THE ANATOMY of the THORAX in RELATION to the FLOW of TIDAL AIR Lecture Delivered at the Symposium Held by the Faculty of Anesthetists on 21St February, 1953 by G

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THE ANATOMY OF THE THORAX IN RELATION TO THE FLOW OF TIDAL AIR Lecture delivered at the symposium held by the Faculty of Anesthetists on 21st February, 1953 by G. Causey, F.R.C.S. Sir William Collins Professor of Human and Comparative Anatomy, Royal College of Surgeons. That the thoracic cavity increases in volume during inspiration and decreases in volume during expiration is accepted by all, but exactly how this change in volume is brought about is by no means clear. On almost all points, whether of rib movements, of intercostal muscle activity, or of the quantitative contribution by the diaphragm, different and often opposing views are expressed. It may seem that enough has been written on the subject already, but I believe that, with the increasing use of muscular relaxants and controlled respiration in man, the search for a logically consistent hypothesis to explain the respiratory movements is not only an intellectual exercise, but a practical necessity. The bony skeleton of the thorax is formed by the thoracic vertebra, 12 pairs of ribs and their costal cartilages, and the sternum. The gaps in this bony skeleton are filled with fibrous and muscular tissues-the intercostal muscles and membranes at the side, the diaphragm below and the suprapleural (Sibson's) fascia, backed by the scalene muscles above. To the inside of this cavity, the outer surface of the lung is firmly held by the surface tension of the pleural fluid that needs a force of some 3600 mm.hg. per sq. cm. to break it. Every increase in the volume of this cavity is transmitted to the underlying lung and, assuming that the airway is patent, will draw air into the alveoli. The important features of this bony skeleton were discussed by Sir Arthur Keith in his contribution to " Further Advances in Physiology (1909). 1. The anterior concavity of the thoracic spine-part of the primary curvature and present before the appearance of the cervical and lumbar curves. 2. The obliquity of the thoracic inlet formed by the body of the first thoracic vertebra, the first pair of ribs and the upper border of the manubrium sterni. This slope is really well marked. The head of the first rib articulates with the upper part of the body of the 1st thoracic vertebra, and the upper border of the 1st costal cartilage is on the level of the disc between the 2nd and 3rd thoracic vertebra, so that there is a vertical drop of two vertebral bodies and one intervertebral disc between the head of the first rib and the manubrium. The antero-posterior distance is only some 5 cm. so that the tangent of the angle of declivity approaches unity and the angle itself approaches 45°. 127 G. CAUSEY The second feature of the thoracic inlet is the continuity of the first costal cartilage with both its rib and the manubrium. There is no joint cavity either costochondral or chondro-manibrial. The third point about the thoracic inlet is the extent ofthe attachment of scalenus anterior and medius muscles to the rib. The usual way of thinking of these structures is to consider the superior surface of the first rib with a large artery and a large vein crossing it, then to make room for a lower trunk of the brachial plexus and have very little space left for the attachment of the scalene muscles. A more accurate impression is obtained by attaching a half cone of muscle to the superior surface of the first rib and then splitting the half cone into two very unequal parts by running the sub- clavian artery through the muscle. The fascia on the deep surface of the muscle cone is attached by a variable amount of areolar tissue to the fascia on the outer surface of the pleura over the apex of the lung, the whole fibrous element forming the suprapleural fascia. 3. The joint between the manubrium and body of the sternum. This joint is symphysial in structure, a fibrocartilaginous union sometimes having cavitation in the centre. The movement at this joint is small but of considerable significance in connexion with elevation of the thoracic inlet so that the manubrium is raised and comes to lie further forward, and the angle between the manubrium and body of the sternum is straightened out. 4. The ribs can be divided into four groups: (a) 1st rib; (b) ribs 2, 3, 4, 5, 6, and 7 (a and b are together the vertebro-sternal ribs); (c) ribs 8, 9 and 10, the vertebrochondral ribs, and (d) 11 and 12, the floating ribs. (a), the first rib, has been already discussed in relation to the thoracic inlet. (b), the 2nd, 3rd, 4th, 5th, 6th and 7th ribs, articulate with two vertebra, one transverse process, and one costal cartilage, and the costal cartilage has itself a diarthrodial articulation with the side of the sternum. The same is true of (c), the 8th, 9th and 10th ribs, except that these cartilages articulate with each other and indirectly with the sternum. But between the articulations there is this other essential difference: the facet on the transverse process for articulation with 2, 3, 4, 5, 6 and 7 is concave, whereas on 8, 9 and 10 it is flat. Fig. 1 shows this marked difference between the facet on the transverse process of the 3rd and 9th thoracic vertebra from the same vertebral column; the change in shape of the joint surfaces is a part of the overall change of function in these sets of ribs. (d), the 11th and 12th ribs, are functionally a part of the abdominal wall; during inspiration their intercostal spaces increase in size as the musculature relaxes. The volume of the thoracic cavity can be increased by the increase of any or all of its three axes. We must therefore consider (1) those factors increasing the height, that is, movements of the diaphragm and thoracic inlet; (2) those factors increasing the antero-posterior dimension, that is the forward displacement of the sternum and its attached ribs and the 128 THE ANATOMY OF THE THORAX IN RELATION TO THE FLOW OF TIDAL AIR straightening of the thoracic vertebral column and (3) those factors which increase the transverse axis of the chest, the upward and outward movements of the ribs.

