Download Relationship of Structure and Function of the Avian Respiratory

Relationship of Structure and Function of the Avian Respiratory
System to Disease Susceptibility
M. R. FEDDE1
Department of Anatomy and Physiology, College of Veterinary Medicine, Kansas State University,
Manhattan, Kansas 66506-5602
ABSTRACT The avian respiratory system exchanges
oxygen and carbon dioxide between the gas and the
blood utilizing a relatively small, rigid, flow-through
lung, and a system of air sacs that act as bellows to
move the gas through the lung. Gas movement through
the paleopulmonic parabronchi, the main gas exchanging bronchi, in the lung is in the same direction during
both inspiration and expiration, i.e., from the mediodorsal secondary bronchi to the medioventral secondary
bronchi. During inspiration, acceleration of the gas at
the segmentum accelerans of the primary bronchus
increases gas velocity so it does not enter the medioventral secondary bronchi. During expiration, airway
resistance is increased in the intrapulmonary primary
bronchus because of dynamic compression causing gas
to enter the mediodorsal secondary bronchi. Reduction
in air flow velocity may decrease the efficiency of this
aerodynamic valving and thereby decrease the efficiency
of gas exchange.
The convective gas flow in the avian parabronchus is
orientated at a 90° angle with respect to the parabronchial blood flow; hence, the cross-current designation of
this gas exchanger. With this design, the partial pressure
of oxygen in the blood leaving the parabronchus can be
higher than that in the gas exiting this structure, giving
the avian lung a high gas exchange efficacy. The
relationship of the partial pressure of oxygen in the
moist inspired gas to that in the blood leaving the lung
is dependent on the rate of ventilation. A low ventilation
rate may produce a low oxygen partial pressure in part
of the parabronchus, thereby inducing hypoxic vasoconstriction in the pulmonary arterioles supplying this
region.
Inhaled foreign particles are removed by nasal
mucociliary action, by the mucociliary escalator in the
trachea, primary bronchi, and secondary bronchi. Small
particles that enter parabronchi appear to be phagocytized by the epithelial cells in the atria and infundibulum. These particles can be transported to interstitial
macrophages but the disposition of the particles from
this site is unknown. The predominant site of respiratory infections in the caudal air sacs, compared to other
parts of the respiratory system, can be explained by the
gas flow pathway and the mechanisms present in the
parabronchi for particle removal.
(Key words: lung, air sacs, ventilation, defense system, pulmonary blood flow)
1998 Poultry Science 77:1130–1138
GENERAL ARRANGEMENT OF THE
AVIAN RESPIRATORY SYSTEM
IN THE BODY COELOM
The respiratory system in birds has the principal
function of exchanging oxygen and carbon dioxide
between atmosphere and blood. It is also involved in
temperature regulation and phonation. It has these
features in common with the respiratory system of
mammals but it differs significantly in the anatomical
arrangement of its parts (Figure 1). The respiratory
system begins at the nares and has passages in the head
that lead inhaled gas to the larynx. The trachea extends
Received for publication August 3, 1997.
Accepted for publication February 21, 1998.
1To whom correspondence should be addressed.
from the larynx and is sometimes very incompressible,
as in ducks and geese, and sometimes easy to compress,
as in chickens. The trachea in some birds is extremely
long (sometimes longer than the entire body) and
tortuous or coiled, as in the trumpet bird. The trachea
branches into two extrapulmonary primary bronchi,
each of which goes to a lung and its associated air sacs.
The lung is a relatively rigid structure that does not
expand and retract with breathing; its function is to
provide a large surface area for gas exchange with the
blood and it does this in a very small space. The air sacs
function as bellows whose change in volume causes
pressure differences across the lungs that result in gas
movement during inspiration and expiration. The air
Abbreviation Key: PCO2 = partial pressure of carbon dioxide; PO2 =
partial pressure of oxygen.
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SYMPOSIUM: INFECTIOUS POULTRY DISEASES
1131
small; in the chicken, the caudal thoracic air sacs are
small and the abdominal air sacs are large.
