111 2 3 4 4 5 6 The Anatomy and Physiology of 7 8 the Diaphragm 9 1011 George R. Harrison 1 2 3 4 5 6 7 8 9 2011 laterally, the ventral ends and costal cartilages 1 Aims of the seventh to twelfth , the transverse 2 processes of the first lumbar , and the 3 To describe development, anatomy and bodies and symphyses of the first three lumbar 4 physiology of the diaphragm. vertebrae. As the periphery of the diaphragm is 5 attached to the anteriorly and 6 laterally, and beyond it posteriorly, it will follow 7 Anatomy that the anterior portion of the diaphragm will 8 be shorter than the lateral and posterior parts. 9 The Shape of the Diaphragm The presence of the viscera in the and 3011 causes the part of the diaphragm sep- 1 The diaphragm is a musculo-fibrous sheet sep- arating them to be roughly horizontal, but will 2 arating the thorax and the abdomen. It takes the determine the shape of the unstressed dome. 3 shape of an elliptical cylindroid capped with a This may be considered as a separate zone from 4 dome [1]. This short description of the shape of the other part of the diaphragm, and will be 5 the diaphragm is not adequate to explain the referred to as the diaphragmatic zone. The other 6 way in which the structure and function are part of the diaphragm will be referred to as the 7 related, and a further expansion of this descrip- apposition zone, because it assumes a roughly 8 tion is necessary. The use of the word dome in vertical direction. It is also the area through 9 itself introduces a degree of inaccuracy, as it which the cage is apposed to the abdominal 4011 gives the impression that there is a curved struc- contents and thus exposed to abdominal pres- 1 ture rising equally from the sides to a central sure (see below). 2 point, whereas a more accurate description is of 3 a pair of cupolas either side of a central plateau. Diaphragmatic Attachments 4 This elliptical shape is determined by the 5 thoracic outlet, which will also have an influence The sternal part is attached by two slips to the 6 upon the function of the diaphragm, as it will back of the , although these slips 7 determine the anatomical structure of it. This is may be absent (Figure 4.1). The costal part is 8 because the thoracic outlet is set obliquely to the attached to the internal surfaces of the lower 9 coronal plane, being superior anteriorly and six costal cartilages and their adjoining ribs, 5011 inferior posteriorly. the vertical fibres of the diaphragm interdigitat- 1 The skeletal attachments of the diaphragm ing with the horizontal fibres from the trans- 2 to the thoracic outlet commence at the xiphoid versi abdominis. The lumbar part is attached 311 process and symphysis centrally, and, moving to the aponeurotic medial and lateral arcuate

45 46

4 · UPPER GASTROINTESTINAL SURGERY

parts of the upper two. As with the anterior lon- 1111 gitudinal ligament, the main area of attachment 2 is at the level of the intervertebral discs and 3 the adjacent margins of the vertebral bodies. 4 Between these attachments the upper lumbar 5 arteries separate the fibres from the bodies of 6 the vertebrae. The fibres ascend and run anteri- 7 orly to cross the aorta in a median arch, where 8 the tendinous margins converge to form the 9 . This ligament is often 1011 poorly defined, but when it occurs it is at the 1 level of the thoracolumbar disc. 2 The fibres of the crura continue in their 3 passage anteriorly and superiorly, but divide 4 Figure 4.1. The inner anterior surface of the diaphragm. into medial and lateral bundles. The lateral 5 (Reproduced with permission from Gluzel P, Similowski T, fibres continue laterally to reach the central 6 Chartrand-Lefebvre C et al. Diaphragm and chest wall: assess- ment of the inspiratory pump with MR imaging – preliminary tendon. The medial fibres from the right crus 7 observations. Radiology 2000;215:574–83. Copyright Radio- ascend to the left of the oesophageal opening. 8 logical Sciety of North America.) Sometimes a muscular fasciculus from the 9 medial side of the left crus crosses the aorta and 2011 runs obliquely through the fibres of the right 1 ligaments (lumbocostal arches) and to the crus towards the vena caval opening but does 2 upper three by crura. The ster- not approach the oesophageal opening. The 3 nocostal and lumbar portions are distinct devel- right margin of the oesophageal opening is 4 opmentally and in 80% of the population are covered by the deeper medial right crural fibres. 5 separated by a hiatus in the muscular sheet – the From part of the right crus near the oesophageal 6 vertebrocostal trigone. This gap lies above the opening originates the suspensory muscle of the 7 twelfth rib so that the upper pole of the kidney duodenum, which goes to connective tissue near 8 is separated from the pleura by loose areolar the coeliac artery. Here it joins with a fibro- 9 tissue only. muscular band of non-striated muscle originat- 3011 The lateral arcuate ligament is a thickened ing along the third and fourth parts of the 1 band in the fascia of quadratus lumborum, duodenum and the duodenojejunal flexure. The 2 which arches across the muscle and is attached exact nature and function of this muscle has 3 medially to the front of the first transverse been the subject of discussion over many years, 4 process and laterally to the inferior margin of and will not be considered here. 5 the twelfth near its midpoint. 6 The is a thickened The Central Tendon of the 7 band in the fascia covering psoas major. 8 Medially it blends with the lateral tendinous Diaphragm 9 margin of the corresponding crus and is thus All the muscular fibres converge upon the 4011 attached to the side of the first or second lumbar central tendon of the diaphragm (Figure 4.2). 1 vertebrae. Laterally it is attached to the front The central tendon is a thin, strong aponeuro- 2 of the first lumbar transverse process at the sis of interwoven collagen fibres, with its ante- 3 lateral margin of psoas. The arcuate ligaments rior margin closer to the front of the diaphragm. 4 allow the contraction of quadratus lumborum This results in the longer fibres being lateral and 5 and psoas to occur without interfering with posterior. The longest fibres of the diaphragm 6 diaphragmatic activity. arise from the ninth costal cartilage. 7 The crura are tendinous at their attachments, 8 blending with the anterior longitudinal verte- 9 bral ligament. The right crus is broader and Embryology 5011 longer and arises from the anterolateral aspect 1 of the bodies and discs of the first three lumbar The diaphragm develops from four main struc- 2 vertebrae, the left crus from the corresponding tures, the septum transversum, the pleuroperi- 311

