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Respiratory mechanics in the bird
Comp. B&hem. Physiol.,1973, Vol. 44A, pp. 599 to 611. Pergamon Press. Printed in Great Britain
RESPIRATORY
MECHANICS
JOHN Sub-Department
IN THE BIRD
H. BRACKENBURY
of Veterinary Anatomy, University of Cambridge (Received
14 April 1972)
Abstract-l.
Air sac and coelomic pressures were measured in chickens and geese. 2. The coelomic pressure wave is composed of the air sac wave together with a wave originating from the stretching or bulging of internal septa during respiration. 3. A model is presented which features the overall mechanical characteristics of the respiratory system, and which generates pressures that are related to each other in the manner of those in the normal bird.
INTRODUCTION SINCE the fundamental work of Rohrer (1919) an d more especially in the past 20 years, respiratory mechanics has been extensively studied in mammals. Comparison of the respiratory system with linear visco-elastic models has permitted a relatively simple treatment to be made of the external breathing mechanism (Mead & MilicEmili, 1964). Recently the chief concerns have been the following:
(a) to establish the values of the various physical parameters of the respiratory system relevant to the classical theory (Otis et al., 1950; Brody, 1954; Brody et al., 1956; Agostoni et al., 1959; Brody et al., 1959; Crosfill & Widdicombe, 1961; Mead, 1961; Amdur & Mead, 1968); (b) measurement of the pressure in the pleural and peritoneal spaces (Agostoni et al., 1960; Agostoni & d’Angelo, 1969; Agostoni et al., 1969); (c) the work involved in breathing, reviewed by Otis (1964) ; (d) the possible effects of coelomic pressures upon haemodynamics, especially venous return (Brecher & Mixter, 1953 ; Guyton, 1963 ; Mead & Whittenberger, 1964). Corresponding studies in the bird have been meagre. In his review of comparative respiratory mechanics Spells (1969) does not mention the bird. Sturkie (1965) gives information about early workers who measured air sac pressures. The most useful work is that of Cohn & Shannon (1968) which gives air sac pressures and respiratory flow readings, and also calculations of average inspiratory and expiratory airway resistances. Scheid & Piiper (1969) determined the respiratory compliance of the fowl. Recently information has been published concerning intrapulmonic pressures and flows (Brackenbury, 1971a, b; Bretz & SchmidtNielsen, 1971; Scheid & Piiper, 1971) and pressure differentials existing between 599
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JOHN H. BRACKENBURY
air sacs (Brackenbury, 1971a; King & Molony, 1971). No details concerning intracoelomic respiratory pressures have yet been published. There is a tacit assumption that the coelom of the bird, and consequently the pressure regime within it, constitutes a unity owing to the absence of a definite diaphragm homologous to that of the mammal, and notwithstanding the fact that there is extensive partitioning of the body cavity. The general layout of the avian respiratory system is quite different from that of the mammal. The lungs are relatively inexpansible structures and are closely associated with the vertebral parts of ribs 3-7. Each contains a complicated system of interconnected air passages some of which lead into air sacs beyond the lungs (Akester, 1960). Although the bird has no muscular diaphragm in the mammalian sense, its coelomic cavity is sub-divided in a complicated way by a number of septa, some of which have muscular attachments, and which have only been described in general terms (Goodrich, 1958; Goodchild, 1970). A brief account of these septa and their relationship to the air sacs is given (Fig. l), as far as it is relevant to the experimental work which follows. The pulmonary diaphragm covers the ventral surface of each lung and is attached by small muscle bundles to the middle of ribs 3-7. It forms the roof of the anterior and part of the posterior thoracic air sacs. The oblique septum runs between the ventral surfaces of thoracic vertebrae 3-7 and their Sterno-costal junctions (Fig. 1). It forms the medial boundary of the anterior and posterior thoracic air sacs on each side; the lateral boundary of which consists of the body wall. The posthepatic septum arises from the posterior border of each lung and attaches transversely to the ANTERhqRRs-ZRACIC POSTERIOR THORACIC
LIVER IN ANTERIOR COELOMIC COMPARTMENT
FIG. 1. Diagram to show the anatomical relations between the coelom, internal septa and air sacs in the bird.
RESPIRATORY MECHANICS IN THE BIRD
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ventral body wall at the level of the caudal end of the sternum. It forms the caudal boundary of each posterior abdominal compartment, and cannot be regarded as being in any way homologous with the mammalian diaphragm. The abdominal air sacs are situated behind the posthepatic septum and are attached to the dorsal body wall. Compared with the mammal the avian situation might be expected to be influenced by four factors: (a) the lung is relatively immobile during respiration and is separated from the rest of the body cavity by the thoracic air sacs and by the dorsal part of the posthepatic septum (Goodrich, 1958); (b) the absence of a muscular diaphragm which might suggest that intracoelomic pressures would be everywhere synchronous and similar; (c) expiration is active by virtue of the contraction of the abdominal muscles and the intercostal muscles (Kadono et al., 1963; Fedde et al., 1964), which are essential in eupnea to the adequate emptying of the abdominal air sacs; (d) owing to the presence of air sacs connected directly to the atmosphere there may be no end-expiratory negative (or positive) pressure in the coelom. However, if the septa bordering the coelomic compartments are elastic then this might not necessarily be the case.
MATERIALS
AND METHODS
Experiments were performed upon a total of fifty anaesthetized and unanaesthetized domesticus) and geese (Anser anser). Air sac and coelomic pressures and chickens (Gab respiratory air flows were recorded from standing and supine animals breathing voluntarily through the nares and anaesthetized where necessary with a 1 : 1 mixture of 40% urethane and pentobarbitone sodium. This was administered intravenously. Grass PT5 volumetric air pressure transducers were used to measure air pressures and, in conjunction with a Fleisch pneumotachograph, air flows. Coelomic pressures were monitored via Statham P23AC liquid manometers. Both air and liquid manometers had damping less than critical. An electromagnetic instrument was devised to record sternal velocities (Fig. 2). It has a very high frequency response, from OH, upwards, and presented negligible impedance to breathing movements. All signals were displayed on a Grass Model 7 polygraph. A Grass 7PlO integrator was used for the electronic integration of the signals representing sternal velocity, air sac pressure and air flow.