The structure of the avian respiratory system has
been extensively studied but there are still some
important questions that remain unanswered and
thereby limit the functional understanding of this
system. Details about the structure can be found in
several original works and reviews (King, 1966; Duncker, 1971; King and White, 1975; Nickel et al., 1977;
Fedde, 1986; Brackenbury, 1987; Abdalla, 1989; King,
1989; Maina, 1989; McLelland, 1989a,b). The most
appropriate terminology to describe the avian respiratory system is presented in detail by King (1993) in the
Handbook of Avian Anatomy: Nomina Anatomica Avium.
GAS FLOW PATTERNS IN
THE RESPIRATORY SYSTEM
DURING BREATHING
FIGURE 1. General organization of the respiratory system in the
chicken. Clav. AS = clavicular air sac; cran. th. AS = cranial thoracic air
sac; caud. th. AS = caudal thoracic air sac; Abd. AS = abdominal air
sac.
sacs have an extremely thin wall, do not contribute to
gas exchange with the blood, and occupy every
available space in the body coelom not occupied by
other viscera. Most birds, including the chicken, have
nine air sacs; paired cervical air sacs (not shown in
Figure 1), an unpaired clavicular air sac that is
connected to each lung, paired cranial thoracic air sacs,
paired caudal thoracic air sacs, and paired abdominal air
sacs. The cervical, clavicular, and cranial thoracic air sacs
arise from the first set of secondary bronchi leaving the
intrapulmonary primary bronchus (medioventral secondary bronchi); they are often considered as a group
called the cranial air sacs because of the similarity in the
oxygen and carbon dioxide concentrations within them.
The caudal thoracic and abdominal air sacs (often called
collectively the caudal air sacs) arise from a second and
third set of secondary bronchi (lateroventral and mediodorsal secondary bronchi) and from the continuation of
the intrapulmonary primary bronchus. The oxygen
concentration is higher and the carbon dioxide concentration is lower in the caudal air sacs than in the cranial
air sac group. The relative sizes of the air sacs vary in
different species; for example, the caudal thoracic air
sacs are large in ducks while the abdominal air sacs are
Active contraction of muscles of the body wall
coupled with its elastic recoil during both inspiration
and expiration are responsible for the cyclic changes in
the volume of the coelom (Fedde, 1987). These volume
changes result in an increase in the volume of the air
sacs during inspiration and a decrease in their volume
during expiration. Pressure in the air sacs is, therefore,
less than that in the atmosphere during inspiration and
gas moves from the atmosphere, through the lungs and
into the air sacs. The pathway for part of the gas flow is
through the paleopulmonic parabronchi that connect
mediodorsal to the medioventral secondary bronchi
(Figure 2). About one-half of an inspired tidal volume
traverses these parabronchi and about one-half of an
inspired tidal volume passes through the much smaller
neopulmonic parabronchial network that connects the
mediodorsal and lateroventral secondary bronchi to the
caudal thoracic and abdominal air sacs, and through the
direct connection from the intrapulmonary primary
bronchus to the abdominal air sacs. Because the
neopulmonic parabronchial network contains only about
15 to 20% of the gas exchange surface in the lung in
chickens, the ventilation/perfusion ratio is very high in
this network (Duncker, 1971; Scheid et al., 1989). Thus,
the gas in the caudal air sacs has only a small reduction
in the oxygen partial pressure compared to that in air,
and has a carbon dioxide partial pressure that is only
increased by a small amount above that in air (Fedde,
1986). On the other hand, gas that enters the cranial air
sacs has been exposed to a large fraction of the gas
exchanging surface in the lung (the paleopulmonic
parabronchi) and has partial pressures of oxygen (PO2)
and carbon dioxide (PCO2) only a few torr different
from that in end-expired gas or in mixed venous blood
entering the lung (Meyer et al., 1976; Scheid et al., 1989).
As will be mentioned later, the gas pathway through the
avian lung can explain the reason for the disposition of
the caudal air sacs to bacterial infections, compared to
the cranial air sacs.
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FEDDE
the avian lung, the unidirectional gas flow through the
paleopulmonic parabronchi has been postulated to occur
because of “aerodynamic valving” (Dotterweich, 1936).