46 47

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 mass of tissue which then extends dorsally and 2 medially towards the dorsal body wall, to meet 3 the dorsal mesentery of the foregut. As it grows 4 it leaves two dorsolateral gaps, which are the 5 orifices of the pleuroperitoneal canals. 6 The pleuroperitoneal membranes are a pair 7 of membranes which gradually separate the 8 pleural and peritoneal cavities. They are 9 attached dorsolaterally to the body wall with 1011 their free edge projecting into the caudal end 1 of the pericardioperitoneal canals. At about the 2 sixth week of gestation they grow medially and 3 ventrally away from the body wall towards the 4 septum transversum. By the end of that week 5 they have come to fuse with the dorsal mesen- 6 tery of the oesophagus and the septum trans- 7 versum to separate the pleural and peritoneal 8 cavities. The closure of the openings is further 9 Figure 4.2. Inner posterior aspect of the diaphragm. 1, The enhanced by the growth of the and muscle 2011 central tendon. 2, Attachment of lateral arcuate ligament to end tissue extension into the membranes. The right 1 of the twelfth rib. 3, Lateral arcuate ligament. 4, Medial arcuate pleuroperitoneal canal closes before the left one, 2 ligament. 5, Transverse process first lumbar vertebra. the latter being the more common site of per- 3 (Reproduced with permission from Gluzel P, Similowski T, sistent communication between the pleural and Chartrand-Lefebvre C et al. Diaphragm and chest wall: assess- 4 ment of the inspiratory pump with MR imaging – preliminary peritoneal cavities. The pleuroperitoneal mem- 5 observations. Radiology 2000;215:574–83. Copyright Radio- branes are believed only to produce a small 6 logical Sciety of North America.) dorsolateral part of the diaphragm in adult life. 7 The dorsal mesentery of the oesophagus fuses 8 with both the septum transversum and the pleu- 9 toneal membranes, the dorsal oesophageal roperitoneal membranes. This mesentery forms 3011 mesentery and the body wall. the medial portion of the diaphragm. The crura 1 The septum transversum forms the bulk of of the diaphragm develop from muscle fibres 2 the diaphragm, namely the central tendon and that grow into the oesophageal mesentery. 3 the majority of centrally placed muscle. It starts The contribution of the muscular body 4 off as a plate of mesoderm developing at the end wall to the diaphragm is the result of the expan- 5 of the fourth week of gestation in a position sion of the pleural cavities between the ninth 6 between the heart and the yolk sac. At this time and twelfth weeks of gestation. To expand, the 7 the headfold and tailfolds form, and the heart pleural cavities extend into the mesoderm 8 and pericardial cavities move ventrally below dorsal to the suprarenal glands, the gonads and 9 the foregut. They open dorsally into the peri- the mesonephric ridges, causing somatopleuric 4011 cardioperitoneal canals, which lie above the mesoderm to be peeled away from the dorsal 1 septum transversum on each side of the foregut body wall to form a substantial area of the dor- 2 connecting the thoracic and abdominal portions solumbar part of the diaphragm. As a result of 3 of the intraembryonic coelom. the extension of the pleural cavities into the 4 The septum transversum is initially at the body wall, the costodiaphragmatic recesses are 5 level of the second cervical segment, but with formed. 6 the growth of the embryo it moves in a caudal It is described variously as trifoliate, trefoil or 7 direction, and at the level of the fourth cervical like the club in a pack of cards, the three parts 8 segment it receives the phrenic nerve and cells being partly separated by slight indentations. 9 destined to differentiate into muscular tissue This description does not seem to agree with the 5011 from the corresponding myotomes. It migrates pictures that are reproduced in many textbooks, 1 caudally during flexion and comes to lie at the which make it look far more like a boomerang. 2 level of the junction between the thoracic and There is a middle part, which is an equilateral 311 lumbar segments. At this site it forms a ventral triangle, its apex towards the xiphoid process.

47 48

4 · UPPER GASTROINTESTINAL SURGERY

This central area is beneath and partly blended vagus nerves, and the oesophageal branches of 1111 with the pericardium above, and relates to the the left gastric vessels and lymphatic vessels. 2 triangular ligament of the liver in the abdomen. The muscle of the oesophageal wall and the 3 The right and left parts posteriorly are longer diaphragm remain separate. However, the infe- 4 and linguiform, curving posterolaterally, the rior diaphragmatic fascia, which is a thin areolar 5 left being the narrower. These are related to stratum rich in elastic fibres, lying between the 6 the parietal pleura above and the peritoneum diaphragm and the peritoneum, and continuous 7 below. In the central area can be recognised four with the transversalis fascia, ascends through 8 diagonal bands, which expand from a thick the opening. It does so like a flattened cone 9 node where decussation of compressed tendi- to blend with the oesophageal wall about 2 cm 1011 nous strands occurs in front of the oesophageal above the gastro-oesophageal junction. Some of 1 aperture and left of the vena caval opening. the elastic fibres penetrate to the submucosa. 2 This fascial expansion, which forms the phreno- 3 The Diaphragmatic Apertures oesophageal ligament, connects the oesophagus 4 and the diaphragm in a flexible manner which 5 As the diaphragm separates the abdominal and allows some freedom of movement during 6 thoracic cavities, there are several structures and swallowing. 7 which will either pass through it, or between it The vena caval aperture is the highest of the 8 and the body wall including blood vessels, three, and lies approximately at the level of 9 nerves and the oesophagus. There are various the disc between the eighth and ninth thoracic 2011 apertures to allow the passage of these, three of vertebrae. It is quadrilateral and sited within the 1 which are large and constant, and various others central tendon, at the junction of its right leaf 2 which are smaller and sometimes variable. with the central area. Therefore the margin is 3 The aortic opening, the most inferior and pos- aponeurotic, to which the vena cava is adherent 4 terior, lies at the level of the lower border of the as it traverses the opening. With it run branches 5 twelfth thoracic vertebra and the thoracolumbar of the right phrenic nerve. The left phrenic 6 intervertebral disc, slightly to the left of the nerve runs off the pericardium to pierce the 7 midline. This is not a true opening, rather it is muscular part of the diaphragm in the form of 8 a vertical osseo-aponeurotic and symphysio- the left limb of the central tendon. 9 aponeurotic channel between the crura laterally There are various minor apertures. Two lesser 3011 and the posteriorly and the apertures in each crus transmit the greater and 1 diaphragm anteriorly. Therefore it is actually lesser splanchnic nerves. The ganglionated 2 behind the diaphragm or the median arcuate sympathetic trunks run from the thorax to the 3 ligament. On occasions there are some tendi- abdomen behind the medial end of the medial 4 nous crural fibres which pass behind the aorta, arcuate ligament. Posterior to the lateral arcuate 5 forming a fibrous ring. It transmits the aorta. ligament runs the . 6 Along with the aorta, generally to the right of Between the sternal and costal margins of the 7 the midline, runs the thoracic duct, posterolat- diaphragm run the superior epigastric arteries 8 eral to which are the azygos vein on the right, and veins, prior to entering the rectus sheath, 9 and the hemi-azygos vein on the left. Sometimes along with lymph vessels from the abdominal 4011 the azygos and hemi-azygos veins will pass wall and liver. Similarly the musculophrenic 1 through the right and left crus respectively. artery and vein run between the attachments 2 Lymphatic trunks also descend through the of the diaphragm to the seventh and eighth 3 opening from the lower posterior thoracic wall. costal cartilages. The neurovascular bundles of 4 The oesophageal aperture is elliptical and the seventh to eleventh intercostal spaces pass 5 lies at the level of the tenth thoracic vertebra, between the digitations of transversus abdo- 6 where its long lies obliquely, ascending to minis with the diaphragm into the neurovascu- 7 the left of the midline in the muscular part of lar plane of the abdominal wall. 8 the right crus which has by now crossed over the Extraperiteoneal lymph vessels on the 9 midline. Its lower end lies anterosuperior to abdominal surface pass through the diaphragm 5011 the aortic opening, its upper end being further to nodes lying on its thoracic surface, mainly in 1 anterosuperior and a short distance to the left. the posterior mediastinum. Finally, openings for 2 It transmits the oesophagus, the trunks of the small veins are frequent in the central tendon. 311