RESULTS
The main purpose of this paper is to develop a theory of respiratory mechanics in the bird. This has been done by correlating coelomic and air sac pressures, respiratory air flow and flow resistance, and changes in body volume aa measured by movements of the sternum. Coelomic pressure In spite of its subdivision by the various septa, pressures having similar waveforms can be recorded from all parts of the body cavity except the heart,
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JOHN H. BRACKENBURY
pericardium, lungs and air sacs. This means that respiratory waves recorded from the peritoneum, the veins and from within the alimentary canal all represent coelomic pressure (Fig. 3b).
INPUT VOLTAGE
FIG. 2. Velocity meter. The application of a d.c. voltage, a 9 V battery in this case, to the primary coil gives rise to a magnetic flux around the metal circuit and across the air gap. A voltage proportional to the velocity of movement of the plunger in the Z-direction is induced in the secondary coil cutting magnetic flux in the air gap. The plunger, which is placed on the sternum of the bird, is constrained to a single movement direction by the compliant spring and the central metal shaft upon which the primary coil is wound. Output voltage is fed into the 7Pl preamplifier of a Grass polygraph.
The coelomic wave shows a continuous rise during expiration and a continuous fall during inspiration. It is convex on the upstroke and concave on the downstroke. The total magnitude of the wave is about twice that of the pressure wave inside the adjacent air sacs. In the posterior abdominal compartment, depending on how close is the point of measurement to an air sac, it is also possible to record an air sac wave. In addition to the dynamic pressure there is a hydrostatic pressure which is related to the level within the viscera at which the particular point of measurement lies. The exact value of coelomic pressure with respect to zero or atmospheric is therefore dependent upon the site of recording. It is more positive the lower in the body this point is.
RESPIRATORY
MECHANICS
IN
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Air sac pressure Pressures throughout the whole of the air-filled part of the respiratory system have almost exactly the same waveform, although there is a progressive diminution in their magnitude from the air sacs to the atmosphere. This means that for most purposes pressure changes in one part of the system characterize changes throughout the entire system. There is no resting level different to atmospheric.
lull
Ii,0 -
cm
t
FIG. 3. Coelomic and air sac pressures in a standing chicken. cm
Hz0
FIG. 4. Pressure within the interclavicular air sac of a standing chicken.
Air sac pressure has the same waveform as airflow since the pressure generated in each air sac is the motive force bringing about flow. Figure 4 shows the pressure wave in a standing chicken. Inspiration begins before the pressure from the preceding expiration has reached zero. The initial decline in pressure is rapid, reflecting the rapid reversal in airflow, then it shallows and pressure begins to return towards zero before the onset of the next expiration. Expiration starts as a sudden rise in pressure to zero and beyond, which may be accounted for by the elastic recoil of the thoracic cage. Thereafter the pressure may continue to rise gently until the next inspiration supervines or it may reach an early peak and fall towards the baseline, according to the prolongation of expiratory effort in particular
604
JOHN H. BRACKENBURY
cycles. Pressure values vary below 1 cm H,O in the positive phase and a little more negative than - 1 cm H,O in the negative phase. There are slight differences between the pressures measured in the standing and the supine bird. In the supine animal the expiratory phase assumes the greater total pressure excursion, owing to the weight of the sternum and pectoral muscles. The expiratory pressure, after an initial rapid rise to a maximum positive caused by the inertial recoil of the chest, declines to zero in an almost exponential fashion. According to the degree of anaesthesia in supine birds expiration is variably passive and largely so in deep anaesthesia. Indeed the mechanical efficiency of the abdominal muscles is much reduced as a result of the collapse of the abdominal air sacs. Respiratory
airJEoevand jlow resistance
Air flow directly reflects the rate of expansion or contraction of the body cavity which may be measured by movements of the sternum. It might therefore be expected that air sac pressure would have a waveform the same as that of the velocity of the sternum. Simultaneous recordings have shown this to be the case , I set
,
Air sac
pr8ssure
SternoI
velocity
FIG. 5. Comparison between the air sac pressure (a) and the sternal velocity (b).
Resistance to air flow is caused by a combination of the viscosity and the inertia of air particles, of which the former is the more important at normal flow rates. This ainvay resistance can be calculated at any stage in the respiratory cycle by dividing the instantaneous air sac pressure by the airflow recorded at the mouth and nares. Such calculations have shown that viscous resistance, as measured by the gradient of the pressure/flow curve at zero flow, is approximately 0.007 cm H,O/ml per set in the goose, and 0.015 cm H,O/ml per set in the chicken. Overall resistance to air flow increases slightly at higher flow rates owing to the increasing inertial reactance of the air, which is represented by the horizontal distance between the dotted and full lines in Fig. 6. It will be seen from Fig. 6 that throughout the physiological range, between 0 and about 60 ml/set, the inertial effect is relatively small.
RESPIRATORY
MECHANICS
IN
THE
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605
Relationship between air sac and coelomic pressures
In the preceding two sections the relationship was noted between air flow, air sac pressure and sternal velocity. The integral of any one of these waves, which measures the cumulated area (with time) between them and the baseline, has a form
t:.::: O-6 0.5
‘
0.4
0.3
0.2
0.‘
0.1
0.2
0.3
O-4 0.5
0.6
PRESSURE CM Hz0 /
AA
t 50
FIG. 6. The air sac pressure/respiratory flow relationship throughout respiration determined from dynamic records. Different symbols represent determinations from separate respiratory waves. Expiratory resistance increases with flow rate owing to the inertia of the air. The zero flow resistance is indicated, being in this case O-007 cm H,O/ml per sec. The inspiratory loop is most probably caused by variation in the size of the glottis, and is bisected by the line Raw continued through the origin.
very similar to that of the respiratory volume, or the degree of expansion or contraction of the body cavity. Such a wave is also found to resemble in several respects the coelomic wave, chiefly in that they both rise and fall continuously in
606
JOHN H. BRACKENBURY
expiration and inspiration. Moreover, if the air sac pressure is subtracted from the coelomic pressure by using a differential manometer, the resulting wave resembles more exactly the respiratory volume (Fig. 7). The coelomic wave is therefore a composition of pressures which derive on the one hand from the air sac and on the other from a factor within the coelom which generates pressures in a more positive direction during expiration and in a more negative direction during inspiration. What this factor actually is will be dealt with in the Discussion.