There has recently been renewed interest in determining
the mechanisms responsible for aerodynamic valving in
the avian lung during both inspiration and expiration
(Banzett et al., 1987; Butler et al., 1988; Kuethe, 1988;
Wang et al., 1988, 1992; Banzett et al., 1991; Brown et al.,
1995). A constricted region of the primary bronchus
(termed the segmentum accelerans) just cranial to the
opening of the medioventral secondary bronchi (at least
in the goose lung, Brown et al., 1995) causes the gas
stream to be accelerated during inspiration so that it
does not enter the medioventral secondary bronchi.
Thus, aerodynamic valving during inspiration depends
on gas velocity (as well as gas density), and is most
effective when velocity is high. The smooth muscle in
the wall of the segmentum accelerans appears to relax in
the presence of elevated carbon dioxide concentration
and unless the gas velocity simultaneously increases, the
FIGURE 2. Pathway of gas flow in the avian respiratory system
during inspiration. Enlargement of the body cavity by inspiratory
muscle action lowers pressure in the air sacs relative to that in the
atmosphere and gas flows into the system. Gas does not enter the
medioventral secondary bronchi, but passes into the mediodorsal
secondary bronchi. Some of the gas passes through the paleopulmonic
parabronchi, and the remainder passes into the neopulmonic
parabronchi and caudal air sacs.
During expiration, reduction in coelomic volume
increases the pressure in the air sacs relative to that in
the atmosphere and gas moves out of the air sacs
(Figure 3). Some of the gas from the caudal air sacs
again traverses the neopulmonic parabronchi and most
of the gas enters the paleopulmonic parabronchi,
traveling in the same direction through these latter
structures as during inspiration. Gas from the cranial air
sacs travels through the medioventral secondary bronchi
to exit the lung via the intrapulmonary primary
bronchus without contacting any parabronchial gas
exchanging surfaces. Thus, exchange of oxygen and
carbon dioxide between gas and blood occurs both
during inspiration and expiration in birds and nearly all
of the gas that was inhaled has passed over paleopulmonic parabronchial gas exchanging surfaces during
some part of the respiratory cycle.
The pattern of gas flow through the avian respiratory
system and the proposed mechanisms responsible for
this pattern has been discussed by Scheid and Piiper
(1989). Because of the lack of any anatomical valves in
FIGURE 3. Pathway of gas flow in the avian respiratory system
during expiration. Reduction in volume of the body cavity by
expiratory muscle action increases pressure in the air sacs relative to
that in the atmosphere and gas flows out of the system. Compression
of intrapulmonary primary bronchus causes gas coming from the
caudal air sacs to pass through neopulmonic parabronchi, into
mediodorsal secondary bronchi and through the paleopulmonic
parabronchi. Gas from the cranial air sacs does not pass through
parabronchi on the way to the primary bronchus and trachea.
SYMPOSIUM: INFECTIOUS POULTRY DISEASES
1133
FIGURE 4. Gas exchange characteristics of the cross-current system in the bird lung during normal ventilation. PI = partial pressure of oxygen
entering a parabronchus; PE = partial pressure of oxygen in the gas exiting a parabronchus; Pa = partial pressure of oxygen in the blood leaving a
parabronchus; Pv̄ = partial pressure of oxygen in the blood entering a parabronchus. Open arrow represents the change in the partial pressure of oxygen
in the gas from its entry into the parabronchus to its exit from the parabronchus; closed arrow represents the change in the partial pressure of oxygen in
the blood leaving the parabronchus from that in the blood entering the parabronchus. Note that the partial pressure of oxygen in the blood leaving the
parabronchus can be higher than that in the gas leaving the parabronchus (overlap of the arrows). (Modified from Piiper and Scheid, 1989).
efficiency of the aerodynamic valve decreases and some
gas may enter the medioventral secondary bronchi, pass
into the cranial air sacs, and fail to contribute to gas
exchange. Further, under conditions of low ventilation
rates, similar inefficiencies of valving may occur leading
to reduced gas exchange.
