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The Celiac Axis Revisited: Anatomic Variants, Pathologic Features, and Implications for Modern Endovascular Management1 Richard D.White, FRCR Jonathan R.Weir-McCall, FRCR Carl M. Sullivan, FRCR Syed A. R. Mustafa, MBBS Phey M.Yeap, MBChB Matthew J. Budak, FRCR Thiru A. Sudarshan, FRCR Ian A. Zealley, FRCR Abbreviations: CA = celiac axis, GDA = gastroduodenal artery, LGA = left gastric artery, MIP = maximum intensity projection, SMA = superior mesenteric artery, VAA = visceral artery aneurysm RadioGraphics 2015; 35:0000–0000 Published online 10.1148/rg.2015140243 Content Codes: From the Department of Clinical Radiology, University Hospital of Wales, Heath Park, Cardiff CF14 4XW, Wales (R.D.W., S.A.R.M.); Department of Clinical Radiology, Ninewells Hospital, Dundee, Scotland (J.R.W.M., P.M.Y., M.J.B., T.A.S., I.A.Z.); and Department of Clinical Radiology, Morriston Hospital, Swansea, Wales (C.M.S.). Presented as an education exhibit at the 2013 RSNA Annual Meeting. Received June 23, 2014; revision requested September 23 and received November 11; accepted December 11. For this journal-based SA-CME activity, the authors, editor, and reviewers have disclosed no relevant relationships. Address correspondence to R.D.W. (e-mail:
[email protected]). 1
SA-CME LEARNING OBJECTIVES After completing this journal-based SA-CME activity, participants will be able to: ■■Identify the common anatomic variants of the celiac axis. ■■Recognize
a range of pathologic conditions involving the celiac axis. ■■Discuss
the role of endovascular treatment for a range of pathologic conditions affecting the celiac axis. See www.rsna.org/education/search/RG.
The celiac axis (CA) and its branches are critically important arteries that supply blood to the vital solid and hollow abdominal viscera of the foregut. There are many potential anatomic configurations, with up to half the population having a variation from the classic pattern of the CA bifurcating into the hepatosplenic trunk and left gastric artery. These configurations result from permutations in the fusion of the paired dorsal aortas during the first trimester. Despite the short length of the CA, it is affected by a wide range of pathologic conditions, including mesenteric ischemia due to intrinsic occlusion (secondary to causes such as atherosclerosis or thromboembolic events) and extrinsic compression from masses or the median arcuate ligament. Symptoms of mesenteric ischemia are nonspecific and include postprandial abdominal pain and weight loss; thus, the underlying pathologic condition may be found only when being sought specifically. More unusual pathologic conditions include dissection, aneurysms, and vascular malformations. Awareness of the pathologic conditions that affect the CA is important for both diagnostic and interventional radiologists. Early recognition and treatment of CA disease may prevent catastrophic hemorrhage and bowel infarction. Both endovascular and surgical approaches to treatment are greatly enhanced by correct identification of arterial anatomic variants; catheter angiography, computed tomographic angiography, and magnetic resonance angiography can facilitate detection of these variants. Knowledge of the different anatomic permutations is essential to guide endovascular procedures, such as hemorrhage control, transarterial interventional oncologic therapy, and treatment of visceral artery aneurysms. Online supplemental material is available for this article. ©
RSNA, 2015 • radiographics.rsna.org
Introduction
As the first branch of the abdominal aorta and the source of arterial supply for the entire foregut, the celiac axis (CA) and its branches are critical for the function of numerous vital solid and hollow abdominal viscera. With the continuous advancement of computed tomographic (CT) scanner technology, invasive angiography is no longer the sole method for evaluation of arterial pathologic conditions (1). CT angiography is now widely used as the first step in evaluation of abdominal vascular pathologic features because of its speed, high spatial resolution, and ability to depict associated extra-arterial structures. Interventional radiology has undergone similar technological advancement in recent years. Although use of
VASCULAR/INTERVENTIONAL RADIOLOGY
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TEACHING POINTS ■■
Fourteen nonstandard anatomic variations exist; in one study, these accounted for nearly 10% of patterns overall. The three most common variations are (a) LGA origin separate from the aorta and a common hepatosplenic trunk (4.4%), (b) hepatomesenteric and gastrosplenic trunks (2.6%), and (c) a common celiomesenteric trunk (1.1%).