I
set
FIG. 7. (a). Pressure differential between the coelom and the air sac throughout respiration. Coelomic pressure in this case was recorded from an abdominal air sac whose connexions to the lung were blocked. The dotted line represents the respiratory volume, obtained by integrating the air sac waveform. (b). Air sac pressure.
DISCUSSION
General mechanics of respiration
Respiratory efforts in the bird cause the air sacs to bring about a controlled movement of air through the lungs by their bellows-like action. The resultant flow will depend upon the force generated by the respiratory muscles and on the nature of the impedance to movement offered by the entire respiratory system. In quiet breathing, if we ignore the inertia of the moving tissues and the air, this impedance consists of two elements: the viscous resistance to air flow and tissue movement, Rrs; and the compliance of the rib cage and abdominal wall, as well as of the internal septa, Crs. Since the lung is relatively inexpansible its contribution to the compliance will be negligible. Each of the parameters Rrs and Crs can be estimated. One component of Rrs, the gaseous resistance of the airway, Raw, has already been calculated by relating airflow at the mouth and nares to air sac pressure (Fig. 6). The other component,
RESPIRATORY
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tissue resistance, Rw + ab, is located predominantly in the ribs, sternum and the associated muscles and ligaments. Respiratory compliance is measured by noting the volume change of the animal for a given pressure rise anywhere in the body cavity when an apnoeiac or recently dead bird is inflated by air. Using this method Scheid & Piiper (1969) estimated the average compliance in the fowl to be 9.5 ml/cm H,O. This value is large, and comparable to that of man. Compliance ultimately relates the volume of that part of the body which is dilatable with air to the extent to which that part is elastic. In all vertebrates the main site of elasticity is the rib cage and its associated structures. In mammals in particular the only dilatable chamber is of course the thorax which contains the lungs. As regards birds, however, the whole of the coelom is expansible since both anterior and posterior compartments of the abdomen contain air sacs. Moreover, the lung air sac system is open-connected throughout and incipient pressure changes in any one part can be reduced by transmission to every other part. Another important parameter which stems from the existence of an impedance is the respiratory time-constant, Trs. This is given by the product of Rrs and Crs. Its value, whether it is large or small, determines how rapidly the system will respond to the application of muscular effort, thereby bringing about movement of air into or out of the body. If Trs is sufficiently small, and the chest is sufficiently elastic, as is the case in mammals, then the energy stored in the thoracic wall during inspiration is large enough in itself to effect adequately rapid expiration. In the bird, however, Trs is increased relative to the mammal on two accounts: firstly, owing to the large compliance of the respiratory system, and secondly, owing to the large airway resistance. Consequently the bird must have recourse to active expiration as well as active inspiration. The respiratory mechanism is not necessarily any the less efficient for its having biphasic muscular activity, since in those animals practising passive expiration a proportionally greater inspiratory effort is required in order to stretch the elastic elements in the chest wall. When considering higher ventilation rates and especially those characteristic of panting, it becomes important to take into account not only those parts of the respiratory impedance already referred to viz. Rrs and Crs, but also a third component: the tissue inertance, Mrs. A certain combination of Mrs and Crs is observed to give for any particular animal a defined frequency of panting at which the greatest minute volume of air is shifted for the least amount of work done, This combination is given by &l/M rs C rs ) an d is called the natural or resonant frequency. In adult chickens, for example, the panting frequency is generally 4-5 counts/set. During panting the respiratory system is driven almost sinusoidally at the characteristic frequency. Inserted between sequences of quiet breathing and true panting are trains of waves which are a hybrid of two consecutive pants. Further use of this shallow in the work/frequency graph is made during “clucking” in the chicken. Here once again the rate of individual “clucks” is the same as the natural frequency.
JOHN H. BRACKENBURY
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Pressure relationships Air sac pressure reflects quite faithfully the flow of air through the respiratory system. At quiet breathing rates the coelomic wave shows morphological characteristics which are 180” out of phase with the air sac wave. This is demonstrated by the fact that it has a component resembling the time-integral of the air sac wave. Accordingly, in order to explain both the size and phase differences between the two waves factors other than simple (linear) viscous resistances must be invoked. The mass of the tissues of the body wall and viscera is not responsible since the same relations between waves are seen in both standing and supine birds. However, the internal septa of the body cavity, despite their being highly tensile and only weakly elastic, must undergo some deformation throughout respiration. Moreover, the tension in an element undergoing stretch varies in direct proportion to its change in length. In the particular context of the bird’s coelomic membranes length is related directly to respiratory volume (or total change in body volume.) Therefore, if the tension within such a membrane were transmitted to the adjacent tissues in the form of a pressure, then the coelomic wave would show, in addition to the air sac pressure which separates the coelom from the atmosphere, another pressure varying in form very much in the way of the respiratory volume. Results have shown this to be the case (Fig. 7). The former component would be proportional in value to the airflow; the latter to the respiratory volume, the integral of air flow. If we take for example the oblique septum (Fig. 8), pressure inside the anterior abdominal cavity medial to the septum falls continuously during inspiration as it is stretched, or displaced, to an extent proportional to the respiratory volume, or the downward displacement of the keel. The posthepatic septum will also be pulled or displaced as the abdominal sac fills. Pulling tensions from the septa will be transmitted to the viscera. During expiration coelomic pressure gradually rises to a
PULMONARY APONEUROSI
OBLIQUE SEPTUM
STERNUM
ikl
FIG. 8. Transverse section of the bird in the region just behind the heart.
