Diaphragm

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CHAPTER 58 Diaphragm

The diaphragm is a curved musculofibrous sheet that separates the thoracic from the abdominal cavity (Figs 58.1, 58.2). Its mainly convex upper surface faces the thorax, and its concave inferior surface is directed towards the abdomen. The positions of the domes or cupolae of the diaphragm are extremely variable because they depend on body build and the phase of ventilation. Thus the diaphragm will be higher in short, fat people than in tall, thin people, and overinflation of the lung, as occurs for example in emphysema, causes marked depression of the diaphragm. Usually, after forced expiration the right cupola is level anteriorly with the fourth costal cartilage and therefore the right nipple, whereas the left cupola lies approximately one rib lower. With maximal inspiration, the cupola will descend as much as 10 cm, and on a plain chest radiograph the right dome coincides with the tip of the sixth rib. In the supine position, the diaphragm will be higher than in the erect position, and when the body is lying on one side, the dependent half of the diaphragm will be considerably higher than the uppermost one.

ATTACHMENTS AND COMPONENTS

The muscle fibres of the diaphragm arise from the highly oblique circumference of the thoracic outlet: the attachments are low posteriorly and laterally, but high anteriorly. Although it is a continuous sheet, the muscle can be considered in three parts, sternal, costal and lumbar, which are based on the regions of peripheral attachment. The sternal part arises by two fleshy slips from the back of the xiphoid process, and is not always present. The costal part arises from the internal surfaces of the lower six costal cartilages and their adjoining ribs on each side, and interdigitates with transversus abdominis (see Fig. 54.14). The lumbar part arises from two aponeurotic arches, the medial and lateral arcuate ligaments (sometimes termed lumbocostal arches) and from the lumbar vertebrae by two pillars or crura.

The lateral arcuate ligament is a thickened band in the fascia that covers quadratus lumborum, and it arches across the upper part of that muscle. It is attached medially to the front of the transverse process of the first lumbar vertebra, and laterally to the lower margin of the twelfth rib near its midpoint. The medial arcuate ligament is a tendinous arch in the fascia that covers the upper part of psoas major. Medially, it is continuous with the lateral tendinous margin of the corresponding crus, and is thus attached to the side of the body of the first or second lumbar vertebra. Laterally, it is fixed to the front of the transverse process of the first lumbar vertebra.

The crura are tendinous at their attachments, and blend with the anterior longitudinal ligament of the vertebral column. The right crus is broader and longer than the left, and arises from the anterolateral surfaces of the bodies and intervertebral discs of the upper three lumbar vertebrae. The left crus arises from the corresponding parts of the upper two lumbar vertebrae. The medial tendinous margins of the crura meet in the midline to form an arch, the median arcuate ligament, which crosses the front of the aorta at the level of the thoracolumbar disc; it is often poorly defined.

From these circumferential attachments, the fibres of the diaphragm converge into a central tendon. Fibres from the xiphoid process are short, run almost horizontally and are occasionally aponeurotic. Fibres from the medial and lateral arcuate ligaments, and more especially those from the ribs and their cartilages, are longer. They rise almost vertically at first and then curve towards their central attachment. Fibres from the crura diverge, and the most lateral become even more lateral as they ascend to the central tendon. Medial fibres of the right crus embrace the oesophagus where it passes through the diaphragm, the more superficial fibres ascend on the left, and deeper fibres cover the right margin. Sometimes, a fleshy fasciculus from the medial side of the left crus crosses the aorta and runs obliquely through the fibres of the right crus towards the vena caval opening, but this fasciculus does not continue upwards around the oesophageal passage on the right side.

The central tendon of the diaphragm is a thin but strong aponeurosis of closely interwoven fibres situated near the centre of the muscle, but closer to the front of the thorax, so that the posterior muscular fibres are longer. In the centre it lies immediately below the pericardium, with which it is partially blended. Its shape is trifoliate. The middle, or anterior, leaf has the form of an equilateral triangle with the apex directed towards the xiphoid process. The right and left folia are tongue-shaped and curve laterally and backwards, the left being a little narrower. The central area of the tendon consists of four well-marked diagonal bands fanning out from a thick central node where compressed tendinous strands decussate in front of the oesophagus and to the left of the vena cava.