48 49

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 Nerve Supply The venous drainage mirrors the blood 2 supply. The superior surface drains through 3 The diaphragm receives its nerve supply pre- the pericardiacophrenic veins, musculophrenic 4 dominantly from the phrenic nerve. This arises veins and superior epigastric veins which all 5 mainly from the ventral root of the fourth cer- drain into the internal thoracic vein. The infe- 6 vical nerve, with contributions from the third rior surface of the diaphragm drains through 7 and fifth cervical nerve roots. The intrathoracic the inferior phrenic veins. The right drains to 8 course of these nerves will not be discussed the IVC. The left is often double, the anterior 9 here. branch going to the IVC, the posterior branch 1011 The right phrenic nerve reaches the dia- to the left renal vein or left suprarenal vein. The 1 phragm just lateral to the inferior vena cava two veins may anastomose with each other. 2 (IVC). The left phrenic nerve joins the dia- 3 phragm just lateral to the border of the heart, in Lymphatic Drainage 4 a slightly more anterior plane than the right 5 phrenic nerve. The nerves divide at the level of The diaphragmatic lymph nodes on the thoracic 6 the diaphragm, or just above it into several ter- surface of the diaphragm form three groups. 7 minal branches, the right being the mirror of the An anterior group comprises two or three small 8 left. Apart from small twigs to the serosa of nodes posterior to the base of the xiphoid 9 the diaphragm, there are three main branches: process draining the convex hepatic surface, 2011 a sternal or anterior branch, an anterolateral and one or two nodes on each side near the 1 branch and a posterior branch which divides junction of the seventh rib and cartilage which 2 into a posterolateral branch and a crural branch receive anterior lymph vessels from the 3 that runs posteromedially to the region of the diaphragm and drain to the parasternal nodes. 4 crus. They are usually deep within the muscle A lateral group on each half of the diaphragm 5 rather than lying exposed on the undersurface comprises two or three nodes, close to the site 6 of the diaphragm [2,3]. at which the phrenic nerves enter the 7 The phrenic nerve provides the only motor diaphragm, and on the right some of the nodes 8 supply to the diaphragm. The crural motor may lie anterior to the intrathoracic end of the 9 supply comes solely from the phrenic nerve, but IVC within the pericardium. They receive affer- 3011 all crural fibres (regardless of the side of origin) ents from the central diaphragm (bilateral) and 1 right or left of the oesophageal opening are from the convex surface of the liver (right side), 2 supplied by the ipsilateral phrenic nerve. The and send efferents to the parasternal, posterior 3 phrenic nerve also supplies the majority of mediastinal nodes, and brachiocephalic nodes. 4 sensory fibres including muscle spindles [4]. A posterior group consists of a small number 5 There are some sensory fibres to the diaphragm of nodes on the back of the crura, connected 6 from the lower six or seven intercostal nerves with the lateral aortic and the posterior medi- 7 in the area where the diaphragm is attached to astinal nodes. 8 the ribs. 9 Lymph Vessels of the Diaphragm 4011 Blood Supply 1 An extensive lymph plexus is present in each 2 The arterial supply varies above and below the surface of the diaphragm, and the two plexuses 3 diaphragm. The superior surface is supplied by are united by numerous vessels that pierce the 4 the musculophrenic, pericardiacophrenic and diaphragm. The thoracic plexus unites with 5 superior epigastric arteries, all of which are vessels of the mediastinal and costal pleura. 6 branches of the internal thoracic mammary Anterior efferents pass to the anterior diaphrag- 7 artery, and the phrenic branches of the lower matic nodes near the junction of the seventh 8 thoracic aorta. There is also a supply from the ribs and cartilages, the middle efferents to nodes 9 lower five intercostal and subcostal arteries. on the oesophagus and around the inferior vena 5011 The inferior surface is supplied by the inferior cava, and posterior efferents to nodes around 1 phrenic arteries, which are branches of the the aorta as it leaves the thorax. The abdominal 2 abdominal aorta, although sometimes they may plexus anastomoses with hepatic lymphatics 311 be derivatives of the coeliac trunk. and with subperitoneal tissue peripherally.

49 50

4 · UPPER GASTROINTESTINAL SURGERY

Efferents on the right end up either in a group surements of relationships between tension and 1111 of nodes on the inferior phrenic artery or in the muscle elongation. This relationship is non- 2 right lateral aortic nodes. Efferents on the right linear, as a result of the muscle becoming stiffer 3 go to preaortic nodes, lateral aortic nodes and as it is stretched, and is believed to represent a 4 nodes at the lower end of the oesophagus. recruitment phenomenon within the muscle; 5 that is, as the muscle is stretched, fibrous ele- 6 Relations of the Diaphragm ments that are unstressed at low extension are 7 progressively recruited, contributing their elas- 8 Superiorly the diaphragm is associated with ticity in parallel with increasing extension [5]. 9 serous membranes. On either side is the pleura, The collagenous central tendon is less exten- 1011 which separates the diaphragm from the lung sible than the muscle. Collagen has a high 1 bases, and in the middle is pericardium sepa- modulus of elasticity, such that a high stress is 2 rating it from the heart. The middle part of the necessary for a small amount of extension. It 3 central tendon is slightly lower, flatter and more is believed that the central tendon has a func- 4 horizontal than the other parts, which form tion similar to that of a normal muscular 5 rounded cupolas. The inferior surface is covered tendon, namely transmitting the stress gener- 6 with peritoneum, that of the right cupola being ated by the muscle, and allowing this to be 7 in contact with the convex right lobe of the converted into movement. 8 liver, the right kidney and suprarenal gland. The 9 peritoneum of the left cupola is in contact with Contraction of the Diaphragm 2011 the left lobe of the liver, the gastric fundus, the 1 , left kidney and adrenal gland. During quiet breathing, the zone of apposition 2 represents one-quarter to one-third of the total 3 surface of the . In an average human 4 Physiology in the upright position the axial extent of the 5 zone of apposition from costal insertion to the 6 The main function of the diaphragm is ventila- diaphragmatic reflection increases from nearly 7 tion, but there is also a non-ventilatory role of 0 to 5 cm as the lung volume is reduced from 8 the diaphragm. This will be considered at the total lung capacity to functional residual capac- 9 end of this section. Prior to that, this section will ity, and increased further to 10 cm at residual 3011 concentrate upon the ventilatory function of the volume [6]. 1 diaphragm, looking at three different areas, When the diaphragmatic muscle shortens 2 firstly the elastic properties of the diaphragm, during inspiration, the axial length of the 3 then the effects of contraction, followed by an cylindrical portion diminishes and the dome 4 examination of the importance of relaxation in descends relative to its costal insertions. The 5 maintaining normal ventilation. zone of apposition of the diaphragm cannot 6 change shape during breathing, unless the 7 Elastic Properties of the shape of the rib cage does. The dome part of 8 Diaphragm the diaphragm is able to change, but does not 9 normally do so during quiet breathing. 4011 As the diaphragm is a composite structure the During quiet breathing the decrease in axial 1 elasticity will vary with the type of tissue. The length of the apposed diaphragm is about 2 cm, 2 collagenous central tendon is relatively inelas- whereas the increase in sagittal and coronal 3 tic. The muscular component will vary in its diameters of the rib cage is only approximately 4 elasticity dependent upon the state of expansion 0.3 and 0.5 cm, respectively. Therefore the 5 of the chest wall, as this will have an impact most important change in diaphragmatic shape, 6 upon the resting length of the muscle groups. responsible for the majority of volume dis- 7 Muscle is composed of a contractile compo- placement during normal quiet breathing, is the 8 nent, and an elastic component. The elastic piston-like axial displacement of the dome of 9 component can be divided into a series compo- the diaphragm by the contraction of the axial 5011 nent and a parallel component. Elasticity of length of the zone of apposition. 1 resting muscle is usually described in terms The pressure difference across the diaphragm 2 of its tensile properties, characterised by mea- (the transdiaphragmatic pressure (Pdi)) is 311