RESPIRATORY
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IN THE BIRD
609
value commensurate with the normal configuration of the septa at end-expiration (which may or may not be zero). Complementing the effect of the septa, throughout expiration as the abdominal sac becomes emptied and the abdominal muscles squash the viscera in the posterior abdominal cavity, a steadily rising pressure will be transmitted across the posthepatic septum to the anterior abdominal viscera. Figure 9 shows a model of the avian respiratory system which epitomizes the anatomical relations between the coelom, septa and air sacs. It generates, upon the application of appropriate forces representing muscular effort, a pressure in the coelom which is a combination of that in the air sac and another resembling the integral of the air sac pressure. In other words, a combination of pressures proportional respectively to air flow and respiratory volume. At higher respiratory frequencies, where flow rates are large but tidal volume is small, there will be minimal stretching, or bulging, of the septa, and the predominating influence of the viscosity of the air in the sacs will result in both coelomic and air sac pressure waves being similar in phase and form. This, too, has been observed experimentally. COSTAL PUMP
INSPllfATION 1
STERNAL VELOCITY
AIRWAY RESISTANCE
)
1 EXPIRATION I-I
ABDOMINAL PUMP
FIG. 9. Model representing the respiratory system of the bird and emphasizing the relation between the coelom, viscera, the internal septa and the air sacs. Two pumps represent inspiratory and expiratory muscular effort. The product of rib cage elasticity and rib cage and airway resistance gives the overall time constant of the respiratory system, Trs = Rrs Crs.
610
JOHN H. BRACKENBURY SUMMARY
1. Simultaneous recordings were made from chickens and geese of coelomic and air sac pressures, air flow at the mouth and sternal velocity. 2. Air sac pressure, air flow and sternal velocity wave forms are very similar and all represent the rate of change of body volume. 3. The coelomic wave is a composition of the air sac wave and that of change in body volume which can be obtained by time-integrating the wave form of air sac pressure, air flow or sternal velocity. 4. A model is presented which reduces the respiratory system to a combination of two types of physical components: resistance and compliance; and which takes into account the stretching or bulging of the internal septa of the body cavity. The model generates wave forms in the air sac and coelom which in their essential features closely resemble those obtained by experimental recording. Acknowledgement-This Council.
work was supported by a grant from the Agricultural Research
REFERENCES AGOSTONIE. & D’ANGELOE. (1969) Thickness and pressure of the pleural fluid at various heights and with various hydrothoraces. Resp. Physiol. 6, 330-342. AGOSTONIE., MISEROCCHI G. & BONNANIM. U. (1969) Thickness and pressure of the pleural liquid in some mammals. Resp. Physiol. 6, 245-256. AGOSTONIE., SANT’AMBROGIO G. & DEL PORTILLOCARRASCO H. (1960) Electromyography of the diaphragm in man and trans-diaphragmatic pressure. r. appl. Physiol. 15, 10931097. AGOSTONIE., THIMM F. F. & FENN W. 0. (1959) Comparative features of the mechanics of breathing. r. appl. Physiol, 14, 679-687. AKESTERA. R. (1960) The comparative anatomy of the respiratory pathways in the domestic fowl, pigeon and duck. r. Anat. 94, 487-505. AMDURM. 0. & MEAD J. (1958) Mechanics of respiration in unanaesthetised guinea-pigs. Am.J. Physiol. 192, 364-368. BRACKENBURY J. H. (1971a) Airflow dynamics within the avian lung. Resp. Physiol. 13, 319-329. BRACKENBURY J. H. (1971b) Some pressure flow relations within the avian respiratory system. r. Anat. 108, 609-610. BRECHERG. A. & MIXTER G., JR. (1953) Effect of respiratory movements on superior caval flow under normal and abnormal conditions. Am. J. Physiol. 171, 710-711. BRETZW. L. & SCHMIDT-NIELSENK. (1971) Bird respiration: flow patterns in the duck lung. J. exp. Biol. 54, 103-118. BRODY A. W. (1954) Mechanical compliance and resistance of the lung-thorax calculated from flow recorded during passive expiration. Am. J. Physiol. 178, 189-196. BRODY A. W., DUBOIS A. B., NISELL 0. I. & ENGELBERGJ. (1956) Natural frequency, damping factor and inertance of chest-lung system in cats. Am.J. Physiol. 186, 142-148. BRODY A. W., CONNOLLYJ., JR. & WANDERH. (1959) Influence of abdominal muscles, mesenteric viscera and liver on respiratory mechanics. J. appl. Physiol. 14, 121-128. COHNJ. E. and SHANNONR. (1968) Respiration in unanaesthetised geese. Resp. Physiol. 5, 259-268. CROSFILLM. L. & WIDDICOMBEJ. G. (1961) Physical characteristics of chest and lungs and the work of breathing in different mammalian species. J. Physiol., Lond. 158, l-14.
