Respiratory diaphragm and phrenic nerves


The respiratory diaphragm is a domed musculofibrous sheet, approximately 2–4 mm thick that separates the thoracic and abdominopelvic cavities ( Fig. 55.1 ). The superior surface of the respiratory diaphragm is mainly convex and forms the floor of the thoracic cavity. It is covered by a layer of phrenicopleural fascia, a continuation of the endothoracic fascia, covered in turn by a layer of diaphragmatic parietal pleura, except in the region inferior to the heart, which is covered by a layer of parietal serous pericardium. The concave inferior surface of the respiratory diaphragm forms the roof of the abdominopelvic cavity and is mostly covered by a layer of diaphragmatic fascia, a continuation of the transversalis fascia, which is then covered by a layer of parietal peritoneum. The position of the domes or cupulae of the respiratory diaphragm is variable and may be altered by body position, ventilatory phase, thoracic cavity morphology, height and body mass. Conditions resulting in lung over-inflation, e.g. emphysema, cause diaphragmatic depression or flattening. Usually, after forced expiration, the right dome is level with the fourth costal cartilage anteriorly, whereas the left dome lies approximately one costal cartilage level lower. At end tidal inspiration in the supine position, the domes of the diaphragm descend to sit at the level of the fifth intercostal space anteriorly on the right and sixth rib on the left. On a posteroanterior (PA) chest radiograph at full inspiration, the highest point of the right hemidiaphragm is located at the anterior end of the sixth rib, or at the posterior end of the tenth rib; the left hemidiaphragm is normally 1.5–2.5 cm lower (see Fig. 56.17A ). Unilateral paralysis may be seen as a raised hemidiaphragm on a chest radiograph, but this sign may be inconsistent.

Fig. 55.1
B–E , Axial T2-weighted MRI images through the upper abdomen showing the posterior diaphragmatic attachments and hiatuses from superior to inferior. Key: a, aorta; i, inferior vena cava; l, left crus of respiratory diaphragm; o, oesophagus; r, right crus of respiratory diaphragm.

A, With permission from Drake RL, Vogl AW, Mitchell AWN (eds) Gray’s Anatomy for Students, 3rd ed. Elsevier, Churchill Livingstone. Copyright 2015.

In the erect position the amount of respiratory diaphragmatic excursion is approximately 1–2 cm during quiet breathing and 5–7 cm during deep breathing; all movements are slightly greater in males compared to females ( , ). The diaphragm lies more superiorly in the supine compared to the erect position. In the lateral decubitus position the lowermost gravity-dependent dome of the diaphragm sits at a higher level than the uppermost dome; this results in greater diaphragmatic muscle displacement, and therefore ventilation, on the gravity-dependent side ( ).

Movement of the respiratory and pelvic diaphragms is often complementary. Magnetic resonance imaging has shown the respiratory and pelvic diaphragms to move symmetrically during normal respiration and other physiological processes: as the respiratory diaphragm descends during inspiration, the pelvic floor also descends in response to the change in intra-abdominal pressure. These changes assist with supporting the trunk and maintaining urinary continence during respiration and coughing ( ).

Attachments and Components

The respiratory diaphragm consists of a central tendinous portion, the central tendon, and a muscular peripheral portion. The muscle fibres arise from the circumference of the inferior thoracic aperture and converge to an attachment to the central tendon; the posterior and lateral attachments are therefore located relatively inferior to the anterior attachments ( Fig. 55.2 ) ( ). The muscle can be considered in three parts, sternal, costal and lumbar. The sternal part is the smallest and varies in size and presence, it may be a broad and continuous band or may be absent ( ). It commonly arises as two muscular strips from the posterior surfaces of the rectus sheath and the xiphoid process, near its apex. On each side, the costal part arises from the internal surfaces and superior margins of the lower six costal cartilages and their adjoining ribs, and interdigitates with transversus abdominis (see Fig. 53.15A ) ( ).

Fig. 55.2, The respiratory diaphragm with attachments, openings and arterial blood and nerve supply.