APERTURES

A number of structures pass between the thorax and abdomen via apertures in the diaphragm. There are three large openings, for the aorta, oesophagus and inferior vena cava, and a number of smaller ones (Fig. 58.2).

The aortic aperture is the lowest and most posterior of the large openings, and is found at the level of the lower border of the twelfth thoracic vertebra and the thoracolumbar intervertebral disc, slightly to the left of the midline. It is an osseo-aponeurotic opening defined by the diaphragmatic crura laterally, the vertebral column posteriorly and the diaphragm anteriorly. Strictly speaking, it lies behind the diaphragm and its median arcuate ligament (when present). Occasionally, some tendinous fibres from the medial parts of the crura also pass behind the aorta, converting the opening into a fibrous ring. The aortic opening transmits the aorta, thoracic duct, lymphatic trunks from the lower posterior thoracic wall and, sometimes, the azygos and hemiazygos veins.

The oesophageal aperture is located at the level of the tenth thoracic vertebra, above, in front and a little to the left of, the aortic opening. It transmits the oesophagus, gastric nerves, oesophageal branches of the left gastric vessels and some lymphatic vessels. The elliptical opening has a slightly oblique long axis, and is bounded by muscle fibres that originate in the medial part of the right crus and cross the midline, forming a ‘chimney’ approximately 2.5 cm long, which accommodates the terminal portions of the oesophagus. The outermost fibres run in a craniocaudal direction, and the innermost fibres are arranged circumferentially. There is no direct continuity between the oesophageal wall and the muscle around the oesophageal opening. The fascia on the inferior surface of the diaphragm is continuous with the transversalis fascia and is rich in elastic fibres. It extends upwards into the opening as a flattened cone to blend with the wall of the oesophagus 2–3 cm above the oesophago-gastric (squamocolumnar) junction. Some of its elastic fibres penetrate to the submucosa of the oesophagus. This peri-oesophageal areolar tissue is referred to as the phreno-oesophageal ligament. It connects the oesophagus flexibly to the diaphragm, permitting some freedom of movement during swallowing and ventilation while at the same time limiting upward displacement of the oesophagus.

The vena caval aperture, the highest of the three large openings, lies at about the level of the disc between the eighth and ninth thoracic vertebrae. It is quadrilateral, and located at the junction of the right leaf with the central area of the tendon, and so its margins are aponeurotic. It is traversed by the inferior vena cava, which adheres to the margin of the opening, and by some branches of the right phrenic nerve.

There are two lesser apertures in each crus: one transmits the greater, and the other the lesser, splanchnic nerve. The ganglionated sympathetic trunks usually enter the abdominal cavity behind the diaphragm, deep to the medial arcuate ligament. Openings for minute veins frequently occur in the central tendon.

On each side of the diaphragm there are small areas where the muscle fibres are replaced by areolar tissue. One, between the sternal and costal parts, contains the superior epigastric branch of the internal thoracic artery and some lymph vessels from the abdominal wall and convex surface of the liver. The other, between the costal part and the fibres that spring from the lateral arcuate ligament, is less constant; when it is present, the posterosuperior surface of the kidney is separated from the pleura only by areolar tissue.

Congenital hernias/eventration

Abdominal organs, usually the stomach, may herniate through the diaphragm into the thorax. There are three sites at which such hernias can occur: posterolateral (Bochdalek), subcostosternal (Morgagni) and oesophageal.

The most common is a posterolateral (Bochdalek) hernia, which occurs as a result of a defect in the posterior diaphragm in the region of the tenth or eleventh ribs. It is more common on the left, and presents with abdominal contents in the left hemithorax at birth; clinically significant cases develop hypoxaemia and respiratory failure at birth. A chest radiograph demonstrates mediastinal shift to the contralateral side and the presence of the gastrointestinal contents in the thorax; the diagnosis should be made at routine prenatal ultrasound. Treatment involves decompression of the gastrointestinal contents and cardiopulmonary stabilization. Surgical repair is performed when the patient is stable, but prognosis is determined by the degree of accompanying pulmonary hypoplasia, severity of pulmonary vascular abnormalities and any associated congenital heart defects.

Subcostosternal hernia, first described by Morgagni, is uncommon and occurs through a defect in the anterior diaphragm just lateral to the xiphoid process. It is frequently asymptomatic.

Oesophageal hernia occurs as a result of a defect in the oesophageal aperture, so that part of the stomach herniates into the thorax. It is rarely congenital in origin, usually develops later in life, and is believed to be acquired.