50 51

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 related to the orthogonal tensions and radii of As the contents of the abdomen are virtually 2 curvature by Laplace’s law, but in the zone incompressible (apart from a small amount of 3 of apposition the radius of curvature in the gas within the bowel), there must be an equal 4 axial direction is large, and so local Pdi would and outward displacement of the abdominal 5 be related to circumferential tension and curva- wall. In the human the abdomen is bounded 6 ture. Pdi is therefore the total axial force devel- by the lumbar spine posteriorly and pelvis 7 oped by the apposed diaphragmatic fibres inferiorly, which are not readily displaced, and 8 divided by the cross-sectional area at the zone by the rib cage, which nearly meets the iliac 9 of apposition. Because the number of fibres con- crest at the side. The free abdominal wall is 1011 tracting is probably fairly consistent, the Pdi is therefore limited to the ventral abdominal wall, 1 directly related to the tension developed within and contraction of the diaphragm should dis- 2 the fibres and inversely related to the thoracic place it. However, if the rib cage expands suffici- 3 cross-sectional area. As recent radiological ently the diaphragm may contract during 4 studies have shown that the area of the dome of inspiration without producing any abdominal 5 the diaphragm varies very little between resid- displacement. 6 ual volume and functional residual capacity, There is evidence in humans to demonstrate 7 this may not need to be considered in assessing that there are changes in the rib cage that 8 the Pdi [7]. occur as a result of diaphragmatic activity. This 9 The shape of the dome does not vary signifi- work has been done by studying the breath- 2011 cantly during quiet breathing as mentioned ing patterns in patients who have had transec- 1 above, and therefore the radius of curvature of tions of the cervical spine, so that there is an 2 the diaphragmatic dome also does not need to active phrenic nerve, but no intercostal muscle 3 be considered in assessing the Pdi. This is an activity [8]. Measurements were made in sitting 4 advantage because the shape of the diaphragm subjects at the third and seventh costal inter- 5 is complex as described above, and has many faces, and demonstrated a difference between 6 radii of curvature, all of which will conspire the two parts of the rib cage. During inspiration 7 to make estimates of Pdi from Laplace’s law the abdominal wall moves out, associated with 8 difficult. an increase in the sagittal and coronal diame- 9 The piston analogy breaks down when the ters of the lower rib cage. In contrast, at the 3011 diaphragm has shortened enough to eliminate upper rib cage the movement in both planes 1 the zone of apposition. Under these conditions is inward. 2 the transdiaphragmatic pressure has to be Thus the contraction of the diaphragm 3 analysed by considering the radii of curvature appears to have two actions on the rib cage. 4 and the anisotropic (i.e. varying with position) Firstly, the decrease in pleural pressure that it 5 tension within the muscular sheet of the produces would tend to displace the rib cage 6 diaphragm. A major variable for determin- inwards. This is an effect predominantly on 7 ing the force generated by the diaphragmatic the upper ribs, although in the non-tetraplegic 8 muscle is the length–tension behaviour of the patient the scalene and intercostal muscles tend 9 muscle. Generally the greater the initial length to prevent this. Secondly, it also has an inspira- 4011 of the muscle fibre, the greater the force devel- tory action, which tends to affect the lower ribs. 1 oped, and therefore the greater the transdia- The inspiratory action has two components to 2 phragmatic pressure. When considering the it, one being related to the force developed 3 diaphragm, one of the determinants of fibre through the insertion into the ribs (insertional 4 length will be the lung volume; the lesser the component), the second being the force exerted 5 volume the greater the fibre length. through the zone of apposition by the increase 6 in abdominal pressure that occurs during 7 Effect of Diaphragmatic Contraction on diaphragmatic contraction (appositional com- 8 ponent). The net action of the diaphragm at this 9 Abdomen and Rib Cage level will depend upon the balance between the 5011 The descent of the dome of the diaphragm, insertional and appositional inspiratory forces 1 which occurs during inspiration, will increase and the expiratory force generated by the fall in 2 the subdiaphragmatic pressure and cause pleural pressure. In general inspiration is the 311 displacement of the abdominal viscera caudally. greater force.

51 52

4 · UPPER GASTROINTESTINAL SURGERY

The insertional component of the inspiratory contraction on the rib cage has been discussed 1111 action of the diaphragm relates to the manner above, the situation in the normal subject is 2 of insertion of the costal fibres, namely into the complicated by the fact that there are inspira- 3 lower ribs. As these fibres are directed upwards tory muscles other than the diaphragm, includ- 4 and parallel to the rib cage axis, their contrac- ing the intercostals and scalenes. These appear 5 tion exerts a force that tends to raise the ribs, to be automatically brought into play with the 6 and therefore move them outwards. This is diaphragm. 7 dependent upon forces resisting the descent of However, even when these are taken into con- 8 the diaphragm. Part of this resistance is pro- sideration, it has been demonstrated that the 9 vided by the abdominal pressure, as well as by diaphragm expands the lower rib cage less in 1011 the solid elements in the abdomen, the latter the supine position than the erect. This evidence 1 providing resistance by resisting displacement, comes from tetraplegic patients, in whom, 2 which is not reflected in the abdominal pres- during inspiration in the upright posture, the 3 sure. That the abdominal viscera provide a lower rib cage moves outwards [10]. However, 4 fulcrum on which the diaphragm acts to raise in the supine position, during inspiration 5 the lower ribs has been confirmed in canine the lower rib cage moves inwards, whilst the 6 experiments, which demonstrate that eviscera- abdominal diameter increases. The rib cage 7 tion of the animal causes the costal fibres of the then moves outwards during expiration. Thus 8 diaphragm to contract rather than to expand the diaphragm has an inspiratory activity in the 9 the rib cage [9]. erect posture, but expiratory effect in the supine 2011 The appositional component of lower rib cage position. 1 expansion relates to changes in abdominal pres- The explanation for the mechanism behind 2 sure. This increase in abdominal pressure that these differences in posture is not fully eluci- 3 occurs during diaphragmatic contraction will dated. Whatever the position of the body, the 4 act through the zone of apposition. There are effect of diaphragmatic contraction is to cause 5 several variables that will affect the appositional a fall in pleural pressure, and therefore for the 6 component, the main two being the abdominal same increase in lung volume the expiratory 7 pressure and the size of the zone of apposition, force of the rib cage would be assumed to be 8 but the compliance of the abdominal wall will equal. Thus the differences in rib cage move- 9 also have an impact upon it. ment between supine and erect posture are 3011 If there is a large zone of apposition, the considered to be related to differences in appo- 1 increase in abdominal pressure will be trans- sitional and/or insertional forces. The zone of 2 mitted to the rib cage over a large area, and will apposition is known to vary between erect and 3 act by causing outward movement of the ribs. supine posture, both in shape and size, the 4 This will be greater if the abdominal compliance dorsal component being greater when supine, 5 is low. This is the situation occurring during the ventral component being less. In transfer- 6 normal tidal breathing. However, if the zone of ring between the upright and horizontal posi- 7 apposition is greatly reduced, which occurs at tion the abdominal contents are displaced 8 lung volumes approaching vital capacity, the cephalad and the lung volume at functional 9 pressure generated upon the abdominal con- residual capacity is reduced by approxi- 4011 tents will not have such a great inspirational mately 15% of the vital capacity. The diaphrag- 1 component. matic muscles are lengthened and develop 2 appreciable passive tensions at relatively higher 3 Influence of Posture lung volumes. Also, the diaphragmatic dome 4 is subject to varying transmural pressures, 5 In normal upright subjects quiet breathing increasing from the uppermost to the lower 6 occurs in such a manner that with inspiration surfaces, as a result of gravitational effects. The 7 there is an increase in the anteroposterior diam- gradient of pleural pressure is probably less 8 eters of both the abdomen and the rib cage than that of the abdominal side, and in humans 9 which is reversed on expiration. In the supine the difference in transmural pressure between 5011 subject there is a greater increase in the abdom- the upper and lower surfaces is about 10 cmH2O. 1 inal component than the rib cage during inspi- This will give the dome an increase in curvature 2 ration. Although the effect of diaphragmatic in the direction of gravity. 311