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FEDDE M. R., BURGERR. E. & KITCHELL R. L. (1964) Electromyographical studies of the effects of bodily position and anaesthesia on the activity of the respiratory muscles of the domestic cock. Poult. Sci. 43, 839-846. GOODCHILDW. M. (1970) Differentiation of body cavity and air sacs of Gallus domesticus post mortem and location in vivo. BY. ‘j’. Pot&. Sci. II, 209-215. GOODRICHE. S. (1958) Studies on the Structure and Development of Vertebrates, Vol. II. Dover, New York. GUYTON A. T. (1963) Venous return. In Handbook of Physiology, Sect. 2, Circulation, (Edited by HAMILTONW. F. & Dow P.) Vol. II, Chapt. 32. Am. Physiol. Sot., Washington, D.C. KADONOH., OKADAT. & ONO K. (1963) Electromyographic studies on the respiratory muscles of the chicken. Poult. Sci. 42, 121-128. MEAD J. (1961) Mechanical properties of lungs. PhysioZ. Rev. 41, 281-330. MEADJ. & MILIC-EMILI J. (1964) Theory and methodology in respiratory mechanics with a glossary of symbols. In Handbook of Physiology, Sec. 3, Respiration (Edited by FENN W. 0. & RAHN H.), Vol. 1, Chapt. 11. Am. Physiol. Sot. Washington, D.C. MEADJ. & WHITTENBERCER J. L. (1964) Lung inflation and haemodynamics. In Handbook of Physiology. Sect. 3, Respiration (Edited by FENN W. 0. & RAHNH.), Vol. 1, Chapt. 18. Am. Physiol, Sot. Washington D.C. OTIS A. B. (1964) The work of breathing. In Handbook of PhysioZogy, Sect. 3, Respiration, (Edited by FENN W. 0. & RAHN H.), Vol. 1, Chapt. 17. Am. Physiol. Sot., Washington, D.C. OTIS A. B., FENN W. 0. & RAHN H. (1950) Mechanics of breathing in man. J. appE. Physiol. 2, 592-607. ROHRER F. (1916) Der Zusammenhang der Atemkrafte und ihrer Abhangigkeit von Dehnungszustand der Atemsorgan. Pjltigers arch. ges. Physiol. 165, 419-444. SCHEIDP. & PIIPER J. (1969) Volume, ventilation and compliance of the respiratory system in the domestic fowl. Resp. Physiol. 6, 298-308. SCHEIDP. & PIIPER J. (1971) Direct measurement of the pathway of respired gas in duck lungs. Resp. Physiol. 11,308-314. SPELLS K. E. (1969) Comparative studies in lung mechanics based on a survey of literature data. Resp. Physiol. 8, 37-57. STURKIEP. D. (1965) Avian Physiology, 2nd edn. Cornell University Press, Ithaca, New York. Key Words Index-Coelomic pressure; air sac pressure; respiratory airRow; airflow resistance; respiratory mechanics; pressure relationships; bird respiration; Anser anser; Gallus domesticus.
RESPIRATORY
MECHANICS
JOHN Sub-Department
IN THE BIRD
H. BRACKENBURY
of Veterinary Anatomy, University of Cambridge (Received
14 April 1972)
Abstract-l.
Air sac and coelomic pressures were measured in chickens and geese. 2. The coelomic pressure wave is composed of the air sac wave together with a wave originating from the stretching or bulging of internal septa during respiration. 3. A model is presented which features the overall mechanical characteristics of the respiratory system, and which generates pressures that are related to each other in the manner of those in the normal bird.
INTRODUCTION SINCE the fundamental work of Rohrer (1919) an d more especially in the past 20 years, respiratory mechanics has been extensively studied in mammals. Comparison of the respiratory system with linear visco-elastic models has permitted a relatively simple treatment to be made of the external breathing mechanism (Mead & MilicEmili, 1964). Recently the chief concerns have been the following:
(a) to establish the values of the various physical parameters of the respiratory system relevant to the classical theory (Otis et al., 1950; Brody, 1954; Brody et al., 1956; Agostoni et al., 1959; Brody et al., 1959; Crosfill & Widdicombe, 1961; Mead, 1961; Amdur & Mead, 1968); (b) measurement of the pressure in the pleural and peritoneal spaces (Agostoni et al., 1960; Agostoni & d’Angelo, 1969; Agostoni et al., 1969); (c) the work involved in breathing, reviewed by Otis (1964) ; (d) the possible effects of coelomic pressures upon haemodynamics, especially venous return (Brecher & Mixter, 1953 ; Guyton, 1963 ; Mead & Whittenberger, 1964). Corresponding studies in the bird have been meagre. In his review of comparative respiratory mechanics Spells (1969) does not mention the bird. Sturkie (1965) gives information about early workers who measured air sac pressures. The most useful work is that of Cohn & Shannon (1968) which gives air sac pressures and respiratory flow readings, and also calculations of average inspiratory and expiratory airway resistances. Scheid & Piiper (1969) determined the respiratory compliance of the fowl. Recently information has been published concerning intrapulmonic pressures and flows (Brackenbury, 1971a, b; Bretz & SchmidtNielsen, 1971; Scheid & Piiper, 1971) and pressure differentials existing between 599
600
JOHN H. BRACKENBURY
air sacs (Brackenbury, 1971a; King & Molony, 1971). No details concerning intracoelomic respiratory pressures have yet been published. There is a tacit assumption that the coelom of the bird, and consequently the pressure regime within it, constitutes a unity owing to the absence of a definite diaphragm homologous to that of the mammal, and notwithstanding the fact that there is extensive partitioning of the body cavity. The general layout of the avian respiratory system is quite different from that of the mammal. The lungs are relatively inexpansible structures and are closely associated with the vertebral parts of ribs 3-7. Each contains a complicated system of interconnected air passages some of which lead into air sacs beyond the lungs (Akester, 1960). Although the bird has no muscular diaphragm in the mammalian sense, its coelomic cavity is sub-divided in a complicated way by a number of septa, some of which have muscular attachments, and which have only been described in general terms (Goodrich, 1958; Goodchild, 1970). A brief account of these septa and their relationship to the air sacs is given (Fig. l), as far as it is relevant to the experimental work which follows. The pulmonary diaphragm covers the ventral surface of each lung and is attached by small muscle bundles to the middle of ribs 3-7. It forms the roof of the anterior and part of the posterior thoracic air sacs. The oblique septum runs between the ventral surfaces of thoracic vertebrae 3-7 and their Sterno-costal junctions (Fig. 1). It forms the medial boundary of the anterior and posterior thoracic air sacs on each side; the lateral boundary of which consists of the body wall. The posthepatic septum arises from the posterior border of each lung and attaches transversely to the ANTERhqRRs-ZRACIC POSTERIOR THORACIC
LIVER IN ANTERIOR COELOMIC COMPARTMENT
FIG. 1. Diagram to show the anatomical relations between the coelom, internal septa and air sacs in the bird.