Diaphragmatic trauma

Closed and penetrating thoracoabdominal injuries may result in rupture or laceration of the diaphragm. With closed injuries and diaphragmatic rupture, there may be subsequent herniation of the abdominal contents into the thorax. Spiral CT with planar reformation should be the primary investigation (Shanmuganathan et al 2000): MRI is usually performed when other imaging modalities have produced equivocal findings. Early operative repair is recommended in diaphragmatic trauma, because untreated cases are at risk of developing gastrointestinal obstruction or perforation. Patients with penetrating injuries may require additional assessment by thoracoscopy (Lowdermilk & Naunheim 2000).

VASCULAR SUPPLY

ARTERIES

The lower five intercostal and subcostal arteries supply the costal margins of the diaphragm while the phrenic arteries supply the main central portion of the diaphragm. The anastomotic arrangement (see p. 1010) ensures profuse blood supply.

INNERVATION

The diaphragm receives its motor supply via the phrenic nerves (Fig. 58.3). Sensory fibres are distributed to the peripheral part of the muscle by the lower six or seven intercostal nerves. The right crus of the diaphragm, the fibres of which divide to the right and left of the oesophageal opening, is innervated by both right and left phrenic nerves. There is some evidence that the crural fibres contract slightly before the costal part, and this may be functionally significant for non-respiratory tasks (Sharshar et al 2005).

Phrenic nerve

The phrenic nerve is a mixed nerve that provides the sole motor supply to the diaphragm. It is derived mostly from the fourth cervical ramus, but also receives contributions from the third and fifth cervical rami (see Fig. 43.6). The course of the cervical part of the phrenic nerve is described on page 456. Within the thorax, the phrenic nerve descends anterior to the pulmonary hilum, between the fibrous pericardium and mediastinal pleura, to the diaphragm, accompanied by the pericardiophrenic vessels. In its thoracic course, each phrenic nerve supplies sensory branches to the mediastinal pleura, fibrous pericardium and parietal serous pericardium. The right and left phrenic nerves differ in their intrathoracic relationships (Rajanna 1947).

Diaphragmatic relationships

The right phrenic nerve passes through the central tendon of the diaphragm, either by the caval aperture or just lateral to it. The left phrenic nerve passes through the muscular part of the diaphragm anterior to the central tendon, just lateral to the left cardiac surface and more anterior than the right phrenic nerve (Fig. 58.2). At the diaphragm or slightly above it, each phrenic nerve supplies fine branches to the parietal pleura above, and the parietal peritoneum below, the central diaphragm. Typically, the trunk of each nerve then divides into three branches as it passes through the diaphragm. These are commonly arranged as follows (with some variation): an anterior (sternal) branch, which runs anteromedially towards the sternum and connects with its fellow; an anterolateral branch, which runs laterally anterior to the lateral leaf of the central tendon; a short posterior branch, which divides into a posterolateral ramus coursing behind the lateral leaf and a posterior (crural) ramus which supplies the crural fibres. Posterolateral and crural branches may arise separately from the phrenic nerve. These main branches may be submerged in diaphragmatic muscle or lie below it. They supply motor fibres to the muscle and sensory fibres to the peritoneum and pleura related to the central part of the diaphragm. They also relay proprioceptive fibres from the musculature. The right phrenic nerve supplies the part of the right crus to the right of the oesophagus, and the left phrenic nerve supplies the left crus and the part of the right crus that lies on the left of the oesophagus. Phrenic rami connect with branches of the coeliac plexuses on the inferior surface of the diaphragm, and there is a small phrenic ganglion on the right, at the junction of the plexuses. Rami from the plexuses supply the suprarenal glands and, on the right, the hepatic falciform and coronary ligaments, the inferior vena cava and, possibly (via connections with coeliac and hepatic plexuses), the gallbladder.

Lesions of the phrenic nerve

An appreciation of the location of the main branches of the phrenic nerves is important to avoid iatrogenic surgical damage. Radial incisions in the diaphragm from the costal margin to the oesophageal hiatus lead to diaphragmatic paralysis, whereas thoracoabdominal incisions in a circumferential manner in the periphery of the diaphragm do not involve any significant branches of the phrenic nerves and preserve diaphragmatic function. Similarly, incisions of the central tendon are safe.

