Emergency Radiology (2001) 8: 6±14

Ó American Society of Emergency Radiology 2001

RE VI EW ARTICLE

Kathirkamanathan Shanmuganathan ´ Stuart E. Mirvis

CT diagnosis of diaphragm injuries

Abstract Admission supine chest radiographs are the initial and most commonly performed imaging study to evaluate the thorax following trauma. Whenever the chest radiograph is ambiguous or suggestive of a diagnosis of acute diaphragmatic injury, CT is the next study of choice since it is generally available and often used to examine other body regions of the polytraumatized patient. CT is usually diagnostic, particularly if supplemented by multiplanar reformations obtained using a thin slice thickness. Currently MR imaging is used at our trauma center to evaluate the diaphragm in patients with an indeterminate diagnosis after spiral CT. A limited MR imaging examination with T1-weighted sagittal and coronal imaging has been extremely accurate in establishing or excluding diaphragm injury. Key words Diaphragm injury ± Computed tomography ± CT ± MR imaging The initial diagnosis of diaphragm injury is often missed because distinct clinical and radiologic signs may be absent or subtle. Commonly, diaphragmatic injuries are associated with other major injuries to the solid organs, pelvis, central nervous system, and thoracic aorta that may divert attention from possible diaphragm injury [1, 2, 3]. Hence, diaphragm injury has always been a diagnostic challenge to both radiologist and trauma or emergency physician. A careful review of the literature indiK. Shanmuganathan ´ S. E. Mirvis Department of Diagnostic Radiology, Shock Trauma Center, University of Maryland School of Medicine, Baltimore, Maryland, USA

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K. Shanmuganathan ( ) Department of Radiology, University of Maryland Medical Center, 22 South Greene Street, Baltimore, MD 21201, USA e-mail: [email protected] Tel.: + 1-4 10-3 28 12 95 Fax: + 1-4 10-3 28 32 82

cates that most diaphragm injuries are caused by penetrating trauma (the ratio of penetrating to blunt trauma is 2:1) [3, 4, 5, 6]. Diaphragm injury occurs in 6 % of patients following major blunt force trauma to the lower chest or abdomen and in 3±8 % of patients undergoing emergency celiotomy following blunt abdominal trauma [7, 8, 9, 10, 11, 12, 13, 14, 15, 16]. Chest radiography serves today as the initial screening study performed to evaluate for diaphragm injury. Previous studies utilizing conventional CT have reported a poor accuracy in diagnosing diaphragm injury [17, 18]. However, more recent literature indicates that the ability to obtain high-quality axial images with coronal and sagittal reformations using spiral CT has improved accuracy in diagnosing diaphragm injury [19]. This article reviews recent imaging advances in spiral CT that are helpful in diagnosing diaphragm injury.

Anatomy The diaphragm is a thin, flat, half-dome-shaped muscle located between the pleuropericardial space above and the peritoneal space below. The most posterior portion of the diaphragm, the lumbar part, attaches to the medial and lateral arcuate ligaments and the periosteal surface of the upper three lumbar vertebrae on the right side and upper two vertebrae on the left side. Laterally the costal part attaches anteroposteriorly to the inner aspect of the sixth to twelfth ribs. The anterior diaphragm attaches anteriorly to the posterior aspect of the lower sternum and xiphoid process. Fibers from these three parts of the diaphragm converge to a central tendon. Three large openings interrupt the continuity of the diaphragm: the aortic hiatus, the lowest and most posterior, at the level of the thoracolumbar junction; the esophageal hiatus, at the level of the tenth vertebra; and the highest of the three, the inferior vena caval aperture, at about the level of the eighth vertebra. The abdominal surface of the diaphragm is covered by peritoneum and is in contact with the dome of the liver, fundus

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of the stomach, spleen, both kidneys and the adrenal glands.

Clinical diagnosis Primary clinical symptoms described in cases of diaphragmatic injury are generally related to lung compression by intra-abdominal viscera herniating into the thoracic cavity and referred pain from the diaphragm. These symptoms include chest pain, localized or diffuse abdominal pain, pain referred to the scapula or shoulder, dyspnea, and orthopnea. Physical findings described with diaphragmatic injury include diminished respiratory movement, prominence of the hemithorax, ipsilateral decrease or absence of breath sounds, displacement of the heart and mediastinum to the contralateral side, and auscultation of bowel sounds over the hemithorax. Guarding with localized or diffuse abdominal tenderness and a scaphoid abdomen may also be present if a large amount of intra-abdominal viscera herniates into the thoracic cavity. Since none of these symptoms or clinical findings are specific for diaphragm injury or may be overlooked because of more apparent or life-threatening concurrent injuries. A high index of suspicion is required to diagnose this injury in patients with an appropriate trauma mechanism [4, 14, 20].

