capillary
gas with a progressively higher Po2 and lower Pco2. According to Scheid
and Piiper (1972) the rate of gaseous diffusion in the exchange tissue may
be sufficiently rapid to maintain a very steep partial pressure gradient along
part of the air capillary length. However, the actual length of the overall diffusion
path may be highly dependant upon the degree of atrial smooth muscle contraction. Although physiological tests of this dependence are lacking at present,
it would seem, for example, that the restriction of the bulk flow of parabronchial
gas to a central aperture by atrial muscle contraction would considerably increase
the length of the overall diffusion path into the exchange tissue.
The pulmonary blood capillaries eventually join atrial veins which lie superficially in the walls surrounding the parabronchial lumen and which collect oxygenated blood from the capillary beds of 3-5 atria (Figs. 10, 11). These venules
are therefore in a prime position to control atrial outflow if they can alter
their flow resistance, especially since resistance changes in one venule could
Avian Pulmonary Microvasculature
563
e
: ~
I II
~
r
I
I
~
I TM
I
p
e
~
,
e
Fig. 11. Schematicdiagram of the vascular supply to a group of four atria whichform a microvascular
unit. The exchange tissue of the nearer two atria has been removed, al interparabronchial artery;
a2 short intraparabronchial artery giving rise to capillaries; c gas exchange capillary; vl atrial
vein; v2 interparabronchial vein; s septal venule (Abdulla and King, 1975); sp arteriolar sphincter;
m smooth muscle band; at atrium; i infundibulum; ac air capillaries; e exchange tissue. The
arrow indicates the direction of capillary blood flow
control perfusion in a small group of atria. The above observations are of
special interest in view of Duncker's (1974) suggestion that resistance increases
in the atrial veins could occur on exposure to parabronchial gases of endexpiratory composition, for example, in the distal ends of parabronchi in conditions of low ventilation. In this case constriction of the vessels exposed to
end-expiratory gas tensions would allow for autoregulation of regional perfusion
along the length of a parabronchus, and serve to prevent effective arterial-venous
shunts occuring in the distal ends of poorly ventilated parabronchi. It should
be pointed out that the contraction of venules in order to regulate flow does
not appear to be a c o m m o n feature of any circulation, although "vigorous
contraction" has been observed in muscular venules of the bat wing (Wiederhielm and Weston, 1973). In view of the lack of any histological evidence
of the presence of substantial quantities of smooth muscle in the veins however,
the arteriolar sphincters situated at the junction of the inter- and intra-parabronchial arteries described in G a l l u s d o m e s t i c u s by Abdalla and King (1975) must
be considered more likely (Fig. ll) candidates for the control of perfusion in
the pulmonary microvasculature. It has not yet proved feasible to determine
whether those atrial capillary beds with a single venous outlet are also served
by a single arteriolar inlet although they are shown as such in Figure 11. If
564
N.H. West et al.
this were so then it would be possible to view the capillaries of one such
group of atria as a single functional unit of microcirculation and the microvasculature of a parabronchus as an aggregate of such repeating units, each with
the potential for an independantly controlled degree of perfusion.
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Accepted September 22, 1976