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Eighteen percent of patients over 65 years of age have mesenteric arterial stenosis of at least 50%, but only a minority are symptomatic. Double-vessel disease, distal lesions, and single arterial stenosis of more than 70% may produce symptoms warranting intervention.
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In median arcuate ligament syndrome, CT angiography, MR angiography, and catheter angiography show a characteristic “J,” or hook shape, at around 5 mm from the CA ostium on sagittal images. This finding differentiates this cause of narrowing from atherosclerotic stenosis, which typically occurs at the ostium.
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In cases of an endoscopically identified site of upper gastrointestinal tract hemorrhage that cannot be controlled by endoscopic means, it is common practice to proceed directly to transcatheter arterial embolization without any intervening investigation. However, preprocedural CT to appropriately direct the procedure may be useful for patients who are stable enough, to identify pertinent CA anatomic variants and pathologic conditions (such as severe atherosclerotic disease of the CA) that may be causing the bleeding or may make transcatheter arterial embolization more technically challenging.
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VAAs are rare (incidence at autopsy, 70%) in both the CA and SMA, treatment of both vessels is frequently undertaken, although the decision is operator dependent.
Acute Mesenteric Ischemia Acute mesenteric ischemia is most commonly attributable to arterial embolic disease (in 40%– 50% of cases). Arterial embolism affects the SMA more frequently than the CA because of the CA’s more favorable angulation in relation to the aorta (16,35,36). Risk factors for acute mesenteric ischemia include older age, female sex, atherosclerosis, hypovolemia, cardiac disease (including arrhythmias and heart failure), intra-abdominal malignancy, and inflammatory bowel disease (37–40). The reported mortality approaches 80%, and this is attributed principally to delayed diagnosis, by which time bowel necrosis has already occurred
(26,40). Acute mesenteric ischemia may also complicate chronic mesenteric ischemia (acuteon-chronic mesenteric ischemia). CT allows identification of both the causative arterial lesion and the features of gastrointestinal tract ischemia, including bowel wall thickening, pneumatosis, and perforation (26) (Fig 11). Endovascular strategies similar to those for chronic mesenteric ischemia may be used, but laparotomy with resection of ischemic bowel is usually also required (26).
Extrinsic Compression Anatomic Compression.—The median arcuate lig-
ament links the left and right diaphragmatic crura, forming an arch that is part of the aortic hiatus through which the aorta, azygos vein, and thoracic duct pass (41). The median arcuate ligament
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Figures 12, 13. (12) Sagittal portal venous phase CT image in a patient with postprandial abdominal pain and weight loss (symptoms indicating possible chronic mesenteric ischemia) shows a J-shaped CA, with mild median arcuate ligament indentation. No other possible cause of symptoms was identified, and there was no significant atherosclerotic disease. Doppler US (not shown) demonstrated no significant stenosis. The pain was considered to be functional, and the patient was reassured. (13) Sagittal MIP MR angiogram performed for research in a healthy volunteer shows typical median arcuate ligament compression of the CA and mild poststenotic dilatation. This finding was frequently identified at whole-body MR angiography performed for research at our health care center (>1500 healthy volunteers underwent imaging).
Figure 14. Reformatted sagittal CT angiogram in a patient examined for rest pain in the right foot (found to have superficial femoral artery occlusion). Incidental note was made of severe median arcuate ligament compression of the CA, although the patient did not have related symptoms. In the context of incidental significant median arcuate ligament compression, a focused clinical history should be acquired to ensure that there are no relevant symptoms.