Division of the phrenic nerve in the neck completely paralyses the corresponding half of the diaphragm, which atrophies. If an accessory phrenic nerve exists, section or crushing of the main nerve as it lies on scalenus anterior will not produce complete paralysis. The phrenic nerve may be involved with traumatic lesions of the upper brachial plexus. Historically, it was deliberately injured in order to collapse, and hence rest, the lung in patients with pulmonary tuberculosis. Cardiac surgery is one of the most common medical causes of phrenic nerve injury, especially as a result of the instillation of saline slush for myocardial preservation. Other causes include thoracic surgery, tumours of the lung or mediastinum, and infections such as polio. Respiratory muscle weakness of rapid onset is a feature of Guillain–Barré syndrome.

Phrenic nerve damage leads to paradoxical movement of the diaphragm that is best observed fluoroscopically, with the patient first in the upright position (diaphragm unloaded), and then supine with a small weight on the abdomen (diaphragm loaded). Diaphragmatic paralysis can also be assessed by ultrasound examination with a sniff manoeuvre. The ‘gold standard’ for assessment of the phrenic nerve/diaphragm unit is electrical or magnetic stimulation of the phrenic nerve with recording of the compound muscle action potential and/or the transdiaphragmatic pressure. Electrical stimulation of the diaphragm, by ‘pacing’ of one or both phrenic nerves, has been used with some success in infants with central alveolar hypoventilatory syndrome (‘Ondine’s curse’) and in patients with high cervical lesions of the spinal cord, in whom the diaphragm is paralysed but the lower motor neurones are intact. Electrodes are placed adjacent to the nerves, sometimes in the neck but more usually in the chest, and a ventilatory rhythm is established by trains of stimuli delivered by an implanted device. Because this is an unphysiological way of recruiting the muscle, the fibres must be ‘conditioned’ during the initial period of stimulation, so that they acquire the necessary resistance to fatigue.

ANATOMY OF BREATHING

Breathing is a highly coordinated abdominal and thoracic process. The diaphragm is the major muscle of inspiration, responsible for approximately two-thirds of quiet breathing in healthy humans. The external intercostal muscles are most active in inspiration, and the internal intercostals, which are not as strong, are most active in expiration. Increasing the vertical, transverse and anteroposterior dimensions of the chest increases the volume of the pleural space, and the resulting decrease in intrapleural pressure draws air into the lungs. During expiration, the diaphragm relaxes and moves superiorly. Air is expelled from the lungs and the elastic recoil of the lung creates a subatmospheric pressure that returns the lateral and anteroposterior dimensions of the thorax to normal (De Troyer & Estenne 1988, Celli 1998).

During inspiration, the lowest ribs are fixed, and contraction of the diaphragm draws the central tendon downwards. In this movement, the curvature of the diaphragm is scarcely altered. The cupolae move downwards and a little forwards almost parallel to their original positions. The associated downward displacement of the abdominal viscera is permitted by the extensibility of the abdominal wall, but the limit of this extensibility is soon reached. The central tendon, its motion arrested by the abdominal viscera, then becomes a fixed point from which the fibres of the diaphragm continue to contract. This causes the second to tenth ribs to be elevated and the inferior portions of the ribs are turned outwards as a result of direct transmission of pressure through the zone of apposition (Fig. 58.4). The medial aspect of the rib is elevated and this increases the transverse dimension of the chest in the same manner as a bucket handle swinging outwards (Fig. 58.5A). This effect is most evident in the lower ribs (seventh to tenth ribs). Movements at the costovertebral joints cause elevation of the anterior ends of the ribs that push the body of the sternum and the upper ribs forwards. This ‘pump handle’ movement is most evident in the superior ribs (second to sixth ribs) and increases the anteroposterior dimension of the thorax (Fig. 58.5B). The right cupola of the diaphragm, which lies on the liver, has a greater resistance to overcome than the left, which lies over the stomach, and so the right crus and the fibres of the right side are more substantial than those of the left. The balance between descent of the diaphragm, protrusion of the abdominal wall (‘abdominal’ breathing), and elevation of the ribs (‘thoracic’ breathing) varies in different individuals and with the depth of ventilation. The thoracic element is usually more marked in females, but increases in both sexes during deep inspiration.

image

Fig. 58.4 Inspiratory movements: pressure changes during inspiration.