Mechanism of injury Most blunt diaphragm injuries (up to 90 %) result from motor vehicle collisions [7, 8, 21]. The majority of diaphragm injuries diagnosed preoperatively following blunt trauma are more than 10 cm in length, but up to 84 % of the diaphragm tears resulting from penetrating injuries are less than 2 cm in length [21, 22]. A positive pressure gradient of 7±20 cmH2O exists between the peritoneal and pleural spaces. This gradient may facilitate herniation of abdominal viscera through a diaphragm rupture [23]. Multiple mechanisms of blunt diaphragm rupture have been proposed, including a sudden and abrupt increase in intraperitoneal pressure at the time of impact transmitted to the diaphragm by the abdominal viscera and leading to disruption. Right or left lateral impact can deform the chest wall resulting in avulsion of the costal portion of the diaphragm's attachments. Shearing forces can tear the stretched dome of the diaphragm. Finally, rib fracture fragments may directly penetrate the adjacent diaphragm [8, 24].

Anatomical location of injury A congenital weakness that exists along the embryonic fusion of the costal and lumbar parts of the diaphragm predisposes this site to injury [25]. Left-sided blunt hemidiaphragmatic injuries are usually located at the posterolateral aspect of the left hemidiaphragm between

the spleen and the abdominal aorta, extending medially in a radial orientation towards the central tendon. Following blunt trauma, left-sided hemidiaphragm injuries occur three times more commonly than right-sided injuries [8, 11, 21]. An equal incidence of left and right-sided hemidiaphragm injuries is seen in penetrating trauma and among blunt trauma victims who die before reaching definitive medical care [3, 4, 5]. Bilateral injuries of the hemidiaphragms are uncommon, and are reported in only 2±6 % of patients with diaphragm injury [4, 15, 22]. Patients with right-sided hemidiaphragm rupture have a higher prehospital mortality, a result of the greater impacting force required to cause this injury [3, 7, 8, 20, 22, 26]. The apparent low incidence of right-side hemidiaphragm injuries in clinical studies has been attributed to the mass of the liver preventing the transmission of intra-abdominal pressure to the right hemidiaphragm, and the subtlety of radiologic signs of right hemidiaphragm rupture without herniation of abdominal viscera. Experimental studies also consistently indicate that greater force is needed to rupture the right hemidiaphragm than the left.

Associated injuries The anatomical location of the diaphragm and its close proximity to adjacent intrathoracic and intra-abdominal organs accounts for the presence of associated injuries in 52±100 % of patients with diaphragm injuries [1, 7, 11, 15, 30]. Intrathoracic injuries such as pneumohemothoraces and multiple rib fractures are seen in 90 % of patients with blunt diaphragm injuries [30, 31]. Meyers and McCabe reported a 5 % incidence of aortic injury in 68 patients with diaphragm rupture at a level I trauma center [29]. Common associated intra-abdominal injuries involve the spleen in 60 % and liver in 93 % of patients with right- and 24 % of patients with left-sided diaphragm ruptures [7]. Other extrathoracic and extra-abdominal injuries include pelvic fractures (40±55 %), fractures of long bones (45±85 %), and closed head injuries (25±55 %) [27, 29].

Imaging of the diaphragm Chest radiographs Chest radiographs are the initial and most commonly performed imaging study to evaluate the diaphragm following trauma. There are two diagnostic radiographic findings of diaphragmatic rupture with concurrent visceral herniation. One is herniation of stomach or bowel above the hemidiaphragm with a focal constriction of the viscus at the site of tearing in the diaphragm from circumferential compression (ªcollar signº) (Fig. 1). The other is demonstration of the nasogastric tube (Fig. 2) or viscus above the injured hemidiaphragm in the lower hemithorax. Nonspecific chest radiographic