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ventral body wall at the level of the caudal end of the sternum. It forms the caudal boundary of each posterior abdominal compartment, and cannot be regarded as being in any way homologous with the mammalian diaphragm. The abdominal air sacs are situated behind the posthepatic septum and are attached to the dorsal body wall. Compared with the mammal the avian situation might be expected to be influenced by four factors: (a) the lung is relatively immobile during respiration and is separated from the rest of the body cavity by the thoracic air sacs and by the dorsal part of the posthepatic septum (Goodrich, 1958); (b) the absence of a muscular diaphragm which might suggest that intracoelomic pressures would be everywhere synchronous and similar; (c) expiration is active by virtue of the contraction of the abdominal muscles and the intercostal muscles (Kadono et al., 1963; Fedde et al., 1964), which are essential in eupnea to the adequate emptying of the abdominal air sacs; (d) owing to the presence of air sacs connected directly to the atmosphere there may be no end-expiratory negative (or positive) pressure in the coelom. However, if the septa bordering the coelomic compartments are elastic then this might not necessarily be the case.
MATERIALS
AND METHODS
Experiments were performed upon a total of fifty anaesthetized and unanaesthetized domesticus) and geese (Anser anser). Air sac and coelomic pressures and chickens (Gab respiratory air flows were recorded from standing and supine animals breathing voluntarily through the nares and anaesthetized where necessary with a 1 : 1 mixture of 40% urethane and pentobarbitone sodium. This was administered intravenously. Grass PT5 volumetric air pressure transducers were used to measure air pressures and, in conjunction with a Fleisch pneumotachograph, air flows. Coelomic pressures were monitored via Statham P23AC liquid manometers. Both air and liquid manometers had damping less than critical. An electromagnetic instrument was devised to record sternal velocities (Fig. 2). It has a very high frequency response, from OH, upwards, and presented negligible impedance to breathing movements. All signals were displayed on a Grass Model 7 polygraph. A Grass 7PlO integrator was used for the electronic integration of the signals representing sternal velocity, air sac pressure and air flow.
RESULTS
The main purpose of this paper is to develop a theory of respiratory mechanics in the bird. This has been done by correlating coelomic and air sac pressures, respiratory air flow and flow resistance, and changes in body volume aa measured by movements of the sternum. Coelomic pressure In spite of its subdivision by the various septa, pressures having similar waveforms can be recorded from all parts of the body cavity except the heart,
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pericardium, lungs and air sacs. This means that respiratory waves recorded from the peritoneum, the veins and from within the alimentary canal all represent coelomic pressure (Fig. 3b).
INPUT VOLTAGE
FIG. 2. Velocity meter. The application of a d.c. voltage, a 9 V battery in this case, to the primary coil gives rise to a magnetic flux around the metal circuit and across the air gap. A voltage proportional to the velocity of movement of the plunger in the Z-direction is induced in the secondary coil cutting magnetic flux in the air gap. The plunger, which is placed on the sternum of the bird, is constrained to a single movement direction by the compliant spring and the central metal shaft upon which the primary coil is wound. Output voltage is fed into the 7Pl preamplifier of a Grass polygraph.
The coelomic wave shows a continuous rise during expiration and a continuous fall during inspiration. It is convex on the upstroke and concave on the downstroke. The total magnitude of the wave is about twice that of the pressure wave inside the adjacent air sacs. In the posterior abdominal compartment, depending on how close is the point of measurement to an air sac, it is also possible to record an air sac wave. In addition to the dynamic pressure there is a hydrostatic pressure which is related to the level within the viscera at which the particular point of measurement lies. The exact value of coelomic pressure with respect to zero or atmospheric is therefore dependent upon the site of recording. It is more positive the lower in the body this point is.
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Air sac pressure Pressures throughout the whole of the air-filled part of the respiratory system have almost exactly the same waveform, although there is a progressive diminution in their magnitude from the air sacs to the atmosphere. This means that for most purposes pressure changes in one part of the system characterize changes throughout the entire system. There is no resting level different to atmospheric.
lull
Ii,0 -
cm
t
FIG. 3. Coelomic and air sac pressures in a standing chicken. cm
Hz0
FIG. 4. Pressure within the interclavicular air sac of a standing chicken.
Air sac pressure has the same waveform as airflow since the pressure generated in each air sac is the motive force bringing about flow. Figure 4 shows the pressure wave in a standing chicken. Inspiration begins before the pressure from the preceding expiration has reached zero. The initial decline in pressure is rapid, reflecting the rapid reversal in airflow, then it shallows and pressure begins to return towards zero before the onset of the next expiration. Expiration starts as a sudden rise in pressure to zero and beyond, which may be accounted for by the elastic recoil of the thoracic cage. Thereafter the pressure may continue to rise gently until the next inspiration supervines or it may reach an early peak and fall towards the baseline, according to the prolongation of expiratory effort in particular
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cycles. Pressure values vary below 1 cm H,O in the positive phase and a little more negative than - 1 cm H,O in the negative phase. There are slight differences between the pressures measured in the standing and the supine bird. In the supine animal the expiratory phase assumes the greater total pressure excursion, owing to the weight of the sternum and pectoral muscles. The expiratory pressure, after an initial rapid rise to a maximum positive caused by the inertial recoil of the chest, declines to zero in an almost exponential fashion. According to the degree of anaesthesia in supine birds expiration is variably passive and largely so in deep anaesthesia. Indeed the mechanical efficiency of the abdominal muscles is much reduced as a result of the collapse of the abdominal air sacs. Respiratory
airJEoevand jlow resistance
Air flow directly reflects the rate of expansion or contraction of the body cavity which may be measured by movements of the sternum. It might therefore be expected that air sac pressure would have a waveform the same as that of the velocity of the sternum. Simultaneous recordings have shown this to be the case , I set
,
Air sac
pr8ssure
SternoI
velocity
FIG. 5. Comparison between the air sac pressure (a) and the sternal velocity (b).
Resistance to air flow is caused by a combination of the viscosity and the inertia of air particles, of which the former is the more important at normal flow rates. This ainvay resistance can be calculated at any stage in the respiratory cycle by dividing the instantaneous air sac pressure by the airflow recorded at the mouth and nares. Such calculations have shown that viscous resistance, as measured by the gradient of the pressure/flow curve at zero flow, is approximately 0.007 cm H,O/ml per set in the goose, and 0.015 cm H,O/ml per set in the chicken. Overall resistance to air flow increases slightly at higher flow rates owing to the increasing inertial reactance of the air, which is represented by the horizontal distance between the dotted and full lines in Fig. 6. It will be seen from Fig. 6 that throughout the physiological range, between 0 and about 60 ml/set, the inertial effect is relatively small.
