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Department of Anatomy and Physiology, College of Veterinary Medicine, Kansas State University,
Manhattan, Kansas 66506-5602
ABSTRACT The avian respiratory system exchanges of oxygen in the blood leaving the parabronchus can be
oxygen and carbon dioxide between the gas and the higher than that in the gas exiting this structure, giving
blood utilizing a relatively small, rigid, flow-through the avian lung a high gas exchange efficacy. The
lung, and a system of air sacs that act as bellows to relationship of the partial pressure of oxygen in the
move the gas through the lung. Gas movement through moist inspired gas to that in the blood leaving the lung
the paleopulmonic parabronchi, the main gas exchang- is dependent on the rate of ventilation. A low ventilation
ing bronchi, in the lung is in the same direction during rate may produce a low oxygen partial pressure in part
both inspiration and expiration, i.e., from the mediodor- of the parabronchus, thereby inducing hypoxic vasocon-
sal secondary bronchi to the medioventral secondary striction in the pulmonary arterioles supplying this
bronchi. During inspiration, acceleration of the gas at region.
the segmentum accelerans of the primary bronchus
Inhaled foreign particles are removed by nasal
increases gas velocity so it does not enter the medioven-
mucociliary action, by the mucociliary escalator in the
tral secondary bronchi. During expiration, airway
trachea, primary bronchi, and secondary bronchi. Small
resistance is increased in the intrapulmonary primary
bronchus because of dynamic compression causing gas particles that enter parabronchi appear to be phagocy-
to enter the mediodorsal secondary bronchi. Reduction tized by the epithelial cells in the atria and infundibu-
in air flow velocity may decrease the efficiency of this lum. These particles can be transported to interstitial
aerodynamic valving and thereby decrease the efficiency macrophages but the disposition of the particles from
of gas exchange. this site is unknown. The predominant site of respira-
The convective gas flow in the avian parabronchus is tory infections in the caudal air sacs, compared to other
orientated at a 90° angle with respect to the parabron- parts of the respiratory system, can be explained by the
chial blood flow; hence, the cross-current designation of gas flow pathway and the mechanisms present in the
this gas exchanger. With this design, the partial pressure 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 from the larynx and is sometimes very incompressible,
AVIAN RESPIRATORY SYSTEM as in ducks and geese, and sometimes easy to compress,
as in chickens. The trachea in some birds is extremely
IN THE BODY COELOM
long (sometimes longer than the entire body) and
The respiratory system in birds has the principal tortuous or coiled, as in the trumpet bird. The trachea
function of exchanging oxygen and carbon dioxide branches into two extrapulmonary primary bronchi,
between atmosphere and blood. It is also involved in each of which goes to a lung and its associated air sacs.
temperature regulation and phonation. It has these The lung is a relatively rigid structure that does not
features in common with the respiratory system of expand and retract with breathing; its function is to
mammals but it differs significantly in the anatomical provide a large surface area for gas exchange with the
arrangement of its parts (Figure 1). The respiratory blood and it does this in a very small space. The air sacs
system begins at the nares and has passages in the head function as bellows whose change in volume causes
that lead inhaled gas to the larynx. The trachea extends pressure differences across the lungs that result in gas
movement during inspiration and expiration. The air
1130
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; Dun-
cker, 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 respira-
tory system is presented in detail by King (1993) in the
Handbook of Avian Anatomy: Nomina Anatomica Avium.
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 appears to be greatly reduced under conditions of low
gas may enter the medioventral secondary bronchi, pass gas velocity, as would occur if the rate of ventilation
into the cranial air sacs, and fail to contribute to gas was low.
exchange. Further, under conditions of low ventilation
rates, similar inefficiencies of valving may occur leading GAS EXCHANGE IN A PARABRONCHUS
to reduced gas exchange.