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Fig. 1 ªCollar signº. Admission chest radiograph of a 44-year-old male blunt trauma patient shows herniation of the stomach into the left hemithorax. A focal constriction (arrows) of the stomach is seen at the site of the diaphragmatic tear. Left rib fractures, shift of the mediastinum to the right side, and pulmonary contusion in the left lung is seen. (From [37], with permission)

post-traumatic pneumatoceles, loculated pneumothorax, aspiration pneumonia, phrenic nerve palsy, segmental or total congenital eventration of the hemidiaphragm, gastric dilatation, and subphrenic fluid collections. These findings can thus either mask or mimic the signs of diaphragm rupture and visceral herniation. Initial chest radiographs are normal or nonspecific in 20±50 % of patients with diaphragm injury. This may account for the great variability (7±66 %) of initially missed diaphragm injuries seen in polytrauma patients reported in the literature [3, 21, 22, 31, 33, 33]. The admission radiographs are diagnostic in 27±62 % of patients with left-sided and 18±33 % of cases with right-sided hemidiaphragm injuries [1, 17, 24, 30, 34, 35]. The chest radiographs are suggestive but not diagnostic in another 18 % of cases [27, 32]. Serial chest radiographs are often useful. As concurrent trauma-related acute pulmonary abnormalities in the lower thorax resolve, the findings of diaphragm injury may become more evident on chest radiographs obtained in the subacute or chronic phase. The diagnosis of diaphragm injury may be delayed for patients receiving positive-pressure ventilatory support, since the natural pressure gradient across the pleuroperitoneal cavity is abolished or reversed and visceral herniation may not occur until positive-pressure ventilator support is terminated [17, 30]. Computed tomography Technique

Fig. 2 Nasogastric tube above the injured hemidiaphragm. Admission chest radiograph shows herniation of the nasogastric tube (arrow) into the left hemithorax. The mediastinum is shifted to the right side. (From [37], with permission)

findings suggestive of a diaphragmatic rupture on a chest radiograph include obliteration of the outline of the diaphragm, distortion of the contour of the diaphragm, pleural effusion, apparent elevation of the hemidiaphragm, air±fluid levels in the lower thorax, and contralateral shift of the mediastinum. Often these nonspecific radiologic signs can result from traumatic and nontraumatic pathology in the lung bases such as atelectasis, pleural effusion, pulmonary contusion,

Conventional CT has a variable sensitivity of 14±61 % and a specificity of 76±99 % for diagnosing diaphragm rupture [6, 13, 27, 32, 34]. Limitations of conventional CT include difficulty in visualizing the entire domeshaped diaphragm on axially oriented images, low-resolution sagittal or coronal reformatted images performed with 8±10 mm axial slice thickness, and difficulty in differentiating the diaphragm from adjacent pulmonary pathology or normal soft tissue structures. Spiral CT can overcome these limitations through use of thin slice collimation and slice overlap to optimize z-axis resolution, the capacity to obtain a large volume of data during a single breath hold, and decreased motion and misregistration artifacts [36, 37]. The present authors currently use spiral CT to evaluate patients with chest radiographic findings suspicious for diaphragm injury. In the acute trauma patient, initial spiral CT using the standard protocol (8 mm section, pitch = 1) is performed to evaluate the chest, abdomen, and pelvis. Following completion of this study, scans are performed using a 5-mm collimation and table speed of 5 mm/s (pitch = 1) through the hemidiaphragm in question to the inferior margin of the liver. Overlapping reconstructed images are obtained at 2- or 3-mm intervals to perform sagittal and coronal reformations. Patients presenting with findings suggestive of diaphragm injury on chest radiographs in the subacute or chronic phase are also scanned

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A

C Fig. 3 A±C Defect in the continuity of the diaphragm and herniation of abdominal viscera. Conventional CT images of a 52-yearold patient admitted following a motor vehicle collision. A CT image at the level of the hilum of the liver shows an abrupt discontinuity of the left crus (arrow). Multiple splenic lacerations are seen with a perisplenic hematoma (arrowheads). B,C CT images in the mid thoracic region show herniation of the spleen (curved arrows) with multiple lacerations and the stomach (arrow) into the left hemithorax. Active bleeding (arrowheads) is seen in the left pleural cavity from the injured intrathoracic spleen. A 14-cm diaphragmatic tear was repaired at surgery. (From [42], with permission)

using this specific protocol designed to evaluate the diaphragm. This spiral CT protocol results in sagittal and coronal images of improved spatial resolution to assess the diaphragm's contour and its relationship to the abdominal viscera (see Figs. 5, 6) [37, 38]. Blunt trauma Since blunt diaphragm rupture has a high association with torso injuries, the majority of hemodynamically stable patients with blunt diaphragmatic injury will require an admission CT examination to evaluate the extent and anatomical sites of coexisting thoracoabdominal injuries so that clinical management can be planned. Diagnostic CT signs of diaphragm injury include a defect in the continuity of the diaphragm or crus (Fig. 3)