Fig. 1. These movements occur, of course, in combination. The elevation of the thoracic inlet by the scalenes and sterno-mastoid throws the whole sternum forward as well as increasing the height of the thorax. The increase in height of the thorax is, however, most closely connected with the movements of the diaphragm. At each inspiration the diaphragm descends, the abdominal viscera are pushed downwards and forwards, and the muscles of the anterior abdominal wall relax. In deep inspiration, it is not difficult to imagine the condition where abdominal relaxation becomes limited and the continued contraction of the diaphragm will in fact then elevate the lower ribs. These ribs, as has already been mentioned, have flat facets on the tubercles and therefore an upward, outward and back- ward movement of the whole rib will occur, resulting in a small decrease in the antero-posterior diameter with a big increase in the transverse dimension of the lower part of the chest, that is, a big increase in the transverse dimension of the upper part of the abdomen with increased accommodation for the abdominal viscera. The downward movement of the diaphragm, the descent of the viscera, the anterior movement of the abdominal wall, have to be described as though they proceeded in steps, but they are in fact closely integrated activities that are adapting to each other throughout. The work of 129 10 G. CAUSEY Campbell and Green (1953) on the simultaneous recording of respiratory exchange, abdominal action potential and intragastric pressure illustrates this coordination. They have shown that even with volume exchanges of up to 90 litres per min. there is no alteration in intragastric pressure; the intragastric excursion remains less than 10 cm. water with increasing rate and depth of respiration, The mode of action of the diaphragm is generally accepted and it is more on the question of quantity that debate of diaphragmatic function is based. The general view can be summarized by quoting from three standard modern text-books: 1. Throughout life the diaphragm is probably the main muscle of inspiration (Nims in Fulton's Physiology). 2. Quiet breathing is almost entirely diaphragmatic (Lovatt Evans quoting Hoover). 3. The diaphragm is the chief inspiratory muscle (Gray). Before accepting these statements too rigidly, two points should be made: (1) Hoover (1922) showed in the dog that the tidal air was reduced by at least 53 per cent. if the intercostal and abdominal muscles were paralysed, and that this condition reduced the vital capacity even more, that is by 67 per cent. In the human, with paralysis of the intercostals but normal abdominal muscles, the loss of vital capacity was only 15 per cent. (2) Keith (1909) has drawn attention to the relation of the descent of the diaphragm to tidal air. Taking round figures, he finds that the area of the diaphragm in contact with the lung is 250 sq. cm., its descent is a little more than 10 mm. and therefore there is an increase in thoracic capacity of about one half of the tidal air. Another way of looking at the same point is to assess the area of the diaphragm, excluding the peri- cardial area, and to compare it with the area of the pleura lining the chest wall, excluding the mediastinal pleura. In two cadavers the diaphragmatic areas were 678 sq. cm. and 720 sq. cm. and the comparable areas of the chest wall lined with pleura were 1732 sq. cm. and 1820 sq. cm. So that if, in quiet respiration, the diaphragm and ribs took a fifty-fifty share in the increase in capacity the mean rib excursion would only need to be 3 or 4 mm. for a mean diaphragmatic excursion of 10-12 mm. In watching the chest excursions on an X-ray screen it does seem that one must be very careful not to be deceived by the easily describable and measurable excursion of the diaphragm as against the complex movement of the ribs. The increase in height of the thorax by the elevation of the ring formed by the first pair of ribs and the manubrium sterni has also found general acceptance. The scalene muscles, the sterno-mastoids and the serratus posterior superior can pull up the thoracic operculum if the cervical vertebra are prevented from flexing by the sacro spinalis group. This elevation of the first rib is easily seen in forced respiration but when does this function really begin? 130 THE ANATOMY OF THE THORAX IN RELATION TO THE FLOW OF TIDAL AIR Primrose has made the following statement concerning the recording of muscle action potentials: " It (the action potential) indicates the surge of tonicity without displaying actual contraction, and as tonicity by itself does not perform gross function, the method by itself does not explain much concerning chest movement" (Primrose 1952). This attitude of mind will not help in understanding the mechanism of respiration. If the first rib were pulled down by inspiratory muscles then the contraction of the scalenes to bring the first rib back into place would be a gross function. Is not the maintenance of the first rib in position just as gross a function? It is like a motor car in gear with its brakes on. As long as the work done by the brakes is greater than or equal to that done by the engine there will be no movement, but gross work will be done by both engine and brakes. This point is emphasised because it has a very direct bearing on the next subject for consideration, the action of the intercostal muscles. The fibres of the external intercostals pass downwards and forwards from the superior to the inferior rib, and do not extend beyond the

