Embryology, anatomy, and physiology

The diaphragm is a musculotendinous organ that separates the thoracic cavity from the abdominal cavity. This important organ arises from the confluence of the abdominal peritoneum and the parietal pleural during the first trimester of pregnancy. The early muscular ingrowth is an extension from the circumference of the thoracic inlet, specifically, the posterior sternal border, the inner surfaces of the lower six costal cartilages, and the posterior lumbocostal arches. During the first trimester, these three muscular groups migrate toward each other and fuse together as a central tendon that has three leaflets, namely, the left, right, and central leaflets ( Figs. 1 , 2 ). The most medial posterior margins of this muscular complex evolve as the crura. The central leaflet is located posterior to the sternum and inferior to the heart; this leaflet contributes to the pericardial fibers. The right and left leaflets are located posterolaterally in each hemithorax and are the last to mature by the end of the first trimester. Incomplete closure of the left posterior lateral leaflet results in herniation in the left posterior lateral foramen of Bochdalek. Incomplete closure of the right leaflet is less crucial clinically because of the buttressing effect of the liver. Closure of the pleural and peritoneal surfaces without interposition of muscle as a central tendon results in an eventration of the diaphragm, which may be an important consideration in the differential diagnosis of blunt diaphragmatic injury ( Figs. 3 , 4 ).

FIGURE 1, Inferior view of the diaphragm highlighting the posteriorly located foramina and central tendon. IVC, inferior vena cava.

FIGURE 2, Lateral view of the diaphragm. Note, xiphoid and sternal attachments anteriorly and the extension of the crus posteriorly. IVC, inferior vena cava.

FIGURE 3, Preoperative anterior-posterior (A) and lateral (B) views of eventration misdiagnosed as ruptured diaphragm after motor vehicle collision.

FIGURE 4, Postoperative view after placation of eventration misdiagnosed as ruptured diaphragm.

This circular, domed muscle fluctuates widely during the ventilatory cycle. During full expiration, the diaphragmatic dome extends high into the thoracic cavity, whereas during forced inspiration, the central tendon contracts inferiorly, and the diaphragm becomes more platelike. Full inspiration reduces the intrathoracic pressure and raises the intra-abdominal pressure, whereas full expiration has the opposite effect. The excursion of the diaphragm during forced expiration is great as the dome of the diaphragm elevates to the level of the fourth intercostal space at the sternal junction on the right side and to about the level of the fifth intercostal space on the left side. During forced inspiration, the diaphragm descends inferiorly at least three intercostal spaces. The most inferior extension posteriorly occurs at the crura.

The right crus arises from the bodies and fibrocartilages of the lumbar vertebrae one through three, whereas the smaller left crus arises from the first and second lumbar vertebrae. They join superiorly to encompass the esophagus at the esophageal foramen. The posterior lateral sulcus or recess of the diaphragm is directly posterior to many of the intra-abdominal organs, and the posterior sulcus extends inferiorly to the midportion of the kidneys. This inferior extension is often not appreciated when patients with upper abdominal gunshot wounds or stab wounds are treated for intra-abdominal injuries; thus, perforation of the diaphragm in this posterior area is easily overlooked. When this occurs, a coexistent hemothorax is often diagnosed postoperatively. Careful intraoperative inspection followed by repair and tube thoracostomy precludes the development of this late complication.

The diaphragm has three major foramina (see Fig. 1 ). The aortic hiatus is the most posterior, located between the diaphragmatic muscle and the 12th vertebral. The esophageal foramen lies anterior to the aortic foramen and is bordered by the strong muscular crura; the left crus encircles the esophagus and contributes to the lower esophageal sphincter. Immediately posterior to the esophagus, sinuous fibers from each hemidiaphragm join as the median arcuate ligament, which is anterior to the aorta and superior to the celiac axis. Immediately posterior to the esophageal foramen on the right side is the foramen for the inferior vena cava (see Fig. 1 ). The anterior foramen of Morgagni is in the retroxiphoid space; the internal mammary arteries pass through this foramen while exiting the mediastinum prior to dividing into the superior epigastric arteries and the subcostal arteries. The accompanying veins follow the same course.

The median plane of the diaphragm extending from the foramen of Morgagni to the esophageal foramen, the so-called median raphe, is less vascular than the more lateral muscular portions of the diaphragm (see Fig. 2 ). This plane can be divided to provide better exposure to the inferior mediastinum. Care must be taken, however, to prevent injury to the phrenic vein, which may cross this median plane about 1 cm above the esophageal hiatus. This vein, if not controlled while dividing the median raphe between the foramen of Morgagni and esophageal hiatus, can lead to major hemorrhage.