(Adapted from Drake, Vogl and Mitchell 2005.)

Diaphragmatic excursion is typically 1.5 cm in quiet breathing. During deep ventilation, the maximum movement ranges from 6 to 10 cm. After a forced inspiration, e.g. when breathing is partially obstructed, the right cupola of the diaphragm can descend to about the level of the eleventh thoracic vertebra, while the left cupola may reach the level of the body of the twelfth thoracic vertebra. After a forced expiration, the right cupola of the diaphragm is level anteriorly with the fourth costal cartilage, laterally with the fifth, sixth and seventh ribs, and posteriorly with the eighth rib, and the left cupola is a little lower.

The level of the diaphragm is affected by the phase and depth of ventilation, and by the degree of distension of the stomach and intestines and the size of the liver. Radiographs show that the height of the diaphragm within the thorax also varies considerably with posture. It is highest when the body is supine, and in this position it performs the greatest ventilatory excursions with normal breathing. When the body is erect, the diaphragm is lower, and its ventilatory movements become smaller. The diaphragmatic profile is still lower in the sitting posture, and ventilatory excursions are smallest under these conditions. When the body is horizontal and on one side, the two halves of the diaphragm do not behave in the same way. The uppermost half sinks to a lower level than that seen when sitting, and moves little with ventilation. The lower half rises higher in the thorax than it does even in the supine position, and its ventilatory excursions are considerably greater. Changes in the level of the diaphragm with alterations in posture explain why patients with severe dyspnoea are most comfortable, and least short of breath, when sitting up.

The primary role of the intercostal muscles is to stiffen the chest wall, preventing paradoxical motion during descent of the diaphragm in inspiration. This becomes most obvious immediately after high spinal injury, when there is flaccid paralysis of the entire trunk and only the diaphragm is left functioning. In a healthy adult with a vital capacity of 4.5 L, some 3 L is accounted for by diaphragmatic excursion. Immediately after high spinal injury, the vital capacity decreases to about 300 mL, even though the diaphragm is moving maximally, because some 2.7 L is lost by paradoxical incursion of the flaccid chest wall as the diaphragm descends. With time (usually several weeks), the paralysis becomes spastic, stiffening the chest wall, and the vital capacity increases towards its phrenic limit of about 3 L.

In the same way, high spinal injury reveals the role of the abdomen in inspiration and expiration. The abdominal musculature plays a major role in active expiration in man. During the flaccid stage of high spinal paralysis, the only mechanisms available for returning the relaxed diaphragm into the thorax on expiration are passive recoil of the lungs and chest wall, and the weight of the abdominal viscera. The latter is the most important, and operates only when patients are lying down. If they are sat up or raised upright, they are unable to breathe out. Trussing the abdomen with an elastic binder can help such patients. Conversely, when paralysis becomes spastic, the stiff abdominal wall opposes inspiration.

The role of the abdomen in breathing is often underestimated. If, for example, the anterolateral wall were made of steel and linked the pelvic rim rigidly to the costal margins, inspiration would be impossible. The diaphragm could not descend (because the abdominal contents are incompressible), and the ribs could not rise (because the links to the pelvis would be inextensible). During normal breathing, the abdomen relaxes as the diaphragm contracts. It is possible to oppose this motion by tensing the abdomen, as in the ‘beach posture’ adopted to exaggerate the size of the chest. In this case, the abdominal contents fix the central tendon of the diaphragm, so that it raises the ribcage as it contracts, but it is a condition of that manoeuvre that the gap between the ribs and the pelvic rim widens.

The ventilatory muscles must also work during sleep, when the pharyngeal muscles relax and upper airway resistance increases. It is now appreciated that in some people, particularly the obese, this relaxation can lead to periodic apnoea and marked hypoxia during sleep, implying that the pharyngeal muscles play an important ventilatory role in waking life. It is also clear that although ventilatory muscles rarely tire in normal life, they do fatigue when placed under abnormal loads, e.g. in chronic obstructive pulmonary disease.

The different pulmonary regions do not all move equally in ventilation. In quiet ventilation, the juxtahilar part of the lung scarcely moves and the middle region moves only slightly. The superficial parts of the lung expand the most, and the mediastinal surface, posterior border and apex move less, because they are related to less movable structures. The diaphragmatic and costomediastinal regions expand most of all. Most of the volumetric change during ventilation occurs in the alveoli.

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