Fig. 2. 131 10-2 G. CAUSEY costochondral junction; the internal intercostal is directed downwards and backwards from the superior to the inferior ribs. This description has probably done considerable disservice. Apart from grave doubts as to its morphological exactitude, it seems that it has made the temptation to correlate the two phases of respiration with the two muscles too great. There seem to be strong grounds for correlating the abdominal and thoracic walls. The segmental nerve lies between the obliquus internus and the transversus abdominis and in the thoracic region it lies between the intercostalis internus and the intercostalis intimus. This relationship is clearly shown in Fig. 2 reproduced from an article by Davies, Gladstone and Stibbe (1932). The intercostalis intimus or intracostal should be included with the transversus thoracis and subcostal muscles as the inner- most layer of musculature, always lying internal to the segmental nerve and spanning one, two or more intercostal spaces. The function of these intercostal muscles has been debated for years m,nd as early as 1867 Duchenne tabulated the possible actions and their main supporters. Duchenne, 1867: 1. Both muscles inspiratory (Borelli, Senac, Boerhaave, Vinslow, Haller, Cuvier). 2. Both expiratory (Vesale, Diemerbroeek, Sabatier). 3. External expiratory, internal inspiratory (Bartholi). 4. External inspiratory, internal expiratory (Spigel, Vesling, Hamberger). 5. External and internal intercostals are at different times both inspiratory and expiratory (Mayer, Magendie, Bouvier, Burdach, Cruveilhier). 6. The external and internal muscles act together and are in different places inspiratory or expiratory (Behrens). 7. That these two muscles are not directly concerned with rib movement but immobilise the chest wall (van Helmont, Arantius, Neueranzius). Duchenne himself comes out as a staunch supporter of Haller-that both muscles are inspiratory. Hamberger's explanation has been repeated time and time again through the intervening years. He considers a system of two isolated ribs articulating at the vertebral end, and, by resolving the forces produced by an individual muscle fibre along and at right angles to the rib, comes to the conclusion that, because the lower attachment of the external intercostal is further from the vertebral column than the upper attachment, it will elevate the rib while the reverse holds for the internal intercostal, and it will therefore depress the rib. This cannot hold in a freely movable 132 THE ANATOMY OF THE THORAX IN RELATION TO THE FLOW OF TIDAL AIR system. The ribs must approximate to each other whichever muscle contracts, the only difference being in the rate of descent or ascent of the respective ribs. This discussion of a freely movable system of the ribs on the vertebral column has been modified by the inclusion of the sternum as a factor maintaining the relative positions of the anterior ends of the ribs. Here again, however, the argument is limited by the presence of a movable costochondral joint and flexible cartilage. To get over this difficulty relative fixity of the ribs is called in; this amounts to the same as group five of Duchenne's table, because between two diarthrodial joints there can be different ranges of movement inherent in the joint, but not different degrees of fixity within that range unless we call into action some ligaments or muscle extraneous to the joint. This leads us to an expanded statement of the fifth and seventh groups in Duchenne's table that can be stated thus: that the intercostal muscles are mechanically able to produce either inspiration or expiration and that the movement in fact produced will be dependent on whether they contract synchronously with those muscles that fix the thoracic inlet (the scalenes, serratus posterior superior and sternal muscles), or whether they contract synchronously with those muscles that fix the lower ribs (quadratus lumborus, serratus posterior inferior and the muscles of the abdominal wall) and that they will at the same time diminish the tendency to wasteful indrawing or bulging of the intercostal spaces. If this hypothesis is to be logically consistent, how does it explain the now classical findings of Bronk and Ferguson (1934)? Their recordings are illustrated in every text book of physiology and reproduced in Fig. 3. The action potentials in the external intercostal nerve twigs are inspiratory and in the internal intercostals expiratory. However, before one draws any generalisation from this picture, as has been frequently done, one must examine the context of Bronk and Ferguson's work.