During expiration, aerodynamic valving also occurs
with gas from the caudal air sacs passing through the
mediodorsal secondary bronchi and into the paleopulmonic parabronchi. Mechanisms responsible for expiratory valving are different from those responsible for
inspiratory valving and depend upon gas flow velocity
but not gas density. The proposed mechanism responsible for producing expiratory valving is dynamic compression of the membranous intrapulmonary primary
bronchus, an action that would increase with increased
expiratory effort and increased flow velocity (Brown et
al., 1995, 1997). Compression of the intrapulmonary
primary bronchus would increase the resistance to flow
through the primary bronchus relative to that in the
mediodorsal secondary bronchi and the paleopulmonic
parabronchi, thus limiting the amount of gas that would
pass directly from the caudal air sacs to the trachea.
During normal breathing, the efficiency of the expiratory
valving is about 95%, i.e., only 5% of the gas from the
caudal air sacs is lost to the tracheal gas without passing
through the paleopulmonic parabronchi. This efficiency
appears to be greatly reduced under conditions of low
gas velocity, as would occur if the rate of ventilation
was low.
GAS EXCHANGE IN A PARABRONCHUS
Gas exchange in the avian lung can be best visualized
using a cross-current model (Powell and Scheid, 1989;
Piiper and Scheid, 1989) (Figure 4). The organization of
this type of gas exchanger is based on the convective
movement of gas through the parabronchial lumen,
diffusion of oxygen from this gas stream into the air
capillaries (which emanate from depressions, atria and
infundibula, in the parabronchial wall), diffusion of
carbon dioxide from the air capillaries into the convective
gas stream, entrance of the mixed venous blood from the
pulmonary arteries all along the periphery of the
parabronchial mantle with blood capillaries in intimate
contact with air capillaries, and collection of the arterialized blood in venules located immediately beneath the
epithelium of the lumen of the parabronchus (King and
McLelland, 1984; Abdalla, 1989). Thus, the convective
flow of gas is approximately 90° from the convective flow
of blood, and hence the cross-current designation of this
model.
As gas moves through a parabronchus, it continuously
loses oxygen to the blood and attains carbon dioxide from
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FEDDE
FIGURE 5. Gas exchange characteristics of the cross-current system in the bird lung during high ventilation. PI = partial pressure of oxygen entering
a parabronchus; PE = partial pressure of oxygen in the gas exiting a parabronchus; Pa = partial pressure of oxygen in the blood leaving a parabronchus;
Pv̄ = partial pressure of oxygen in the blood entering a parabronchus. Open arrow represents the change in the partial pressure of oxygen in the gas
from its entry into the parabronchus to its exit from the parabronchus; closed arrow represents the change in the partial pressure of oxygen in the blood
leaving the parabronchus from that in the blood entering the parabronchus. During a high ventilation rate, the partial pressure of oxygen in the blood
leaving the parabronchus can approach that in the gas entering the parabronchus. (Modified from Piiper and Scheid, 1989).
the blood. Blood entering a parabronchus at its origin
from a mediodorsal secondary bronchus equilibrates with
the high PO2 and low PCO2 in the gas while blood near the
end of the parabronchus equilibrates with a gas that
contains a much lower PO2 and higher PCO2. The arterial
PO2 in the blood that exits the lung is thus determined by
the admixture of blood from all of the capillaries along
each parabronchus (Figure 4). With this gas exchange
design, it is possible for the blood leaving the exchanger to
have a higher PO2 than that in the gas leaving the
exchanger. This signifies a gas exchanging system with an
inherently high efficacy.
If the parabronchial ventilation becomes high, as might
occur when the respiratory control system is stimulated in
hypoxic conditions, the arterial PO2 approaches to within
2 to 3 torr of the PO2 in the moist inspired tracheal gas
(Faraci et al., 1984a; Fedde et al., 1985) (Figure 5). The moist
inspired PO2 is the highest possible value that the arterial
PO2 could attain if the gas exchange system was perfect.
However, under conditions of high parabronchial ventilation, birds become extremely alkalotic and arterial PCO2
may decrease to 6 to 7 torr. The remarkable tolerance of at
least some birds (bar-headed geese) to hypocapnia and
hypoxia may result in part from their ability to maintain a
high cerebral blood flow (Faraci et al., 1985; Faraci and
Fedde, 1986) and to their lack of the pulmonary pressor
response (Faraci et al., 1984b).