During expiration, aerodynamic valving also occurs Gas exchange in the avian lung can be best visualized
with gas from the caudal air sacs passing through the using a cross-current model (Powell and Scheid, 1989;
mediodorsal secondary bronchi and into the paleopul- Piiper and Scheid, 1989) (Figure 4). The organization of
monic parabronchi. Mechanisms responsible for expira- this type of gas exchanger is based on the convective
tory valving are different from those responsible for movement of gas through the parabronchial lumen,
inspiratory valving and depend upon gas flow velocity diffusion of oxygen from this gas stream into the air
but not gas density. The proposed mechanism responsi- capillaries (which emanate from depressions, atria and
ble for producing expiratory valving is dynamic com- infundibula, in the parabronchial wall), diffusion of
pression of the membranous intrapulmonary primary carbon dioxide from the air capillaries into the convective
bronchus, an action that would increase with increased gas stream, entrance of the mixed venous blood from the
expiratory effort and increased flow velocity (Brown et pulmonary arteries all along the periphery of the
al., 1995, 1997). Compression of the intrapulmonary parabronchial mantle with blood capillaries in intimate
primary bronchus would increase the resistance to flow contact with air capillaries, and collection of the arterial-
through the primary bronchus relative to that in the ized blood in venules located immediately beneath the
mediodorsal secondary bronchi and the paleopulmonic epithelium of the lumen of the parabronchus (King and
parabronchi, thus limiting the amount of gas that would McLelland, 1984; Abdalla, 1989). Thus, the convective
pass directly from the caudal air sacs to the trachea. flow of gas is approximately 90° from the convective flow
During normal breathing, the efficiency of the expiratory of blood, and hence the cross-current designation of this
valving is about 95%, i.e., only 5% of the gas from the model.
caudal air sacs is lost to the tracheal gas without passing As gas moves through a parabronchus, it continuously
through the paleopulmonic parabronchi. This efficiency loses oxygen to the blood and attains carbon dioxide from
1134 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 On the other hand, if ventilation is lower than normal,
from a mediodorsal secondary bronchus equilibrates with the PO2 in the parabronchial gas will quickly decrease to
the high PO2 and low PCO2 in the gas while blood near the that in the mixed venous blood (Figure 6). This will
end of the parabronchus equilibrates with a gas that produce an hypoxic environment for arterioles supplying
contains a much lower PO2 and higher PCO2. The arterial blood to this region of the parabronchus and they will
PO2 in the blood that exits the lung is thus determined by constrict. This will reduce the blood flow to this region,
the admixture of blood from all of the capillaries along minimizing the shunt and the arterial PO2 may be
each parabronchus (Figure 4). With this gas exchange maintained near normal. However, the increase in
design, it is possible for the blood leaving the exchanger to pulmonary vascular resistance may increase pulmonary
have a higher PO2 than that in the gas leaving the arterial pressure. It would appear valuable to determine if
exchanger. This signifies a gas exchanging system with an the pulmonary hypertension leading to right ventricular
inherently high efficacy. failure and ascites in fast growing broilers (Odom, 1993;
If the parabronchial ventilation becomes high, as might Wideman and Bottje, 1993) could be explained by this
occur when the respiratory control system is stimulated in mechanism. It is well known that the smooth muscle in the
hypoxic conditions, the arterial PO2 approaches to within pulmonary arterial system in chickens, unlike that in bar-
2 to 3 torr of the PO2 in the moist inspired tracheal gas headed geese, is very reactive to hypoxia (Burton et al.,
(Faraci et al., 1984a; Fedde et al., 1985) (Figure 5). The moist 1968; Kadono and Besch, 1972; Besch and Kadono, 1978;
inspired PO2 is the highest possible value that the arterial Faraci et al., 1984b), which induces pulmonary hyperten-
PO2 could attain if the gas exchange system was perfect. sion.
However, under conditions of high parabronchial ventila-
tion, birds become extremely alkalotic and arterial PCO2
may decrease to 6 to 7 torr. The remarkable tolerance of at MECHANISMS OF DEFENSE AGAINST
least some birds (bar-headed geese) to hypocapnia and INHALED FOREIGN PARTICLES
hypoxia may result in part from their ability to maintain a
high cerebral blood flow (Faraci et al., 1985; Faraci and
Filtration of Inspired Air
Fedde, 1986) and to their lack of the pulmonary pressor The upper respiratory system in the nasal cavity is well
response (Faraci et al., 1984b). 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 ing epithelium of the secondary bronchi is cuboidal
cilia that quickly (10 mm/min) carry the mucous sheet, (sometimes ciliated) or squamous in structure. The cilia
where inspired particulate material may impact, to the appear to move the overlying mucous layer in an oral
pharynx where it can be swallowed and eliminated in the direction. The parabronchi are lined by unciliated cuboi-
feces (Bang, 1961, 1971; Mensah and Brain, 1982; Bang and dal and squamous epithelium and, therefore, do not
Wenzel, 1985). This part of the respiratory system forms possess a means of moving inhaled foreign particles
the first line of defense against large inspired particles orally.