The diaphragm is innervated by the phrenic nerves, which arise from the cervical portion of the spinal cord, namely, C3, C4, and C5 (see Fig. 1 ). After these nerves exit the neck, they pass through the mediastinum to the medial portion of the right and left hemidiaphragms. They then branch laterally, like a fan, from the central medial portion of each hemidiaphragm to the anterior, lateral, and posterior bony attachments (see Fig. 1 ). Ideally, one should protect these nerves while performing surgery on the diaphragm; this may be accomplished by detachment of the diaphragmatic muscular insertion from the peripheral bony insertions. This is seldom necessary for patients with diaphragmatic injury. When the origins of the diaphragm are to be relocated for treatment of unusual injuries, however, care should be taken to protect the neural innovation as much as is practical.

Incidence of diaphragmatic injuries

Fair provided an excellent summary of the demographics of diaphragmatic injury obtained from the American College of Surgeons National Trauma Data Bank. These authors demonstrated that traumatic diaphragmatic injury (TDI) occurred in less than 0.5% of injured patients with the mechanism being blunt injury in 33% and penetrating wounds in 67%. Patients with blunt TDI were slightly older (44 vs. 33 years), had a higher Injury Severity Score (34 vs. 24), and a higher mortality (19.8% vs. 8.8%). Blunt TDI was associated with a higher incidence of an associated aortic injury (2.9% vs. 0.5%), lung injury (48% vs. 28%), bladder injury (5.9% vs. 0.7%), and splenic injury (44.5% vs. 29.1%). Penetrating TDI was associated with a higher incidence of liver injury (39% vs. 54%) and hollow viscus rupture (7% vs. 12%).

Other reports on the incidences of diaphragmatic injury vary widely. Asensio, in a multicenter review, reported a 3% incidence of diaphragmatic injuries for all patients sustaining torso trauma with a range of 0.8% to 5.8%; this wide range reflected the different types of injuries treated at each institution and the diligence one placed on confirming a diaphragmatic perforation. Rural trauma centers were more likely to treat patients with blunt diaphragmatic rupture, whereas penetrating diaphragmatic injury predominated in patients presenting to inner-city trauma centers.

The reported incidence of diaphragmatic rupture may also reflect the different therapeutic approaches to patients with both blunt and penetrating abdominal wounds. Most patients with penetrating stab wounds to the abdomen are now being treated nonoperatively when the patient exhibits no signs of peritonitis or hemoperitoneum. This is also true for patients with lower thoracic stab wounds causing hemopneumothorax. Previously, patients treated for penetrating stab wounds were more likely to undergo an exploratory laparotomy, leading to a higher incidence of confirmed asymptomatic diaphragmatic penetration, which was repaired. Likewise, many patients who have hemothorax after receiving an inferior thoracic stab wound are treated by tube thoracostomy alone without laparotomy if there is a benign abdominal examination. Some of these patients have unrecognized diaphragmatic perforation ( Fig. 5 ). Moreover, patients with through-and-through anterior to posterior right upper quadrant gunshot wounds near the liver and associated right-sided hemopneumothorax are being treated by tube thoracostomy alone, even though, almost certainly, there are at least two diaphragmatic perforations. The missile in this setting would pass through the lower rib cage anteriorly, enter the anterior hemithorax, pass through the anterior portion of the diaphragm, transit the liver, reenter the chest through to the posterior portion of the diaphragm, and exit through the posterior chest wall. When treated only with right tube thoracostomy for hemothorax, the diaphragmatic perforation is not diagnosed, and therefore, not coded in the trauma registry. When diagnostic peritoneal lavage (DPL) was performed routinely for patients with penetrating wounds of the lower rib cage, the effluent would be pink with a red cell count less than 100,000/cm 3 in patients with isolated diaphragmatic perforation. Laparotomy in these patients would confirm a diaphragmatic perforation, which was sutured, and the patient data were recorded in the trauma registry. The current trend for routine ultrasonography in patients with abdominal injury has replaced DPL; ultrasonography is less sensitive for identifying small amounts of blood. Consequently, clinically insignificant diaphragmatic perforations are not being recognized and are not coded in the trauma registry. Penetrating posterior diaphragmatic perforation after upper abdominal wounds may also go unrecognized despite laparotomy for repair of other intra-abdominal visceral injuries. The perforation may be missed because the missile is thought to have penetrated only the transversalis abdominus muscle. When a subsequent hemothorax appears, postoperatively, the treating physician, hopefully, will recognize that there was a missed diaphragmatic injury. Patients with blunt injury are less likely to have a diaphragmatic injury that is not recognized during the same hospitalization ( Fig. 6 ). There are, however, a number of patients who present with a diaphragmatic hernia years after major blunt torso trauma when diaphragmatic injury was not recognized initially. The use of prehospital endotracheal intubation may reduce a diaphragmatic hernia in transit, thus delaying the diagnosis of blunt diaphragmatic rupture.

FIGURE 5, (A) Anterior-posterior view of chest showing diaphragmatic hernia in patient treated 18 months earlier by tube thoracostomy for stab wound of left chest. (B) Gastrografin confirms the presence of stomach in the left hemithorax.

FIGURE 6, (A) Anterior-posterior chest x-ray demonstrates an apparent gastric bubble in the left hemothorax after blunt trauma. (B) Injection of contrast agent through the nasogastric tube confirms the gastric filling.