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Relationship between air sac and coelomic pressures
In the preceding two sections the relationship was noted between air flow, air sac pressure and sternal velocity. The integral of any one of these waves, which measures the cumulated area (with time) between them and the baseline, has a form
t:.::: O-6 0.5
‘
0.4
0.3
0.2
0.‘
0.1
0.2
0.3
O-4 0.5
0.6
PRESSURE CM Hz0 /
AA
t 50
FIG. 6. The air sac pressure/respiratory flow relationship throughout respiration determined from dynamic records. Different symbols represent determinations from separate respiratory waves. Expiratory resistance increases with flow rate owing to the inertia of the air. The zero flow resistance is indicated, being in this case O-007 cm H,O/ml per sec. The inspiratory loop is most probably caused by variation in the size of the glottis, and is bisected by the line Raw continued through the origin.
very similar to that of the respiratory volume, or the degree of expansion or contraction of the body cavity. Such a wave is also found to resemble in several respects the coelomic wave, chiefly in that they both rise and fall continuously in
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expiration and inspiration. Moreover, if the air sac pressure is subtracted from the coelomic pressure by using a differential manometer, the resulting wave resembles more exactly the respiratory volume (Fig. 7). The coelomic wave is therefore a composition of pressures which derive on the one hand from the air sac and on the other from a factor within the coelom which generates pressures in a more positive direction during expiration and in a more negative direction during inspiration. What this factor actually is will be dealt with in the Discussion.
I
set
FIG. 7. (a). Pressure differential between the coelom and the air sac throughout respiration. Coelomic pressure in this case was recorded from an abdominal air sac whose connexions to the lung were blocked. The dotted line represents the respiratory volume, obtained by integrating the air sac waveform. (b). Air sac pressure.
DISCUSSION
General mechanics of respiration
Respiratory efforts in the bird cause the air sacs to bring about a controlled movement of air through the lungs by their bellows-like action. The resultant flow will depend upon the force generated by the respiratory muscles and on the nature of the impedance to movement offered by the entire respiratory system. In quiet breathing, if we ignore the inertia of the moving tissues and the air, this impedance consists of two elements: the viscous resistance to air flow and tissue movement, Rrs; and the compliance of the rib cage and abdominal wall, as well as of the internal septa, Crs. Since the lung is relatively inexpansible its contribution to the compliance will be negligible. Each of the parameters Rrs and Crs can be estimated. One component of Rrs, the gaseous resistance of the airway, Raw, has already been calculated by relating airflow at the mouth and nares to air sac pressure (Fig. 6). The other component,
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tissue resistance, Rw + ab, is located predominantly in the ribs, sternum and the associated muscles and ligaments. Respiratory compliance is measured by noting the volume change of the animal for a given pressure rise anywhere in the body cavity when an apnoeiac or recently dead bird is inflated by air. Using this method Scheid & Piiper (1969) estimated the average compliance in the fowl to be 9.5 ml/cm H,O. This value is large, and comparable to that of man. Compliance ultimately relates the volume of that part of the body which is dilatable with air to the extent to which that part is elastic. In all vertebrates the main site of elasticity is the rib cage and its associated structures. In mammals in particular the only dilatable chamber is of course the thorax which contains the lungs. As regards birds, however, the whole of the coelom is expansible since both anterior and posterior compartments of the abdomen contain air sacs. Moreover, the lung air sac system is open-connected throughout and incipient pressure changes in any one part can be reduced by transmission to every other part. Another important parameter which stems from the existence of an impedance is the respiratory time-constant, Trs. This is given by the product of Rrs and Crs. Its value, whether it is large or small, determines how rapidly the system will respond to the application of muscular effort, thereby bringing about movement of air into or out of the body. If Trs is sufficiently small, and the chest is sufficiently elastic, as is the case in mammals, then the energy stored in the thoracic wall during inspiration is large enough in itself to effect adequately rapid expiration. In the bird, however, Trs is increased relative to the mammal on two accounts: firstly, owing to the large compliance of the respiratory system, and secondly, owing to the large airway resistance. Consequently the bird must have recourse to active expiration as well as active inspiration. The respiratory mechanism is not necessarily any the less efficient for its having biphasic muscular activity, since in those animals practising passive expiration a proportionally greater inspiratory effort is required in order to stretch the elastic elements in the chest wall. When considering higher ventilation rates and especially those characteristic of panting, it becomes important to take into account not only those parts of the respiratory impedance already referred to viz. Rrs and Crs, but also a third component: the tissue inertance, Mrs. A certain combination of Mrs and Crs is observed to give for any particular animal a defined frequency of panting at which the greatest minute volume of air is shifted for the least amount of work done, This combination is given by &l/M rs C rs ) an d is called the natural or resonant frequency. In adult chickens, for example, the panting frequency is generally 4-5 counts/set. During panting the respiratory system is driven almost sinusoidally at the characteristic frequency. Inserted between sequences of quiet breathing and true panting are trains of waves which are a hybrid of two consecutive pants. Further use of this shallow in the work/frequency graph is made during “clucking” in the chicken. Here once again the rate of individual “clucks” is the same as the natural frequency.