(down to about 4 mm) but does not entrap many particles Mensah and Brain (1982) exposed chickens for 30 to 40
smaller than 0.2 mm (Hayter and Besch, 1974). It appears min to aerosol particles (median aerodynamic diameter of
that the trapped particles can be rapidly removed from the 0.45 mm) containing 99mTc-sulfur colloid. Although not
nasal cavity but more studies are required in a variety of
much radioactivity was in the trachea at the end of the
species to determine the effectiveness of this site in the
exposure, most was removed by 12 h after the end of
respiratory system in preventing microorganisms in the
exposure. Likewise, a large fraction of the radioactivity
air stream from entering the trachea and lower parts of the
respiratory system. 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
Mucociliary Escalator in the Trachea
a rapid-phase clearance of the insoluble technetium from
and Bronchi the trachea and lungs to the feces. There was essentially no
The trachea, primary bronchi, and the roots of the radioactivity in the heart, kidneys, ovaries, or liver,
secondary bronchi are lined mostly with ciliated columnar indicating the technetium had not entered the blood. The
epithelial cells (McLelland, 1989a,b). Much of the remain- study also indicated a slow-phase clearance of radioactive
1136 FEDDE
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 1137
attracted into the respiratory system when the appropri- goose lungs depends on gas density and velocity. Respir.
ate chemotactic substance is present (Toth et al., 1987; Toth Physiol. 70:287–300.
et al., 1988). However, airway macrophages may not be Besch, E. L., and H. Kadono, 1978. Cardiopulmonary responses
responsible for maintaining a clean environment in the to acute hypoxia in domestic fowl. Pages 71–78 in:
Respiratory Function in Birds, Adult and Embryonic. J.
respiratory system under normal circumstances.
Piiper, ed. Springer-Verlag, Berlin, Germany.
When ducks were exposed to aerosols (aerodynamic Brackenbury, J. H., 1987. Ventilation of the lung-air sac system.
mass mean diameter of 0.18 mm) containing iron oxide Pages 39–69 in: Bird Respiration. Vol. I. T. J. Seller, ed. CRC
particles, these particles were found trapped within the Press, Boca Raton, FL.
trilaminar substance coating the atria and infundibuli in Brown, R. E., C. E. Kovacs, J. P. Butler, N. Wang, J. Lehr, and R. B.
the parabronchi. The iron oxide particles were seen Banzett, 1995. The avian lung: is there an aerodynamic
entering the epithelial cells, in phagosomes within these expiratory valve? J. Exp. Biol. 198:2349–2357.
cells, passing from the epithelial cells into the interstitium, Brown, R. E., J. D. Brain, and N. Wang, 1997. The avian
and in interstitial macrophages (Stearns et al., 1987) respiratory system: a unique model for studies of respira-
(Figure 7). These observations may explain why parabron- tory toxicosis and for monitoring air quality. Environ. Hlth.
Perspect. 105:188–200.
chial macrophages are not usually seen in the avian lung:
Burton, R. R., E. L. Besch, and A. H. Smith, 1968. Effect of chronic
each epithelial cell the region of atria and parts of the
hypoxia on the pulmonary arterial blood pressure of the
infundibula can function as a macrophage and remove chicken. Am. J. Physiol. 214:1438–1442.
foreign material that becomes embedded in the trilaminar Butler, J. P., R. B. Banzett, and J. J. Fredberg, 1988. Inspiratory
substance overlaying this region. Such a function would valving in avian bronchi: aerodynamic considerations.
act to protect the air capillaries from contamination. Also, Respir. Physiol. 72:241–256.
it is possible to explain the observations that the caudal Dotterweich, H., 1936. Die Atmung der Vögel. Z. vergl. Physiol.
group of air sacs are those most prone to infections while 23:744–770.
the cranial group of air sacs are less often affected. All of Duncker, H.-R., 1971. The lung air sac system of birds. A
the gas must pass through paleopulmonic parabronchi contribution to the functional anatomy of the respiratory
prior to reaching the cranial air sacs, resulting in the apparatus. Ergeb. Anat. Entwicklungsgesch. 45(6):1–171.
trapping and removal of most foreign particles. On the Faraci, F. M., and M. R. Fedde, 1986. Regional circulatory
responses to hypocapnia and hypercapnia in bar-headed
other hand, the gas that enters the caudal group of air sacs
geese. Am. J. Physiol. 250:R499–R504.
passes only through overventilated neopulmonic Faraci, F. M., D. L. Kilgore, Jr., and M. R. Fedde, 1984a. Oxygen
parabronchi (Scheid et al., 1989) or directly into these air delivery to the heart and brain during hypoxia: Pekin duck
sacs and, thereby, is not filtered to the same extent as the vs. bar-headed goose. Am. J. Physiol. 247:R69–R75.
gas reaching the cranial group of air sacs. Faraci, F. M., D. L. Kilgore, Jr., and M. R. Fedde, 1984b.