On the other hand, if ventilation is lower than normal,
the PO2 in the parabronchial gas will quickly decrease to
that in the mixed venous blood (Figure 6). This will
produce an hypoxic environment for arterioles supplying
blood to this region of the parabronchus and they will
constrict. This will reduce the blood flow to this region,
minimizing the shunt and the arterial PO2 may be
maintained near normal. However, the increase in
pulmonary vascular resistance may increase pulmonary
arterial pressure. It would appear valuable to determine if
the pulmonary hypertension leading to right ventricular
failure and ascites in fast growing broilers (Odom, 1993;
Wideman and Bottje, 1993) could be explained by this
mechanism. It is well known that the smooth muscle in the
pulmonary arterial system in chickens, unlike that in barheaded geese, is very reactive to hypoxia (Burton et al.,
1968; Kadono and Besch, 1972; Besch and Kadono, 1978;
Faraci et al., 1984b), which induces pulmonary hypertension.
MECHANISMS OF DEFENSE AGAINST
INHALED FOREIGN PARTICLES
Filtration of Inspired Air
The upper respiratory system in the nasal cavity is well
designed to heat, humidify and filter the inspired air. The
SYMPOSIUM: INFECTIOUS POULTRY DISEASES
1135
FIGURE 6. Gas exchange characteristics of the cross-current system in the bird lung during a low ventilation rate. PI = partial pressure of oxygen
entering a parabronchus; PE = partial pressure of oxygen in the gas exiting a parabronchus; Pa = partial pressure of oxygen in the blood leaving a
parabronchus; Pv̄ = partial pressure of oxygen in the blood entering a parabronchus. Open arrow represents the change in the partial pressure of oxygen
in the gas from its entry into the parabronchus to its exit from the parabronchus; closed arrow represents the change in the partial pressure of oxygen in
the blood leaving the parabronchus from that in the blood entering the parabronchus. During a low ventilation rate, the partial pressure of oxygen in the
parabronchial gas approaches that in the mixed venous blood entering the parabronchus considerably before the gas has reached the end of the
parabronchus. This may produce hypoxic vasoconstriction of many arterioles at this end of the parabronchus, especially in those birds (such as
chickens) whole pulmonary vascular smooth muscle is reactive to hypoxia. The partial pressure of oxygen in the blood leaving the parabronchus may
be nearly normal if vasoconstriction occurs and shunted blood is minimized. (Modified from Piiper and Scheid, 1989).
expanded, mucous-covered epithelial surfaces possess
cilia that quickly (10 mm/min) carry the mucous sheet,
where inspired particulate material may impact, to the
pharynx where it can be swallowed and eliminated in the
feces (Bang, 1961, 1971; Mensah and Brain, 1982; Bang and
Wenzel, 1985). This part of the respiratory system forms
the first line of defense against large inspired particles
(down to about 4 mm) but does not entrap many particles
smaller than 0.2 mm (Hayter and Besch, 1974). It appears
that the trapped particles can be rapidly removed from the
nasal cavity but more studies are required in a variety of
species to determine the effectiveness of this site in the
respiratory system in preventing microorganisms in the
air stream from entering the trachea and lower parts of the
respiratory system.
Mucociliary Escalator in the Trachea
and Bronchi
The trachea, primary bronchi, and the roots of the
secondary bronchi are lined mostly with ciliated columnar
epithelial cells (McLelland, 1989a,b). Much of the remain-
ing epithelium of the secondary bronchi is cuboidal
(sometimes ciliated) or squamous in structure. The cilia
appear to move the overlying mucous layer in an oral
direction. The parabronchi are lined by unciliated cuboidal and squamous epithelium and, therefore, do not
possess a means of moving inhaled foreign particles
orally.
Mensah and Brain (1982) exposed chickens for 30 to 40
min to aerosol particles (median aerodynamic diameter of
0.45 mm) containing 99mTc-sulfur colloid. Although not
much radioactivity was in the trachea at the end of the
exposure, most was removed by 12 h after the end of
exposure. Likewise, a large fraction of the radioactivity
had been removed from the lungs within one hour after
exposure and a large accumulation of radioactivity had
occurred in the gastrointestinal tract. This study indicated
a rapid-phase clearance of the insoluble technetium from
the trachea and lungs to the feces. There was essentially no
radioactivity in the heart, kidneys, ovaries, or liver,
indicating the technetium had not entered the blood. The
study also indicated a slow-phase clearance of radioactive
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FEDDE
material that may have resulted from the phagocytotic
mechanisms discussed below.