52 53

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 The latter may have an impact upon the inser- greater the lung volume, the lesser the length of 2 tional component of the ventral part of the the muscle fibre, placing them on a less advan- 3 diaphragm, possibly as a result of converting the tageous portion of the length/tension curve. It 4 axial tension, which would be created in the has also been shown that for a given electrical 5 erect posture, to a radial tension, which would stimulation of the phrenic nerve, the transdi- 6 cause the ribs to be drawn in. On top of this aphragmatic pressure increases as the abdomi- 7 there will be an increase in abdominal compli- nal anteroposterior diameter decreases (i.e. as 8 ance in the supine position, which will also the diaphragm is more cephalad with its fibres 9 cause the ribs to move inwards, the opposite to longer). At high lung volumes when the zone 1011 the changes occurring in the erect posture. of apposition has disappeared and the muscles 1 The effects of diaphragmatic contraction on are no longer inserting into the ribs tangentially, 2 the upper part of the rib cage are unrelated to the transdiaphragmatic pressure will be less 3 posture. When the rib cage muscles are inactive because of the increasing radius of curvature of 4 the diaphragm causes the upper rib cage to the diaphragm (Laplace’s law). Finally, near 5 move inwards in both erect and supine pos- total lung capacity phrenic nerve stimulation is 6 tures. This has been demonstrated not only in expiratory to the lungs, as a result of both the 7 tetraplegic patients [8] but also in normal sub- rib cage constricting activity of the diaphragm 8 jects during rapid-eye-movement sleep [11], at high lung volumes and the inability of the 9 when there is a reduction of electrical activity flattened dome to expand the abdomen. 2011 in the parasternal area, allowing a paradoxical 1 movement of the rib cage with inspiration. Relaxation of the Diaphragm 2 3 Influence of Lung Volume Muscle relaxation is the process by which the 4 muscle actively returns, after contraction, to its Lung volume will have a marked influence on 5 initial conditions of length and load. The 6 the action of the diaphragm on the rib cage. As diaphragm contracts and relaxes continuously 7 lung volume decreases below functional residual throughout life, and must return to a relatively 8 capacity the zone of apposition will increase. constant resting position at the end of each con- 9 Thus the area of the rib cage exposed to abdom- traction–relaxation cycle. There is evidence to 3011 inal pressure will increase while the areaexposed support the hypothesis that rapid and complete 1 to the pleural pressure decreases. Conversely, relaxation of the diaphragm plays an important 2 with an increase in lung volume, there will be a role in adaptation to changes in respiration 3 reduction in the zone of apposition. From this it load and breathing frequency [12]. Relaxation 4 will be seen that there is a reduction in the abnormalities may contribute, in part, to 5 diaphragm’s inspiratory activity with increasing impaired contractile performance. This may 6 lung volumes. Furthermore, when the lung vol- occur at various levels from the molecular level 7 ume approaches total lung capacity, the zone of upwards. 8 apposition disappears completely, and the mus- 9 cle fibres at their insertion into the ribs are ori- Molecular Aspects of Relaxation in 4011 entated radially towards the body axis rather 1 than axially along the body axis. The insertional Diaphragm Muscle 2 component then enhances rather than opposes There is a complex interplay between inactiva- 3 the expiratory force related to a fall in pleural tion (mainly at the molecular and cellular level) 4 pressure, and contraction of the diaphragm and loading conditions (forces affecting muscle 5 therefore deflates the lower rib cage. length and tension). The rate of inactivation is 6 The ability of the diaphragm to generate pres- limited by various mechanisms, which will be 7 sure is also strongly dependent upon lung described below. 8 volume. As lung volume increases, the trans- Firstly there is active Ca2+ pumping by the 9 diaphragmatic pressure created for a given sarcoplasmic reticulum (SR). The SR is a spe- 5011 stimulation of the phrenic nerve decreases cialised form of agranular endoplasmic reticu- 1 almost linearly. This relationship, demonstrated lum, which forms a plexus of anastomosing 2 in humans [10], is related to the force length membranous channels filling much of the space 311 characteristic of the diaphragmatic fibres, the between the myofibrils. The arrival of the action