The mechanisms by which foreign particles are re- Attenuated pulmonary pressor response to hypoxia in bar-
moved from the lungs after being engulfed by interstitial headed geese. Am. J. Physiol. 247:R402–R403.
macrophages are unknown. These cells may find their Faraci, F. M., D. L. Kilgore, Jr., and M. R. Fedde, 1985. Blood flow
way into the blood stream and thereby be carried to other distribution during hypocapnic hypoxia in Pekin ducks and
organs. Studies to define the disposition of these cells bar-headed geese. Respir. Physiol. 61:21–30.
would be useful to determine the involvement and Fedde, M. R., 1986. Respiration. Pages 191–220 in: Avian
Physiology. 4th ed. P. D. Sturkie, ed. Springer-Verlag, New
reaction of other organs in clearance of lung particulate
York, NY.
matter. Fedde, M. R., 1987. Respiratory muscles. Pages 3–37 in: Bird
Respiration. Vol. I. T. J. Seller, ed. CRC Press, Boca Raton,
REFERENCES FL.
Fedde, M. R., F. M. Faraci, D. L. Kilgore, Jr., G. H. Cardinet, III,
Abdalla, M. A., 1989. The blood supply to the lung. Pages and A. Chatterjee, 1985. Cardiopulmonary adaptations in
281–306 in: Form and Function in Birds. Vol. 4. A. S. King birds for exercise at high altitude. Pages 149–163 in:
and J. McLelland, ed. Academic Press, London, UK. Circulation, Respiration, and Metabolism. R. Gilles, ed.
Bang, B. G., 1961. The surface pattern of the nasal mucosa and its Springer-Verlag, Berlin, Germany.
relation to mucous flow—a study of chicken and herring Ficken, M. D., J. F. Edwards, and J. C. Lay, 1986. Induction,
gull nasal mucosae. J. Morphol. 109:57–71. collection, and partial characterization of induced respira-
Bang, B. G., 1971. Functional anatomy of the olfactory system in tory macrophages in the turkey. Avian Dis. 30:766–771.
23 orders of birds. Acta Anat. 79(Suppl. 58):1–76. Hayter, R. B., and E. L. Besch, 1974. Airborne-particle deposition
Bang, B. G., and B. M. Wenzel, 1985. Nasal cavity and olfactory in the respiratory tract of chickens. Poultry Sci. 53:
system. Pages 195–225 in: Form and Function in Birds. Vol. 1507–1511.
3. A. S. King and J. McLelland, ed. Academic Press, London, Kadono, H., and E. L. Besch, 1972. Effect of progressive hypoxia
UK. on blood pressure in domestic fowl. Fed. Proc. 31:815.
Banzett, R. B., C. S. Nations, N. Wang, J. J. Fredberg, and J. P. (Abstr.)
Butler, 1991. Pressure profiles show features essential to King, A. S., 1966. Structural and functional aspects of the avian
aerodynamic valving in geese. Respir. Physiol. 84:295–309. lungs and air sacs. Pages 171–267 in: International Review of
Banzett, R. B., J. P. Butler, C. S. Nations, G. M. Barnas, J. L. Lehr, General and Experimental Zoology. W.J.L. Felts and R. J.
and J. H. Jones, 1987. Inspiratory aerodynamic valving in Harrison, ed. Academic Press, New York, NY.
1138 FEDDE
King, A. S., 1989. Functional anatomy of the syrinx. Pages Piiper, J., and P. Scheid, 1989. Respiration and gas exchange in
105–192 in: Form and Function in Birds. Vol. 4. A. S. King birds. Pages 153–162 in: Physiology of Cold Adaptation in
and J. McLelland, ed. Academic Press, London, UK. Birds. C. Bech and R. E. Reinertsen, ed. Plenum Press, New
King, A. S., 1993. Apparatus respiratorius. Pages 257–299 in: York, NY.
Handbook of Avian Anatomy: Nomina Anatomica Avium. Powell, F. L., and P. Scheid, 1989. Physiology of gas exchange in
2nd ed. J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, the avian respiratory system. Pages 393–437 in: Form and
and J. C. Vanden Berge, ed. Nuttall Ornithological Club, No. Function in Birds. Vol. 4. A. S. King and J. McLelland, ed.
23, Cambridge, MA. Academic Press, London, UK.
King, A. S., and J. McLelland, 1984. Respiratory system. Pages Pruimboom, I. M., R. B. Rimler, M. R. Ackermann, and K. A.