The right and left sternocostal triangles (of Morgagni) are openings in the anterior part of the diaphragmatic muscle, between the sternal and costal parts ( ). They are covered by connective tissue and are the conduits by which the internal thoracic vessels access the anterior abdominal wall. A retrosternal (parasternal) hernia can pass through the triangles: it is more common on the right side and often congenital, which may reflect a deficit of muscle fibres in this region.

The lumbar part arises from two aponeurotic arches, the medial and lateral arcuate ligaments (Haller’s or the lumbocostal arches), and asymmetrically from the more superiorly located lumbar vertebral bodies via the left and right crura. The medial arcuate ligament covers the upper part of psoas major. Medially, it is continuous with the lateral tendinous margin of the corresponding crus and is attached to the side of the first or second lumbar vertebral body. Laterally, it is fixed to the anterior aspect of the transverse process of the first lumbar vertebra. The lateral arcuate ligament covers and arches across quadratus lumborum, attaching medially to the anterior aspect of the transverse process of the first lumbar vertebra, and laterally to the inferior margin of the midpoint of the twelfth rib ( ).

The lumbocostal triangle (of Bochdalek) represents a developmental defect resulting from an incomplete formation of the pleuroperitoneal membrane. When present, it is located in the posterolateral diaphragm between the lumbar and costal parts, superior to the lateral arcuate ligament. The lumbocostal triangle is devoid of muscle fibres, covered only by the diaphragmatic parietal pleura superiorly and parietal peritoneum inferiorly ( ), and is the most common route for congenital diaphragmatic herniation.

The crura are tendinous at their attachments to the lumbar vertebrae and blend with the anterior longitudinal ligament (see Fig. 55.1 ). The broader and longer right crus arises from the anterolateral surfaces of the bodies and intervertebral discs of the superior three lumbar vertebrae. The left crus arises from the corresponding parts of the superior two lumbar vertebrae and intervertebral disc. The medial tendinous margins of the crura meet in the midline to form the median arcuate ligament, an often poorly defined tendinous arch that crosses anterior to the aorta at the level of the body of the twelfth thoracic vertebra (range, vertebral body of T10–L1). The crura vary greatly in length, thickness and the ratio of muscle to tendon ( , ).

The muscle fibres of the sternal, costal and lumbar parts of the respiratory diaphragm converge into the central tendon. Fibres from the xiphoid process are short, run almost horizontally and are occasionally aponeurotic. Fibres originating from the medial and lateral arcuate ligaments, and particularly the osteochondral surfaces of the ribs, are much longer. They arise almost vertically at first and then curve towards their central attachment. The right crus is commonly divided into three bundles of fibres (medial, middle and lateral), whereas the left crus is divided into two (medial and lateral) ( ). Muscle fibres from the crura diverge, the most lateral fibres pass more laterally as they ascend to the central tendon. Medial fibres of the right crus ascend and loop around the oesophagus where it passes through the diaphragm at the oesophageal hiatus; the more superficial fibres form the left margin, and the deeper fibres form the right margin of the hiatus. Multiple different patterns of crural muscle fibre arrangement may occur around the oesophageal hiatus ( ). 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 caval foramen; this fasciculus does not normally pass around the oesophageal hiatus on the right side.

The central tendon of the respiratory diaphragm is a thin but strong aponeurosis of closely interwoven fibres situated near the centre of the muscle. In the anteroposterior plane, it sits closer to the anterior thoracic wall, which means that the posterior muscle fibres are longer than the anterior fibres ( Fig. 55.3 ). The central region of the central tendon lies immediately inferior to the pericardium, with which it partially blends. This region consists of four diagonal bands of fibres that fan out from a thick central node; from here, compressed tendinous strands decussate anterior to the oesophagus and to the left side of the inferior vena cava.