B and a waist-like constriction of abdominal viscera or omentum at the site of herniation seen on axial or reformatted CT images, the CT ªcollar signº (Fig. 4A, 5). Other CT signs include herniation of abdominal viscera or omentum through the diaphragm rupture into the thoracic cavity (Fig. 3 B, C), and thickening of the diaphragm as a result of edema or hematoma (Fig. 4B) [41]. Previous studies using conventional CT have reported that direct visualization of a diaphragm defect is the most sensitive CT finding in 71±73 % of patients with diaphragm rupture. The CT ªcollar signº has been reported as 100 % specific, but with a limited sensitivity of 27±36 % for diagnosing diaphragm rupture [32, 39]. The present authors performed a retrospective study [19] to determine the sensitivity and specificity of spiral CT in diagnosing blunt diaphragm injury at our institution. Spiral CT was performed on 41 patients (left side in 32 and right side in 10, one patient with bilateral hemidiaphragm injury) with chest radiographic findings suggestive of diaphragm injury. Unlike previous studies, in this study the most common CT finding of diaphragmatic rupture was the CT ªcollar signº, which had a sensitivity of 63 % and a specificity of 100 %. A defect in the crus or diaphragm was only 22 % sensitive to detect left-sided hemidiaphragm injuries [19]. Reformatted coronal and sagittal images were especially helpful for detection of subtle right-sided visceral herniation and to delineate the outline of the diaphragm. Reformatted spiral CT was useful to exclude the diagnosis in 17 patients with chest radiographic findings suggestive of acute diaphragm injury (Fig. 6). Overall, spiral CT was 78 % sensitive for left and 50 % sensitive for right hemidiaphragm rupture and was 100 % specific for injuries to both right and left hemidiaphragm. Spiral CT failed to enable diagnosis of diaphragmatic injuries when there was no associated visceral herniation.

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A

A

B

B Fig. 4 A, B CT ªcollar signº. Spiral CT images of a 34-year-old blunt trauma patient performed to evaluate the extent of abdominal injuries. A Axial CT image shows constriction of the oral contrast material in the stomach (arrows) at the site of a diaphragmatic rent, the CT ªcollar sign.º B Axial CT image at the level of the spleen shows a splenic laceration (arrowhead), perisplenic blood, and a rib fracture (curved arrow). The left hemidiaphragm is thickened (arrows) from blood tracking as a result of the diaphragm and splenic injury. (From [42], with permission)

Penetrating injuries Studies are required to establish the role of spiral CT in evaluating patients with penetrating injuries to the diaphragm. Patients with any penetrating injury to the thoracoabdominal area are likely to have a diaphragmatic injury. The thoracoabdominal area is defined by the costal margin and posteroinferior-most ribs inferiorly. Superiorly this area is defined by a line drawn between the nipples, extending laterally to the sixth rib in the midaxillary line and posteriorly to the inferior margins of scapula or eighth rib. Since the majority of penetrating injuries to the diaphragm are less than 2 cm in length and are far less conspicuous than those that typically result from blunt force trauma, they are diagnosed at surgical exploration or thoracoscopy by direct inspection of the diaphragm [21]. Currently in the United States trauma centers are attempting to utilize CT to diagnose

Fig. 5 A, B Spiral CT of diaphragm injury in a 36-year-old blunt force injury patient. A Axial CT image shows free intaperitoneal fluid (arrowheads) posterior to stomach with a focal constriction (arrows) in body of stomach, the CT ªcollar sign.º B Coronal reformatted CT image shows the CT ªcollar signº (arrows) with herniation of the stomach into left lower hemithorax. (From [37], with permission)

intraperitoneal and retroperitoneal injuries in hemodynamically stable patients with penetrating trauma to the torso. It is important to carefully evaluate the diaphragm contour for direct evidence of injury, including a focal defect (Fig. 7) with adjacent hemorrhage and focal herniation of abdominal contents such as fat into the pleural space. Indirect evidence for diaphragm injury includes demonstration that a bullet or knife tract crosses the diaphragm, extravasation of gastrointestinal contrast into the thoracic cavity, and the presence of injuries to organs on both sides of the hemidiaphragm. Limitations of CT Limitations of spiral CT in diagnosing diaphragm injuries include failure to show diaphragmatic injuries without herniation of intra-abdominal viscera into the thoracic cavity. None of the diaphragmatic injuries occurring without associated visceral herniation was diagnosed in the retrospective study performed using spiral CT at our institution [19]. In the acute setting concurrent pulmonary pathology related to trauma or artifacts as a result of respiratory motion may obscure the outline of the diaphragm. A localized defect in the posterolateral aspect of the left hemidiaphragm (Fig. 8) can be