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Pressure relationships Air sac pressure reflects quite faithfully the flow of air through the respiratory system. At quiet breathing rates the coelomic wave shows morphological characteristics which are 180” out of phase with the air sac wave. This is demonstrated by the fact that it has a component resembling the time-integral of the air sac wave. Accordingly, in order to explain both the size and phase differences between the two waves factors other than simple (linear) viscous resistances must be invoked. The mass of the tissues of the body wall and viscera is not responsible since the same relations between waves are seen in both standing and supine birds. However, the internal septa of the body cavity, despite their being highly tensile and only weakly elastic, must undergo some deformation throughout respiration. Moreover, the tension in an element undergoing stretch varies in direct proportion to its change in length. In the particular context of the bird’s coelomic membranes length is related directly to respiratory volume (or total change in body volume.) Therefore, if the tension within such a membrane were transmitted to the adjacent tissues in the form of a pressure, then the coelomic wave would show, in addition to the air sac pressure which separates the coelom from the atmosphere, another pressure varying in form very much in the way of the respiratory volume. Results have shown this to be the case (Fig. 7). The former component would be proportional in value to the airflow; the latter to the respiratory volume, the integral of air flow. If we take for example the oblique septum (Fig. 8), pressure inside the anterior abdominal cavity medial to the septum falls continuously during inspiration as it is stretched, or displaced, to an extent proportional to the respiratory volume, or the downward displacement of the keel. The posthepatic septum will also be pulled or displaced as the abdominal sac fills. Pulling tensions from the septa will be transmitted to the viscera. During expiration coelomic pressure gradually rises to a
PULMONARY APONEUROSI
OBLIQUE SEPTUM
STERNUM
ikl
FIG. 8. Transverse section of the bird in the region just behind the heart.
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value commensurate with the normal configuration of the septa at end-expiration (which may or may not be zero). Complementing the effect of the septa, throughout expiration as the abdominal sac becomes emptied and the abdominal muscles squash the viscera in the posterior abdominal cavity, a steadily rising pressure will be transmitted across the posthepatic septum to the anterior abdominal viscera. Figure 9 shows a model of the avian respiratory system which epitomizes the anatomical relations between the coelom, septa and air sacs. It generates, upon the application of appropriate forces representing muscular effort, a pressure in the coelom which is a combination of that in the air sac and another resembling the integral of the air sac pressure. In other words, a combination of pressures proportional respectively to air flow and respiratory volume. At higher respiratory frequencies, where flow rates are large but tidal volume is small, there will be minimal stretching, or bulging, of the septa, and the predominating influence of the viscosity of the air in the sacs will result in both coelomic and air sac pressure waves being similar in phase and form. This, too, has been observed experimentally. COSTAL PUMP
INSPllfATION 1
STERNAL VELOCITY
AIRWAY RESISTANCE
)
1 EXPIRATION I-I
ABDOMINAL PUMP
FIG. 9. Model representing the respiratory system of the bird and emphasizing the relation between the coelom, viscera, the internal septa and the air sacs. Two pumps represent inspiratory and expiratory muscular effort. The product of rib cage elasticity and rib cage and airway resistance gives the overall time constant of the respiratory system, Trs = Rrs Crs.
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1. Simultaneous recordings were made from chickens and geese of coelomic and air sac pressures, air flow at the mouth and sternal velocity. 2. Air sac pressure, air flow and sternal velocity wave forms are very similar and all represent the rate of change of body volume. 3. The coelomic wave is a composition of the air sac wave and that of change in body volume which can be obtained by time-integrating the wave form of air sac pressure, air flow or sternal velocity. 4. A model is presented which reduces the respiratory system to a combination of two types of physical components: resistance and compliance; and which takes into account the stretching or bulging of the internal septa of the body cavity. The model generates wave forms in the air sac and coelom which in their essential features closely resemble those obtained by experimental recording. Acknowledgement-This Council.
work was supported by a grant from the Agricultural Research
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FEDDE M. R., BURGERR. E. & KITCHELL R. L. (1964) Electromyographical studies of the effects of bodily position and anaesthesia on the activity of the respiratory muscles of the domestic cock. Poult. Sci. 43, 839-846. GOODCHILDW. M. (1970) Differentiation of body cavity and air sacs of Gallus domesticus post mortem and location in vivo. BY. ‘j’. Pot&. Sci. II, 209-215. GOODRICHE. S. (1958) Studies on the Structure and Development of Vertebrates, Vol. II. Dover, New York. GUYTON A. T. (1963) Venous return. In Handbook of Physiology, Sect. 2, Circulation, (Edited by HAMILTONW. F. & Dow P.) Vol. II, Chapt. 32. Am. Physiol. Sot., Washington, D.C. KADONOH., OKADAT. & ONO K. (1963) Electromyographic studies on the respiratory muscles of the chicken. Poult. Sci. 42, 121-128. MEAD J. (1961) Mechanical properties of lungs. PhysioZ. Rev. 41, 281-330. MEADJ. & MILIC-EMILI J. (1964) Theory and methodology in respiratory mechanics with a glossary of symbols. In Handbook of Physiology, Sec. 3, Respiration (Edited by FENN W. 0. & RAHN H.), Vol. 1, Chapt. 11. Am. Physiol. Sot. Washington, D.C. MEADJ. & WHITTENBERCER J. L. (1964) Lung inflation and haemodynamics. In Handbook of Physiology. Sect. 3, Respiration (Edited by FENN W. 0. & RAHNH.), Vol. 1, Chapt. 18. Am. Physiol, Sot. Washington D.C. OTIS A. B. (1964) The work of breathing. In Handbook of PhysioZogy, Sect. 3, Respiration, (Edited by FENN W. 0. & RAHN H.), Vol. 1, Chapt. 17. Am. Physiol. Sot., Washington, D.C. OTIS A. B., FENN W. 0. & RAHN H. (1950) Mechanics of breathing in man. J. appE. Physiol. 2, 592-607. ROHRER F. (1916) Der Zusammenhang der Atemkrafte und ihrer Abhangigkeit von Dehnungszustand der Atemsorgan. Pjltigers arch. ges. Physiol. 165, 419-444. SCHEIDP. & PIIPER J. (1969) Volume, ventilation and compliance of the respiratory system in the domestic fowl. Resp. Physiol. 6, 298-308. SCHEIDP. & PIIPER J. (1971) Direct measurement of the pathway of respired gas in duck lungs. Resp. Physiol. 11,308-314. SPELLS K. E. (1969) Comparative studies in lung mechanics based on a survey of literature data. Resp. Physiol. 8, 37-57. STURKIEP. D. (1965) Avian Physiology, 2nd edn. Cornell University Press, Ithaca, New York. Key Words Index-Coelomic pressure; air sac pressure; respiratory airRow; airflow resistance; respiratory mechanics; pressure relationships; bird respiration; Anser anser; Gallus domesticus.