Fig. 55.3, Superior and inferior views of the respiratory diaphragm. A , Superior view showing the relationship between the central tendon and muscular components, and the prominent relationship between the diaphragm and the pericardium. Key: 1, anterior oesophageal plexus; 2, azygos vein; 3, costodiaphragmatic recess; 4, costomediastinal recess; 5, fibrous pericardium (cut edge); 6, head of left rib 9; 7, hemiazygos vein; 8, inferior vena cava; 9, intervertebral disc; 10, left greater thoracic splanchnic nerve; 11, left internal thoracic artery; 12, left musculophrenic artery; 13, branches of the left phrenic nerve; 14, left sympathetic trunk; 15, muscle of diaphragm; 16, oesophagus; 17, mediastinal parietal pleura (cut edge); 18, posterior oesophageal plexus; 19, right phrenic nerve; 20, seventh left costal cartilage; 21, spinal cord; 22, left folia of central tendon; 23, right folia of central tendon; 24, descending thoracic aorta; 25, thoracic duct. B , Inferior view showing muscular fibres attaching onto the central tendon, and associated openings and vasculature. Key: 1, abdominal aorta; 2, azygos vein; 3, cauda equina; 4, central tendon of the diaphragm; 5, costal cartilage (cut); 6, muscle of the diaphragm; 7, erector spinae muscle group; 8, L1–L2 intervertebral disc; 9, hemiazygos vein; 10, inferior phrenic vessels; 11, caval foramen; 12, left crus of respiratory diaphragm; 13, thoracolumbar fascia; 14, median arcuate ligament; 15, oesophagus (abdominal part); 16, psoas major; 17, quadratus lumborum; 18, right crus of respiratory diaphragm; 19, spinal cord.

The central tendon is classically described as being trifoliate (cloverleaf) in shape, with middle, right and left folia. The middle folium projects anteriorly and is an equilateral triangle in shape, with the apex directed towards the xiphoid process. The right and left folia are tongue-shaped and similar in length, although the left may be narrower; both curve posterolaterally to form a V-shape that spans the midline. The size and shape of the folia and the ratio of diaphragmatic muscle to tendon varies between individuals, the most common arrangement being a V-shaped central tendon and a 10–15% muscle to tendon ratio ( ). The muscle to tendon ratio can vary disproportionately, such that larger respiratory diaphragms may have a small central tendon, and smaller diaphragms may have a large central tendon and a relatively small amount of muscle.

Profile and Relations

The superior surface of the respiratory diaphragm is covered by three separate serous membranes. On each side, the diaphragmatic parietal pleura separates it from the base of the corresponding lung. Centrally, the parietal pericardium separates mainly the middle folium of the central tendon from the inferior surface of the heart. The middle folium is almost flat and extends more to the left than the right. From an anterior view, the smooth convex domes or cupulae of the left and right sides of the diaphragm rise above the middle folium: the right cupula is higher and slightly broader than the left. Most of the inferior surface of the diaphragm is covered by diaphragmatic fascia and parietal peritoneum. The right cupula conforms to the convex surface of the right lobe of the liver, right kidney and right suprarenal gland; the left cupula conforms to the surface of the left lobe of the liver, gastric fundus, spleen, left kidney and left suprarenal gland. Given the differences in their profiles and anatomical relationships, clinical descriptions of the respiratory diaphragm should always reference a specific side.

The diaphragm is connected to closely related organs by various connective tissue formations known as ligaments. Within the thoracic cavity, the inferior pulmonary ligament, a double-layered fold of parietal pleura, connects the inferior part of the hilum and root of the lung and the mediastinal surface of the inferior lobe of the lung to the diaphragm. The phrenico-oesophageal ligament, formed from peri-oesophageal areolar tissue, connects the diaphragm to the oesophagus as it passes through the oesophageal hiatus. Within the abdominopelvic cavity, a number of peritoneal formations form a series of supportive ligaments. The falciform ligament connects the anterior surface of the liver to the diaphragm and rectus sheath. The right and left coronary and triangular ligaments pass to the diaphragmatic surface of the liver forming the boundaries of the bare area of the liver. The phrenicosplenic and phrenicocolic ligaments connect the diaphragm to the spleen and splenic flexure of the colon, respectively. The suspensory muscle of the duodenum (ligament of Treitz) is formed from a series of muscular bands that originate from the left crus and connect to the duodenojejunal flexure ( ).