During the 1970s when routine laparotomy was performed for all penetrating abdominal wounds and careful examination of the inferior and posterior diaphragmatic extensions was routine, the incidence of diaphragmatic perforation was approximately 19% for upper abdominal gunshot wounds and 11% for upper abdominal stab wounds. Now that laparotomy for penetrating abdominal wounds is performed only for symptomatic or mentally impaired patients, the incidence of confirmed diaphragmatic perforation is about 8% for gunshot wounds and 2% for stab wounds. In contrast, the recent incidence of diaphragmatic injury in patients admitted after blunt torso injury is less than 1%; most patients with blunt rupture of the liver or spleen are treated nonoperatively. Patients requiring laparotomy for blunt abdominal injury have about a 3% incidence of diaphragmatic rupture.

Mechanism and location of injury

The location of diaphragmatic perforation also varies with mechanism of injury. The classic scenario for blunt diaphragmatic injury is a head-on motor vehicle collision or a T-bone impact causing a marked increase in the intra-abdominal pressure, thereby stretching the diaphragm to the point of rupture. The rupture typically occurs in the posterior lateral segment in the central tendon of the left diaphragm, often with extension into the muscular portion of the diaphragm. Blunt rupture can also occur after assaults, stompings, falls from a height, and with explosions. Although the posterior lateral location is the most common site for injury, rupture may occur adjacent to the esophageal hiatus, near the bare area of the liver on the right side, and in a subxiphoid location on either side ( Fig. 7 ).

FIGURE 7, (A) This 86-year-old man was hit by a bus and sustained right rib fractures, subcutaneous emphysema, and hemothorax. Note lack of clarity of the right costal phrenic angle. (B) Right chest tube yielded 500 mL of blood with continued bleeding of 300 mL during the next hour. Laparotomy revealed a large rent in the dome of the diaphragm and a type IV liver injury, which was repaired.

The review of 32 published series with 1589 patients by Asensio showed a distribution of left-sided rupture in 1187 patients (75%), right-sided ruptured in 363 patients (23%), and bilateral rupture in 39 patients (2%). This observation parallels the authors’ experience. The relative protection of the right hemidiaphragm, historically, has been attributed to the protective effects of the liver, which blunts the rapid rise in the intra-abdominal from being transmitted against the right hemidiaphragm. A less common explanation may reflect a weaker left hemidiaphragm that undergoes a later intrauterine closure; an inherent tendonous or muscular weakness, however, has not been demonstrated with carefully constructed bursting tests. The site of injury with penetrating wounds may be anywhere. Bilateral perforations are more likely with missiles. Stab wounds are more commonly located along the periphery of the left diaphragm since most assailants using a knife are right-handed.

Severity of injury

The severity of diaphragmatic injury is best judged by the organ injury scale for diaphragmatic injury developed by the American Association for the Surgery of Trauma. This Abbreviated Injury Scale identifies five grades of injury ( Table 1 ). Grade I injury is a contusion or hematoma without rupture. Grade II injury is a laceration less than 2 cm in diameter. Grade III rupture is a laceration greater than 2 cm but less than 10 cm in magnitude. Grade IV rupture is greater than 10 cm or has loss of diaphragmatic tissue that is <25 cm 2 . Grade-V injury is an extensive tear with tissue loss greater than 25 cm 2 .

TABLE 1
Abbreviated Injury Scale for Diaphragmatic Rupture
Grade Anatomic Description
1 Contusion or hematoma without rupture
2 Full-thickness laceration < 2 cm
3 Full-thickness laceration between 2 and 10 cm
4 Full-thickness laceration, or loss of tissue 10–25 cm
5 Extensive tear with loss of tissue > 25 cm 2

Grade 1 diaphragmatic contusions or hematomas may be seen with penetrating wounds that come in close proximity to the diaphragm without transgressing the full muscular layer. The authors have not treated a grade 1 injury due to blunt trauma. The grade 2 diaphragmatic injury is typically seen in patients with low-velocity gunshot wounds or penetrating stab wounds in the lower thoracic upper abdominal area. Grade 2 diaphragmatic ruptures following blunt injury are uncommon but may occur in proximity to the foramen of Morgagni or adjacent to the crura forming the esophageal foramen. Grade 3 diaphragmatic ruptures are more likely to be seen with higher-velocity gunshot wounds and with blunt trauma; the area of rupture following blunt trauma, usually, is the central tendon of the diaphragm in the posterior lateral location. Grade 4 diaphragmatic injuries may be seen with high-velocity rifle wounds or close-range shotgun blasts or after with a high-velocity blunt deceleration injury, which causes a tear that extends well beyond the central tendon. A grade 5 diaphragmatic rupture will almost never be seen with a penetrating wound unless the wound has caused associated injury to the adjacent rib cage; a blunt grade 5 rupture of the diaphragm would be very extensive and be associated with injuries to the surrounding ribs. Coexisting major organ injuries to the chest and/or abdominal organs are common in patients with grades 4 and 5 diaphragmatic ruptures.

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