53 54

4 · UPPER GASTROINTESTINAL SURGERY potential causing contraction is responsible for Thirdly there are other mechanisms which 1111 the release of large amounts of calcium from may be relevant. It has been suggested that par- 2 the SR, which triggers the development of actin– valbumin, a high affinity Ca2+-binding protein, 3 myosin cross-bridges and hence muscle con- may modulate the relaxation rate of skeletal 4 traction. The reverse is essential for relaxation, muscle by facilitating Ca2+ transport from the 5 the cytosolic Ca2+ being transported into the SR, myofibrils to the SR. In mammalian skeletal 6 an active process assisted by Mg2+- Ca2+-acti- muscle the relaxation rate has been found to 7 vated ATPase. Thus the rate of uptake will be a correlate with the parvalbumin concentration. 8 function of the number of pumping sites and the Another possibility is that changes in mem- 9 rate at which they operate. branous ionic conductances play a role in the 1011 There are variations in the SR of the different slowing of relaxation in fatigued diaphragm by 1 muscle types described elsewhere in this chap- slowing of action potential repolarisation. 2 ter. There is a higher capacity of SR Ca2+ uptake 3 in fast- compared with slow-twitch fibres, which Mechanical Aspects of Relaxation in 4 is mirrored by the higher relaxation rate. This is 5 related to differences in the density of active Diaphragm Muscle 6 pumping sites. There are also molecular differ- Although much work has been done on relax- 7 ences, particularly in the sarco(endo)-plasmic ation of the diaphragm after isometric contrac- 8 reticulum Ca2+-ATPase (SERCA), of which tion, and has demonstrated that there are 9 two isoforms have been found in the human various factors which can impair the relaxation 2011 diaphragm, namely SERCA1 and SERCA2a. rate, such as ageing, maturation, denervation, 1 SERCA1 is found only in fast-twitch skeletal malnutrition, cardiomyopathy and fatigue, 2 fibres, whereas SERCA2a is expressed in slow- this is not the normal situation, as the in 3 twitch skeletal fibres as well as in cardiac and vivo diaphragm contracts and relaxes against 4 smooth muscles. various levels of load. During afterloaded con- 5 It should also be noted that there are age- traction, the muscle relaxation phase classically 6 associated changes within the muscle fibres, as consists of isotonic lengthening, followed by 7 an age-related decline in SR Ca2+ pump function isometric tension decay. 8 has been described in skeletal muscles. This Isotonic relaxation is an increase in length at 9 decline, presumably due to impaired coupling constant tension. It has been shown that the 3011 between ATP hydrolysis and Ca2+ transport into maximum extent of muscle shortening, ⌬L 1 the SR, may contribute to the slowing of the is the main mechanical determinant of peak 2 diaphragm relaxation rate in older persons. lengthening velocity [13]. Peak lengthening 3 Secondly there is Ca2+ removal from troponin velocity (VL) physiologically increases with the 4 C (TnC). The binding of Ca2+ to TnC acts as a extent of muscle shortening, irrespective of 5 switch to allow cross-bridge formation, hence initial muscle length and of the load imposed 6 contraction of the muscle, whilst removal on the muscle during the lengthening process. 7 inhibits cross-bridge attachment and hence The slope of the VL–⌬L relationship is lower in 8 relaxation. The movement will depend in part twitch than in sustained mode and/or when the 9 on the affinity of Ca2+ for TnC, which increases lengthening process is delayed. In myopathic 4011 with sarcomere length and decreases with a models, VL is slowed and the overall duration 1 decline in intracellular pH. Thus the capacity of of isotonic lengthening is prolonged. The myo- 2 TnC to release Ca2+ and the SR to reuptake it pathic process modifies the coupling between 3 explains the length dependence of relaxation in ⌬L and VL. 4 the diaphragm. At heavy load sarcomere short- Isometric relaxation is a falling tension at 5 ening is moderated so that the high affinity of constant length. When tension decay occurs 6 TnC for Ca2+ impedes Ca2+ removal from the at initial length, the peak rate of tension decline 7 myofibrils, whilst at short sarcomere length is mainly determined by the afterload, and 8 and/or low load, the low affinity of TnC to Ca2+ except at approximately isometric load levels 9 promotes the dissociation of the two. Therefore an increase in afterload linearly accelerates the 5011 as long as the Ca2+ can be sequestered into the peak rate of tension decline [14]. 1 SR, relaxation is faster as the sarcomere short- Relaxation of the diaphragm, like the heart, is 2 ening increases. load sensitive, that is, the overall time course of 311

54 55

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 relaxation is strongly affected by the afterload when applied in vivo that it starts to have clin- 2 level. A contraction loaded with light or moder- ical relevance. As mentioned above, it is known 3 ate load terminates earlier than a full isometric that changes in relaxation occur with fatigue of 4 contraction, so that a muscle that is allowed to the diaphragm, and that a suitable means to 5 shorten has a shorter contraction–relaxation measure this clinically would be an advantage. 6 cycle. This is a manifestation of the shortening- Various means have been tried, which involve 7 induced deactivation phenomenon described deriving the relaxation rate from various pres- 8 above. sure curves, measuring either the transdi- 9 Although the muscle appears to relax in two aphragmatic pressure (Pdi) oesophageal, mouth 1011 stages, sarcomeres relax auxotonically, i.e. or nasal pressures. These rely on the assump- 1 changes in sarcomere length and tension occur tion that the chest wall and lungs will not have 2 simultaneously. Because loading conditions a significant effect upon the pressure curves, 3 have opposite effects on isotonic and isometric and that the pressure decay coincides with the 4 relaxation rates, it has been suggested that start of diaphragmatic relaxation. The latter 5 different intracellular mechanisms regulate the may not be true, as studies have demonstrated 6 diaphragmatic muscle-lengthening rate on the that the diaphragm continues to receive motor 7 one hand, and the isometric relaxation rate on output during the early part of expiration [16]. 8 the other [14]. It may be that the sarcomere Two main measures have been derived from 9 length (SL) at the start of the relaxation phase the pressure decay curves. The first is the 2011 is important. maximum relaxation rate (MRR), which is the 1 As has been observed in cardiac muscle, sar- negative peak of the pressure derivative as a 2 comere relaxation in the afterloaded diaphragm function of time, and measures the initial part 3 displays two consecutive phases: an initial phase of the pressure decay. The latter portion of the 4 of rapid sarcomere lengthening corresponding curve is described in terms of its time constant, 5 to the isotonic relaxation phase followed by a as it is normally a mono-exponential curve. The 6 second, slower relaxation phase corresponding MRR varies with Pdi, such that relaxation is 7 to the isometric relaxation phase [15]. It has also accelerated when Pdi increases. 8 been shown, in studies that have examined both It has been shown in the in vivo diaphragm 9 muscle length and SL, that as the load level that respiratory muscle fatigue slows the relax- 3011 increases, isotonic muscle lengthening occurs at ation rate, as demonstrated by an increase in 1 progressively longer SL, which will correspond the time constant and/or a decrease in the 2 to the SL at peak shortening. In contrast, at the MRR. Slowing of relaxation is an early signal of 3 end of the isotonic phase, when the muscle has the onset of fatigue as it precedes failure of the 4 finished shortening, the sarcomere has not yet diaphragm to generate a previously attainable 5 returned to its resting length. At that stage iso- Pdi. A slowing of relaxation has been shown in 6 metric contraction begins, and it is demon- normal subjects who have undergone fatiguing 7 strated that the SL is constant at that time, contractions of the diaphragm, and in patients 8 regardless of the external load. with chronic obstructive airways disease walked 9 Thus there is a complex equilibrium modu- to dyspnoea. Slowing of inspiratory muscle 2+ 4011 lated by the capacity of TnC to liberate Ca and relaxation has been proposed as a predictive 2+ 1 SR to recapture Ca and by length-dependent index of weaning failure in mechanically venti- 2 changes in myofilament lattice spacing, which lated patients. 3 may help to explain why relaxation occurs New techniques have enabled measurements 4 earlier and faster at low loads than it does at to be made in intact animals, and it has been 5 heavy loads. Provided SR is efficient, length- demonstrated that the decay of pleural pressure 6 dependent changes in the affinity of TnC and in ends before the crural and costal parts of 7 myofilament lattice spacing may favour rapid the diaphragm have returned to their initial 8 and early muscle lengthening when the muscle muscle length [17]. Thus pleural pressure 9 length is notably shortened (i.e. at low loads). swings during relaxation do not totally coincide 5011 Relaxation of the Diaphragm In Vivo with diaphragm muscle relaxation. Also it is 1 noted in supine animals that the peak length- 2 Although much is learnt about the function of ening velocity of the crural diaphragm, which 311 the diaphragm from in vitro studies, it is only has a greater extent of shortening, exceeds that