Ultrasound imaging

Ultrasound examination of the posterior and lateral aspects of the respiratory diaphragm is best undertaken with the patient in the supine position, to limit veiling by other organs and reducing the risk of misdiagnosis due to underlying pulmonary pathologies. The respiratory diaphragm is typically identified by its curved morphology, deep location and specific echotexture. It is visualized as a thin, muscular hypoechoic line wedged between two hyperechoic layers consisting of parietal peritoneum and pleura ( Fig. 55.4 ). During inspiration, the hypoechoic line thickens as the muscle contracts, making it more visible. An atrophic diaphragm may be suspected when the thickness of this line does not change during inspiration. The left side of the diaphragm often poses more of a challenge in visualization ( ).

Fig. 55.4, Ultrasound of the respiratory diaphragm at the level of the eighth left intercostal space in the midaxillary line. The diaphragm is visualized as a hypoechoic (dark) line sitting between two hyperechoic (light) layers consisting of the parietal peritoneum and the parietal pleura.

Openings

A number of structures pass between the thorax and abdomen via openings (apertures) in the respiratory diaphragm. There are three large openings, for the aorta, oesophagus and inferior vena cava, and a number of smaller openings (see Figs 55.1A , 55.3 ).

The aortic hiatus transmits the aorta, thoracic duct, lymphatic trunks from the lower posterior thoracic wall and, sometimes, the azygos and hemiazygos veins. It is the most posteroinferior of the openings, and is commonly found at the level of the superior half of the body of the twelfth thoracic vertebra (range, vertebral body of T10 to L1), slightly to the left of the midline. It is an osseo-aponeurotic opening bordered by the diaphragmatic crura laterally, the vertebral column and anterior longitudinal ligament posteriorly and the median arcuate ligament anteriorly; the aorta therefore normally passes posterior to the diaphragmatic musculature and as such is not affected by its contraction ( ). Occasionally, some tendinous fibres from the medial parts of the crura also pass posterior to the aorta, converting the osseo-aponeurotic hiatus into an aponeurotic fibrous ring.

The oesophageal hiatus transmits the oesophagus, anterior and posterior vagal trunks, gastric nerves, oesophageal branches of the left gastric vessels and lymphatic vessels. It is commonly located level with the inferior half of the body of the eleventh thoracic vertebra (range, vertebral body of T9 to L1–L2 intervertebral disc), anterosuperior to, and to the left of, the aortic hiatus. The elliptical hiatus has a slightly oblique long axis, and is bounded by muscle fibres that originate from the medial part of the right crus and cross the midline, forming a tunnel approximately 2.5 cm long that accommodates the distal part 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 hiatus. The fascia on the inferior surface of the diaphragm, rich in elastic fibres, is continuous with the transversalis fascia and extends superiorly into the oesophageal hiatus in the shape of a flattened cone to blend with the oesophageal wall 2–3 cm superior to the gastro-oesophageal (squamocolumnar) junction. Some of its elastic fibres penetrate to the submucosa of the oesophagus. This peri-oesophageal areolar tissue forms the phrenico-oesophageal ligament, that connects the oesophagus flexibly to the diaphragm, thus permitting freedom of movement during swallowing and ventilation while synchronously limiting superior oesophageal displacement.

The caval foramen transmits the inferior vena cava, which adheres to its margins, and branches of the right phrenic nerve (see Fig. 55.1A ). It is the most superior of the three large openings, and lies approximately level with the superior part of the body of the eleventh thoracic vertebra (range, T8–T9 intervertebral disc to the body of the twelfth thoracic vertebra). Quadrilateral in shape with aponeurotic margins, it is located at the junction of the right folium of the central tendon with the central part. During inspiration, dilation of the caval foramen, combined with increased intra-abdominal pressure, increases cardiac venous return ( ).

Two smaller openings within each crus transmit the greater and lesser thoracic splanchnic nerves. The ganglionated sympathetic trunks usually enter the abdominal cavity posterior to the respiratory diaphragm, deep to the medial arcuate ligaments. There are frequently openings for small veins in the central tendon.

On each side of the respiratory diaphragm, small areas of muscle may be replaced by areolar tissue. The superior epigastric branch of the internal thoracic artery and some lymph vessels from the abdominal wall and convex surface of the liver pass through an area of areolar tissue covering the sternocostal triangle (between the sternal and costal attachments of the respiratory diaphragm). An inconstant area of areolar tissue between the costal attachment and the fibres that originate from the lateral arcuate ligament may be all that separates the diaphragmatic parietal pleura from the posterosuperior surface of the kidney. Additional smaller fascial spaces may be found throughout the lateral aspects of the domes of the diaphragm without evidence of vascular penetration. Although these spaces are found on both the left and right sides, they appear to be more numerous on the left ( ).