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B

MR Imaging

C Fig. 6 A±C Spiral CT of eventration of right hemidiaphragm. A Admission chest radiograph shows elevation of right hemidiaphragm with cystic areas in the right lower chest. B Axial CT image shows colon, intra-abdominal fat, and liver in right lower chest. C Reformatted coronal shows an elevated intact right hemidiaphragm with no herniation of intra-abdominal viscera. (From [42], with permission)

seen as a normal variant, especially in elderly women [39, 40, 41]. Injury to organs adjacent to the diaphragm such as the adrenal gland, kidney, liver, spleen (Fig. 4C), or proximal small bowel can produce tracking of hemorrhage or edema along the diaphragm, suggesting primary diaphragm injury [43]. The diagnosis of diaphragm rupture should not be made exclusively on the basis of CT findings of a localized defect in the crus or thickening of the diaphragm. Chest radiography along with clinical assessment can be used to diagnose gross herniation of abdominal contents. A follow-up spiral CT using the diaphragm protocol with axial and reformatted images 7±10 days after admission is suggested, either to verify resolution of blood tracking along an intact diaphragm or to assess for evidence of visceral herniation.

Routine use of respiratory and cardiac gating with direct coronal and sagittal MR imaging helps to optimally visualize the entire diaphragm [24, 44, 45]. T1-weighted and gradient-echo sequences display the normal diaphragm as a continuous hypointense band. Injuries to the diaphragm are seen as an abrupt defect or defects in the low-signal intensity hemidiaphragm (Fig. 9). Herniation of abdominal viscera or omentum through a diaphragm rupture can be accurately demonstrated by MR imaging (Fig. 7) [44]. Currently, at our trauma center the authors use T1-weighted sagittal and coronal images to evaluate the diaphragm in patients presenting with a clinical or radiologic suspicion of a diaphragm injury

Fig. 7 Spiral CT of stab wound to diaphragm in a 36-year-old male. Axial CT image shows an air bubble (arrowhead) in left lower chest wall at site of stab wound. A defect in the left hemidiaphragm (arrows) is seen adjacent to stab wound with herniation of intraperitoneal fat into left lower chest. At surgery a less than 2-cm diaphragm injury was repaired

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A A

B Fig. 8 A, B Congenital defect in diaphragm in a 71-year-old male with no previous history of trauma. A,B Axial CT images show a small defect and deformity (arrowheads) of posterior left diaphragm. Herniation of fat (arrow) is seen through the defect into lower chest

when the diagnosis is uncertain after spiral CT with reformations (Fig. 10).

Conclusion Multiple imaging modalities are available for preoperative diagnosis of diaphragmatic injuries. Chest radiographs are the initial and most commonly performed imaging study to evaluate the diaphragm following trauma. When chest radiography is indeterminate, spiral CT is the most appropriate secondary study since the majority of hemodynamically stable patients with blunt diaphragm injury will require an admission CT examination. Thin, overlapping sections and multiplanar reformatted images maximize the accuracy of CT and should

B Fig. 9 A, B MR imaging of diaphragm injury. A Sagittal and B coronal images show herniation of intra-abdominal fat (open arrow) and fundus of stomach (curved arrow) into the lower left chest through a diaphragmatic tear (arrowheads). The ªcollar signº (arrows) is also seen. (From [44], with permission)

be performed when diaphragm injury is suspected. Multidetector spiral CT can be expected to improve further on the accuracy of CT to assess for diaphragm injury. When CT results remain equivocal, T1-weighted sagittal and coronal MR imaging has proven very useful for both right- and left-sided injury. Further research evaluating both CT and MR imaging to detect to exclude penetrating diaphragm injury is needed. The ability to detect direct interruption of the hemidiaphragms without concurrent abdominal content herniation would significantly improve the overall accuracy of diagnostic imaging.

13 Fig. 10 Thoracic diagnostic imaging algorithm (From [42], with permission)

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