55 56

4 · UPPER GASTROINTESTINAL SURGERY of the costal part, suggesting that VL is related further limit diaphragmatic perfusion, espe- 1111 to ⌬L in vivo as well as in vitro. cially at high breathing frequencies [21]. 2 3 4 Role of Diaphragm Relaxation in Non-ventilatory Properties of the Respiratory Function 5 Diaphragm 6 The ventilatory performance of the diaphragm 7 depends upon its resting length, which also The concept that the diaphragm had functions 8 depends upon the relaxation and compliance of other than that of ventilating the lungs origi- 9 the muscle. The optimal resting length (Lo) of nated in the work of Bartelink [22]. This study 1011 the diaphragm is at or slightly below functional looked at the load placed upon the lumbar inter- 1 residual capacity (FRC) [18]. During inspiration vertebral discs when lifting heavy objects, and 2 between FRC and total lung capacity the human calculated that the load applied to the discs 3 diaphragm will shorten by 25–35% Lo. It is nec- would be greater than that required to rupture 4 essary for the diaphragm length to return to Lo them (as measured in vitro). Thus there must be 5 by the end of expiration. If this does not occur, some form of protective mechanism available to 6 due to incomplete or delayed relaxation, there the body. Bartelink further demonstrated that 7 will be incomplete expiration to FRC. This will the intra-abdominal pressure increased with 8 cause multiple problems, as the lungs will move lifting heavy weights, but also that the pressure 9 up the lung compliance curve, potentially was much greater as the trunk was flexed, in 2011 increasing the work of breathing, while the comparison with the erect position. He postu- 1 diaphragm moves down its passive length– lated that the abdominal contents acted as a 2 tension relation, is placed at a mechanical dis- fluid ball, surrounded by muscles, namely the 3 advantage for optimal force generation, and its diaphragm, the transverse abdominal muscles 4 inspiratory shortening capacity is curtailed. and the muscles of the pelvic floor. He suggested 5 This will increase the risk of ventilatory failure. that if there were such a ball present between 6 As in other skeletal muscle, contractile per- the costal margin and the pelvis, the lumbar 7 formance is dependent upon adequate energy spine could be removed, and the body would 8 supplies, hence an adequate blood supply. The not collapse as a result thereof. In the presence 9 relaxation phase is responsible for accommo- of the lumbar spine, the increase in intra- 3011 dating most of the changes in blood perfusion abdominal pressure will serve to unload the 1 brought about by increased diaphragmatic spine and increase trunk stability. 2 work. Diaphragmatic blood flow is reduced It was recognised that the abdominal and tho- 3 during inspiration and can be completely abol- racic cavities upon which the diaphragm acts 4 ished during forceful contractions [19]. Blood are involved with the stability of the trunk and 5 flow restriction has been attributed to intra- postural control [23]. Other respiratory muscles 6 muscular pressure acting on the blood vessels acting upon the rib cage and abdomen perform 7 between muscle fibres. The pressure in turn a postural function which is integrated with 8 depends upon the load to which the diaphragm their respiratory role, for example the inter- 9 is subjected and the degree of muscle shorten- costal muscles stabilise the rib cage [24]. 4011 ing. However, the zone of apposition is known Contraction of the abdominal muscles con- 1 to increase greatly in thickness during inspira- tributes to trunk stability prior to and during 2 tion, which may have a beneficial effect upon the movement of the limbs, an action which is 3 regional blood flow by minimising the pressure increased when respiratory demands increase 4 surrounding the microvasculature [20]. During [25]. 5 relaxation intramuscular pressure declines to Contraction of the pelvic floor muscles and 6 baseline, thus allowing diaphragmatic perfusion abdominal muscles, in particular transversus 7 to occur. At a low respiratory rate the duration abdominis, correlates closely with the increase 8 of relaxation is long and the blood flow can in intra-abdominal pressure in a variety of 9 increase to meet the metabolic demands. At postural tasks [23]. When the stability of the 5011 higher rates the relaxation period may be insuf- trunk is challenged by reactive forces due to 1 ficient to meet diaphragmatic oxygen require- limb movement, transversus abdominis con- 2 ments. Thus delayed or slowed relaxation may tracts before the agonist limb muscle, which 311

56 57

THE ANATOMY AND PHYSIOLOGY OF THE DIAPHRAGM

111 suggests that the response might be pre-pro- movement was superimposed on its ventilatory 2 grammed by the central nervous system [25,26]. and tonic activation. Therefore ventilation can 3 More recent studies have demonstrated that continue uncompromised by the activity of 4 the diaphragm contributes to the increased other muscle groups whilst the diaphragm is 5 intra-abdominal pressure prior to the initiation acting as a spinal support. 6 of movements of large segments of the upper Further studies of a similar nature have 7 limb. This contraction is independent of the demonstrated that there is a reciprocal activity 8 phase of respiration [24]. This evidence suggests of transversus abdominis with the diaphragm 9 that the diaphragm has a function in the main- during breathing under conditions of repeti- 1011 tenance of the postural control of the human tive arm action. With the initiation of move- 1 trunk. The same paper also showed that the ment the diaphragm and abdominal muscles 2 preparatory contraction of the diaphragm is contract simultaneously to increase abdominal 3 associated with initial shortening of its muscle pressure. Breathing is facilitated by the relax- 4 fibres and occurs simultaneously with activa- ation of transversus abdominis during diaphra- 5 tion of transversus abdominis. gmatic contraction, to allow displacement of 6 The argument in favour of this conclusion the abdominal contents, and vice versa during 7 relates to the fact that any movement of a limb expiration [29]. 8 is associated with reactive forces imposed upon That the diaphragm acts tonically with activ- 9 the trunk which are equal and opposite to ity in other parts of the body is consistent with 2011 those producing the movement, and that the earlier findings, which demonstrate the sus- 1 diaphragm in itself is unable to move the trunk tained elevation of transdiaphragmatic pressure 2 directly to oppose these forces. during lifting [30]. More recent studies have 3 Moreover, the contraction of the diaphragm demonstrated that the greatest increase in 4 increases pressure within the abdominal transdiaphragmatic pressure is seen during sit- 5 cavity, which may contribute to trunk stability. ups and power lifts, and studies in weight-lifters 6 Also, diaphragmatic contraction could increase has demonstrated an increase in the diaphrag- 7 stability of the trunk by minimising displace- matic mass in these people [31]. This is further 8 ment of the abdominal contents into the thorax, evidence to support the proposition that the 9 maintaining the hoop-like geometry of the diaphragm is recruited in non-ventilatory activ- 3011 abdominal muscles, which could then increase ities. As well as supporting the spine, it is impor- 1 spinal stability through tension in the thora- tant in maintaining ventilation. With lifting of 2 columbar fascia. This study also demonstrated heavy objects, or even upper limb movement, 3 that there was co-activation of the costal and there is an increase in intra-abdominal pres- 4 crural portions of the diaphragm [24], which sure. If there were no diaphragmatic recruit- 5 suggests that for postural reasons the two parts ment, the elevated intra-abdominal pressure 6 of the diaphragm may function together, would be transmitted to the thorax, provoking 7 although there have been previous studies the unwanted effects of raised intrathoracic 8 which demonstrate that the two portions of the pressure (raised central venous, intracranial 9 diaphragm may function independently [27]. and systemic blood pressures). 4011 Unlike other muscles that are involved with In patients with phrenic nerve paralysis there 1 the maintenance of posture, the diaphragm has is often a difficulty in breathing with bending 2 to continue to act in its primary role as a muscle or lifting. Measurements made within such 3 of ventilation. That it is able to do so is demon- patients [31] demonstrate that there is a rise in 4 strated in studies looking at the activity of the intra-abdominal pressure with lifting, but there 5 diaphragm during repetitive arm activity [28]. is no transdiaphragmatic pressure, i.e. the pres- 6 This modifies diaphragmatic activity in two sure in the abdomen is transmitted directly 7 ways unrelated to ventilation. First, unlike to the thorax. Thus these patients become dys- 8 breathing at rest, the diaphragm contracted ton- pnoeic on exertion, as they are only able to 9 ically throughout the respiratory cycle. If this breathe in between bouts of activity, unlike the 5011 were accompanied by abdominal muscle activ- normal person who is able to breathe and lift or 1 ity, the intra-abdominal pressure would be move at the same time. 2 elevated. As well as this, phasic modulation of It will be apparent from this section that 311 diaphragm activity at the frequency of limb there is still a great deal of uncertainty about the