110–144 in: Birds, Their Structure and Function. 2nd ed. Brogden, 1996. Capsular hyaluronic acid-mediated adhe-
Baillière Tindall, London, UK. sion of Pasteurella multocida to turkey air sac macrophages.
King, A. S., and S. S. White, 1975. Aves respiratory system. Pages Avian Dis. 40:887–893.
1883–1918 in: Sisson and Grossman’s The Anatomy of the Scheid, P., and J. Piiper, 1989. Respiratory mechanics and air flow
Domestic Animals. 5th ed. Vol. 2. R. Getty, ed. W. B. in birds. Pages 369–391 in: Form and Function in Birds. Vol.
Saunders, Philadelphia, PA. 4. A. S. King and J. McLelland, ed. Academic Press, London,
Klika, E., D. W. Scheuermann, M.H.A. DeGroodt-Lasseel, I. UK.
Bazantova, and A. Switka, 1996. Pulmonary macrophages in Scheid, P., M. R. Fedde, and J. Piiper, 1989. Gas exchange and air-
birds (barn owl, Tyto tyto alba), domestic fowl (Gallus gallus f. sac composition in the unanesthetized, spontaneously
domestica), quail (Coturnix coturnix), and pigeons (Columbia breathing goose. J. Exp. Biol. 142:373–385.
livia). Anat. Rec. 246:87–97. Stearns, R. C., G. M. Barnas, M. Walski, and J. D. Brain, 1987.
Kuethe, D. O., 1988. Fluid mechanical valving of air flow in bird Deposition and phagocytosis of inhaled particles in the gas
lungs. J. Exp. Biol. 136:1–12. exchange region of the duck, Anas platyrhynchos. Respir.
Kunkle, R. A., and R. B. Rimler, 1996. Pathology of acute Physiol. 67:23–36.
aspergillosis in turkeys. Avian Dis. 40:875–886.
Toth, T. E., and P. B. Siegel, 1986. Cellular defense of the avian
Maina, J. N., 1989. The morphometry of the avian lung. Pages
respiratory tract: Paucity of free-residing macrophages in
307–368 in: Form and Function in Birds. Vol. 4. A. S. King
the normal chicken. Avian Dis. 30:67–75.
and J. McLelland, ed. Academic Press, London, UK.
Toth, T. E., P. Seigel, and H. Veit, 1987. Cellular defense of the
McLelland, J., 1989a. Larynx and trachea. Pages 69–103 in: Form
avian respiratory system. Influx of phagocytes: Elicitation
and Function in Birds. Vol. 4. A. S. King and J. McLelland,
versus activation. Avian Dis. 31:861–867.
ed. Academic Press, London, UK.
Toth, T. E., R. H. Pyle, T. Caceci, P. B. Siegel, and D. Ochs, 1988.
McLelland, J., 1989b. Anatomy of the lungs and air sacs. Pages
Cellular defense of the avian respiratory system: Influx and
221–279 in: Form and Function in Birds. Vol. 4. A. S. King
and J. McLelland, ed. Academic Press, London, UK. nonopsonic phagocytosis by respiratory phagocytes acti-
Mensah, G. A., and J. B. Brain, 1982. Deposition and clearance of vated by Pasteurella multocida. Infect. Immun. 56:1171–1179.
inhaled aerosol in the respiratory tract of chickens. J. Appl. Wang, N., R. B. Banzett, C. S. Nations, and F. A. Jenkins, Jr., 1992.
Physiol. 53:1423–1428. An aerodynamic valve in the avian primary bronchus. J.
Meyer, M., H. Worth, and P. Scheid, 1976. Gas-blood CO2 Exp. Zool. 262:441–445.
equilibrium in parabronchial lungs of birds. J. Appl. Physiol. Wang, N., R. B. Banzett, J. P. Butler, and J. J. Fredberg, 1988. Bird
41:302–309. lung models show that convective inertia effects inspiratory
Nickel, R., A. Schummer, E. Seiferle, W. G. Siller, and P.A.L. aerodynamic valving. Respir. Physiol. 73:111–124.
Wight, 1977. Pages 62–69 in: Anatomy of the Domestic Birds. Wideman, R. F., Jr., and W. G. Bottje, 1993. Current understand-
Springer-Verlag, New York, NY. ing of the ascites syndrome and future research directions.
Odom, T. W., 1993. Ascites syndrome: overview and update. Pages 1–20 in: Nutrition and Technical Symposium Proceed-
Poult. Dig. 52(1):14–22. ings. Novus International, Inc., St. Louis, MO.