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Fig. 3. Firstly they were concerned with rhythmic activity of the respiratory centres and were concerned to show that the motor neurones were rhythmically discharging in the absence of the afferent impulses that Adrian had analysed (Adrian, 1933). One must therefore face quite clearly that in these experiments there were no muscle movements. They were abolished with curare. This does not, however, affect the basic conclusion that these muscles are stimulated by these motor neurones in the respiratory phases just stated. It is in fact a demonstration of the 133 G. CAUSEY central integration that was being emphasised here. Secondly, the statement made by these authors is: " The rhythmic groups of impulses in the fibres to the external intercostal muscle are generally associated with inspiration." The exceptions form three groups, the first of which is illustrated in another of their records. Here the nerve to the external intercostal is firing both in inspiration and expiration. The second group is illustrated by a further quotation from their text-" It should be pointed out that in some cases the impulses in nerve fibres supplying the internal intercostals were found to be synchronous with those to the external intercostals and therefore with inspiration." Thirdly in asphyxia-" The discharge then becomes continuous and the two sets of cells may discharge simultaneously." This all shows a central control of the stimulation of the intercostal muscles and is consistent with the conception that all the intercostals musculature can act as inspiratory or expiratory depending on what synergists are active. It has been possible to get some further support for this view of intercostal muscle activity by recording the potentials from the surface of the

Fig. 4. 134 THE ANATOMY OF THE THORAX IN RELATION TO THE FLOW OF TIDAL AIR scalene muscles in dogs anesthetised with nembutal. Fig. 4 shows the increased activity of the muscle potentials during each of four inspiratory phases. These potential changes were, of course, grossly exaggerated when the air intake was obstructed. It does seem that even in " quiet respiration " the scalene muscles are functionally active in preventing the first rib from being pulled down by the contraction of the intercostal muscles. All the possible functional combinations of the intercostal muscles had had their different supporters by 1867. The case for integrated respiratory function of the kind that has been stressed in this paper was put forward strongly and convincingly by Hoover in 1922. He had under his care a patient with paralysis of nearly all his intercostal muscles from poliomyelitis, and then verified his experience in man by experimental work on dogs. I quote one of his concluding paragraphs. " In the case of the intercostal muscles, their action is the same in inspiration and expiration, but they aid expansion or constriction of the thorax according to the gradient, which is determined for the inspiration by synchronous activation of the scaleni and serratus posterior superior and for expiration by the serratus posterior inferior, triangularis sterni and abdominal muscles." I wish to acknowledge the technical assistance of Mr. S. A. Edwards, Mr. C. G. Bush and Mr. C. H. Redman.

REFERENCES ADRIAN, E. D. (1933) J. Physiol. 79, 332. BRONK, D. W. and FERGUSON, L. K. (1934-5) Amer. J. Physiol. 110, 700. CAMPBELL, M. and GREEN, J. H. (1953) J. Physio. 120, 409. DAVIES, F., GLADSTONE, R. J. and STIBBE, E. P. (1931-32) J. Anat. 66, 323. DUCHENNE, G. B. (1867) Physiologie des Mouvements. Bailli6re et Fils, Paris. GRAY, H. (1949) Anatomy, descriptive and applied. Ed. T. B. Johnston and J. Whillis. Longmans Green & Co. HOOVER, L. (1922) Arch. int. Med. 30, 1. KEITH, SIR ARTHUR (1909) Respiration in Man, in Further Advances in Physiology. Edward Arnold & Co. LOVATT EVANS, C. E. (1949) Principles of Human Physiology. J. A. Churchill. NIMS, L. E. (1946) Howell's Textbook of Physiology. Ed. J. F. Fulton. p. 858. W. B. Saunders. PRIMROSE, W. B. (1952) Brit. J. Anaesth. 24, 3.

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