57 58

4 · UPPER GASTROINTESTINAL SURGERY complete function of the diaphragm, and that 11. Tusiewicz K, Moldofsky H, Bryan AC, Bryan MH. 1111 there is a lot of work ongoing investigating the Mechanics of the rib cage and diaphragm during sleep. 2 J Appl Physiol 1977;43:600–2. activity of the diaphragm in health and disease, 12. Coirault C, Chemla D, Lecarpentier Y. Relaxation of 3 utilising newer and more sophisticated tech- diaphragm muscle. J Appl Pysiol 1999;87:1243–52. 4 niques. It will be interesting to see what more 13. Coirault C, Chemla D, Pery N et al. Mechanical deter- 5 will be learned about this fascinating organ in minants of isotonic relaxation in isolated diaphragm 6 the coming years. muscle. J Appl Physiol 1993;75:2265–72. 7 14. Coirault C, Chemla D, Pery-Man N et al. Isometric relax- ation of isolated diaphragm muscle: influences of load, 8 length, time and stimulation. J Appl Physiol 1994;766: 9 1468–75. 1011 Questions 15. Coirault C, Chemla D, Suard I et al. Sarcomere relax- 1 ation in hamster diaphragm muscle. J Appl Physiol 2 1996;81:858–65. 1. Which structures pass through the 3 diaphragm? 16. Easton PA, Katagiri M, Kieser TM, Platt RS. Postinspi- ratory activity of costal and crural diaphragm. J appl 4 2. Describe the nerve supply. Physiol 1999;87:582–9. 5 3. What is the function of the diaphragm? 17. Newman S, Road J, Bellemare F et al. Respiratory mus- 6 cle length measured by sonomicrometry. J Appl Physiol 7 1984;56:753–64. 18. Margulies SS, Farkas GA, Rodarte JR. Effects of body 8 References position and lung volume on in situ operating length of 9 the canine diaphragm. J Appl Physiol 1990;69:1702–8. 2011 1. De Troyer A, Loring SH. Action of the respiratory mus- 19. Bellemare F, Wight D, Lavigne CM, Grassino A. Effect of 1 cles. In: Fishman AP, Mackelm PT, Mead J, Geiger SR tension and timing of contraction on the blood flow of (eds). Handbook of physiology Section 3: The respira- the diaphragm. J Appl Physiol 1983;54:1597–1606. 2 tory system Volume III. Mechanics of breathing, part 2. 20. Wait JL, Johnson RL. Patterns of shortening and thick- 3 Bethesda, MD: American Physiological Society, 1986; ening of the human diaphragm. J Appl Physiol 1997;83: 4 443–62. 1123–32. 5 2. Fell SC. Surgical anatomy of the diaphragm and the 21. Hu F, Comtois A, Grassino AE. Optimal diaphragmatic 6 phrenic nerve. Chest Surg Clin N Am 1998;8:281–94. blood perfusion. J Appl Physiol 1992;72:149–57. 3. Merendino KA, Johnson RJ, Skinner HH, Maguire RX. 22. Bartelink DL. The role of abdominal pressure in reliev- 7 The intradiaphragmatic distribution of the phrenic ing the pressure on the lumbar intervertebral discs. J 8 nerve with particular reference to the placement of Joint Surg 1957;39B:718–25. 9 diaphragmatic incisions and controlled segmental 23. Grillner S, Nilsson J, Thorstensson A. Intra-abdominal 3011 paralysis. Surgery 1956;39:189–98. pressure changes during natural movements in man. 1 4. Muller N, Volgyesi L, Bryan MH, Bryan AC. Diaphrag- Acta Physiol Scand 1978;103:275–83. matic muscle tone. J Appl Physiol 1979;47:279–84. 24. Hodges PW, Butler JE, McKenzie DK, Gandevia SC. 2 5. Smith JC, Loring SH. Passive mechanical properties of Contraction of the human diaphragm during rapid 3 the chest wall. In: Fishman AP, Mackelm PT, Mead J, postural adjustments. J Physiol 1997;505:539–48. 4 Geiger SR (eds). Handbook of physiology Section 3: The 25. Hodges PW, Richardson CA. Contraction of the abdom- 5 Respiratory System Volume III. Mechanics of breathing, inal muscles associated with movement of the lower 6 part 2. Bethesda, MD: American Physiological Society, limbs. Phys Ther 1997;77:132–44. 1986; 429–42. 26. Hodges PW, Richardson CA. Feedforward contraction 7 6. Braun NMT, Arora NS, Rochester DF. Force-length rela- of transversus abdominis is not influenced by the direc- 8 tionship of the normal human diaphragm. J Appl tion of arm movement. Exp Brain Res 1997;114:362–70. 9 Physiol 1982;53:405–12. 27. De Troyer A, Sampson M, Sigrist S, Macklem PT. The 4011 7. Cluzel P, Similowski T, Chartrand-Lefebvre C et al. diaphragm: two muscles. Science 1981;213:237–8. Diaphragm and chest wall: assessment of the inspiratory 28. Hodges PW, Gandevia SC. Activation of the human 1 pump with MR imaging preliminary observations. diaphragm during a repetitive postural task. J Physiol 2 Radiology 2000;215:574–83. 2000;522:165–75. 3 8. Mortola JP, Sant’Ambrogio G. Motion of the rib cage 29. Hodges PW, Gandevia SC. Changes in intra-abdominal 4 and the abdomen in tetraplegic patients. Clin Sci Mol pressure during postural and respiratory activation of 5 Med 1978;54:25–32. the human diaphragm. J Appl Physiol 2000;89:967–76. 9. De Troyer A, Sampson M, Sigrist S, Macklem PT. Action 30. Hemborg B, Moritz U, Löwing H. Intra-abdominal pres- 6 of costal and crural parts of the diaphragm on the rib sure and trunk muscle activity during lifting. IV. The 7 cage in dog. J Appl Physiol 1982;53:30–9. causal factors of the intra-abdominal pressure rise. 8 10. Danon J, Druz WS, Goldberg NB, Sharp JT. Function of Scand J Rehabil Med 1985;17:25–38. 9 the isolated paced diaphragm and the cervical accessory 31. Al-Bilbeisi F, McCool F. Diaphragm recruitment during 5011 muscles in C1 quadriplegics. Am Rev Respir Dis 1979; nonrespiratory activities. Am J Respir Crit Care Med 119:909–19. 2000;162:456–9. 1 2 311

58