Oesophageal reflux

Reflux of gastric contents into the oesophagus, with risk of pulmonary aspiration, is normally prevented by the specialized smooth muscle of the inferior oesophageal wall and the encircling crural muscle fibres forming a physiological barrier at the gastro-oesophageal junction. The diaphragm acts as a ‘physiological’ sphincter to prevent gastro-oesophageal reflux by constricting during inspiration ( ) (see also Ch. 63 ).

Hiatus hernia

Deep inspiration followed by closure of the glottis and contraction of the muscles of the abdominal and thoracic walls provides additional power to all expulsive efforts including sneezing, coughing, laughing, crying, urination, defecation, vomiting and uterine fetal expulsion. The resulting increase in intra-abdominopelvic pressure can also be used to provide an anteriorly located pneumatic support to the vertebral column when lifting heavy objects. Repeated mechanical stress may eventually compromise the integrity of the oesophageal hiatus, leading to widening of the muscular hiatal tunnel. Concomitant laxity of the phrenico-oesophageal ligament allows the gastro-oesophageal junction to migrate into the posterior mediastinum, a condition that is normally termed a sliding (type I) hiatus hernia. Sliding hernias are typically acquired in the fifth decade of life, and are found in more than 50% of patients with gastro-oesophageal reflux. This reflux induces tonic contraction of the longitudinal oesophageal muscle, further exacerbating the hiatus hernia.

Herniation of the stomach into the thoracic cavity adjacent to the oesophagus is termed a para-oesophageal (type II) hiatus hernia. There are three distinct types: II, III and IV. Type II refers to a herniated stomach with normal positioning of the gastro-oesophageal junction. Type III, a ‘mixed’ hernia, refers to both a herniated stomach and a sliding-type hernia. Type IV refers to a hernia in which more than one-third of the stomach is herniated into the thoracic cavity. Para-oesophageal herniae can be diagnosed with barium swallow, CT or endoscopy ( ).

Congenital hernia

Congenital respiratory diaphragmatic defects may cause abdominal organs, usually the stomach and/or the small bowel, colon, liver and spleen, to herniate through the diaphragm into the thoracic cavity; they are described in Chapter 20 .

Eventration

Eventration is a focal bulge, usually located in the anteromedial segment of the muscular portion of the diaphragm. It is most often caused by a congenital thinning of the diaphragmatic muscle: such regions are covered by a thin fibroelastic connective tissue that stretches over time: eventration may be mistaken for a diaphragmatic hernia.

Eventration may be congenital or acquired as a result of pathological processes, including malignancy, trauma, infection and obesity. On X-ray imaging, the affected region appears as an elevated hump on a hemidiaphragm with an otherwise normal contour; there is often a sharp transition between the area of eventration and the surrounding normal diaphragm. The elevation becomes more pronounced with increased abdominal pressure and is typically found on the left; the affected part shows diminished or paradoxical movement during inspiratory ‘sniff’ testing while the posterior aspect of the ipsilateral dome acts normally ( ). Eventration and hemidiaphragmatic paralysis are differentiated by the amount of diaphragm involved: specifically, eventration involves only a part of a hemidiaphragm. Management is usually conservative but more aggressive treatment might be warranted should the patient become symptomatic, e.g. worsening dyspnoea, chronic atelectasis or recurrent pneumonia ( ).

Diaphragmatic trauma

Closed or penetrating thoraco-abdominal injuries may result in rupture or laceration of the diaphragm. With closed injuries and diaphragmatic rupture, abdominal contents may herniate into the thorax. CT imaging with planar reformation should be the primary mode of investigation ( ): magnetic resonance imaging is usually performed when other imaging modalities have produced equivocal findings. Early operative repair is recommended because untreated cases may develop gastrointestinal obstruction or perforation. Patients with penetrating injuries may require additional assessment by thoracoscopy ( ).

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