The impact of poultry house pollutants on particulate
clearance from the respiratory system of birds remains
largely unknown (see Brown et al., 1997 for review).
However, any substance that reduces ciliary motility or
disrupts the ciliated epithelium could be expected to
adversely affect the resistance of birds to microorganisms
that normally enter their bodies via the respiratory
system.
Phagocytosis
Wandering macrophages are rarely found in the
healthy avian respiratory system (Toth and Siegel, 1986;
Klika et al., 1996). They can be induced to enter the air sacs
by injecting foreign substances (Freund’s adjuvant or
Sephadex G-100), disease producing organisms, and
spores (Aspergillus fumigatus) into their lumen (Ficken et
al., 1986; Kunkle and Rimler, 1996; Pruimboom et al., 1996).
These macrophages have strong phagocytic reactions to
many substances and organisms, and can be quickly
FIGURE 7. Electron micrographs showing phagocytosis of aerolized iron oxide particles by atrial epithelial cells in the parabronchus of a duck. A)
iron oxide particles entering the apical surface an atrial epithelial cell. Bar equals 0.25 mm. B) Phagosome (a) in an atrial epithelial cell containing iron
oxide and large amounts of trilaminar substance and (b) iron oxide particles with only small fragments of trilaminar substance. Bar equals 0.25 mm. C)
Atrial epithelial cell emptying iron oxide (arrow) into the subjacent interstitium through the basal surface of the cell. Bar equals 0.25 mm. D) Atrial
interstitial macrophage containing iron oxide particles (arrow). Bar equals 0.5 mm. (Reprinted from Respir. Physiol., 67:23–36, 1987, Stearns, R. C., G. M.
Barnas, M. Walski and J. D. Brain, Deposition and phagocytosis of inhaled particles in the gas exchange region of the duck,Anas platyrhynchos, with kind
permission of Elsevier Science-NL, Sara Burgerhartstraat 25, 1055 KV Amsterdam, The Netherlands).
SYMPOSIUM: INFECTIOUS POULTRY DISEASES
attracted into the respiratory system when the appropriate chemotactic substance is present (Toth et al., 1987; Toth
et al., 1988). However, airway macrophages may not be
responsible for maintaining a clean environment in the
respiratory system under normal circumstances.
When ducks were exposed to aerosols (aerodynamic
mass mean diameter of 0.18 mm) containing iron oxide
particles, these particles were found trapped within the
trilaminar substance coating the atria and infundibuli in
the parabronchi. The iron oxide particles were seen
entering the epithelial cells, in phagosomes within these
cells, passing from the epithelial cells into the interstitium,
and in interstitial macrophages (Stearns et al., 1987)
(Figure 7). These observations may explain why parabronchial macrophages are not usually seen in the avian lung:
each epithelial cell the region of atria and parts of the
infundibula can function as a macrophage and remove
foreign material that becomes embedded in the trilaminar
substance overlaying this region. Such a function would
act to protect the air capillaries from contamination. Also,
it is possible to explain the observations that the caudal
group of air sacs are those most prone to infections while
the cranial group of air sacs are less often affected. All of
the gas must pass through paleopulmonic parabronchi
prior to reaching the cranial air sacs, resulting in the
trapping and removal of most foreign particles. On the
other hand, the gas that enters the caudal group of air sacs
passes only through overventilated neopulmonic
parabronchi (Scheid et al., 1989) or directly into these air
sacs and, thereby, is not filtered to the same extent as the
gas reaching the cranial group of air sacs.
The mechanisms by which foreign particles are removed from the lungs after being engulfed by interstitial
macrophages are unknown. These cells may find their
way into the blood stream and thereby be carried to other
organs. Studies to define the disposition of these cells
would be useful to determine the involvement and
reaction of other organs in clearance of lung particulate
matter.
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