usually meets the anterior aspect of the aorta above the CA (at around the L1 level), but it passes anterior to the CA in 10%–24% of cases, causing compression of the CA and nearby structures, including the celiac ganglion (Figs 12, 13). Variable degrees of median arcuate ligament compression are common in asymptomatic individuals, most markedly during expiration. Severe compression is seen in 1% of the population (Fig 14). Even when median arcuate ligament compression is present, it does not usually manifest clinically because of the rich collateralization between the CA and SMA. However, a minority of the population (usually women aged 20–40 years) (42) develop symptoms of median arcuate ligament syndrome or Dunbar syndrome (42,43). Signs and symptoms are variable but include abdominal pain that is not necessarily postprandial,
weight loss, and an epigastric bruit that varies with respiration. Postulated mechanisms for the cause of pain associated with median arcuate ligament syndrome include ischemia secondary to CA compression and direct compression of celiac ganglia (44). Because CA impingement in median arcuate ligament syndrome is more marked during expiration, Doppler US characteristically shows increased flow velocities during deep expiration (45). In median arcuate ligament syndrome, CT angiography, MR angiography, and catheter angiography show a characteristic “J,” or hook shape,
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larization through reimplantation or bypass. Surgical intervention is more likely to be effective for patients aged 40–60 years who experience postprandial pain and weight loss of greater than 9 kg and have poststenotic dilatation and collateralization (42). Treatment with percutaneous transluminal angioplasty or stent placement has been described but typically provides symptomatic relief only in the short term and does not address the underlying cause. Overall success rates for treatment of median arcuate ligament syndrome are reported to be 53%–79% (49–51). Pathologic Compression.—Pathologic compresFigure 15. Axial MIP arterial phase CT image shows extension of malignant soft tissue (arrows) from the pancreas around the CA (which is narrowed and appears irregular) and its branches. The splenic artery is occluded, and the common hepatic artery is tightly stenosed proximally.
sion typically occurs when a retroperitoneal mass encases the CA and its branches (Fig 15, Movie 1). Enlargement of the mass can result in compression or invasion of these vessels. The range of pathologic conditions that can result in compromise of the CA arterial supply to the foregut is wide but most commonly includes retroperitoneal fibrosis, lymphoma, pancreatic cancer, nodal metastases, and retroperitoneal sarcomas (52). Extrinsic compression results in smooth welldefined narrowing of the artery with an obtuse angle, whereas local invasion is often indistinct and poorly defined and may rarely have an acute margin with the vessel wall.
Dissection
Figure 16. Axial thin-section CT angiogram shows CA dissection secondary to aortic dissection. Note the associated aortic aneurysm and intramural hematoma.
at around 5 mm from the CA ostium on sagittal images. This finding differentiates this cause of narrowing from atherosclerotic stenosis, which typically occurs at the ostium. Angiography may also reveal indentation of the adjacent aortic border and collateral pathway formation. However, evaluation of the relationship between the median arcuate ligament and the CA is necessary to make a diagnosis, and this requires cross-sectional imaging (46–48). CT in particular is useful in assessing for alternative causes of symptoms. Management of median arcuate ligament syndrome is controversial. Medical therapy with vasodilators may be appropriate for patients whose symptoms are not sufficiently severe to merit invasive intervention. However, the mainstay of treatment is surgery, which may involve transection of the median arcuate ligament or revascu-
CA dissection is most commonly encountered secondary to propagation of aortic dissection in the CA (Figs 16, 17). It is rarely seen as a primary phenomenon, with only about 20 cases described in the literature (53). However, CA dissection is likely to be underreported; most patients are asymptomatic, presumably because of the relatively infrequent development of associated small bowel ischemia due to extensive collateralization in the foregut (54). CA dissection is usually iatrogenic but may also be secondary to causes including atherosclerosis, pregnancy, trauma, fibromuscular dysplasia, cystic medial degeneration, and inflammatory or infectious diseases (55,56). It is more common in males, with a mean age at diagnosis of 55 years (57). Acute dissection can be painful because of visceral involvement (eg, due to propagation into the splenic artery), and extension into the SMA can lead to bowel ischemia. Chronic CA dissection can result in chronic mesenteric ischemia– type symptoms, such as postprandial abdominal pain (56). CA dissection may also be complicated by aneurysm formation, with associated risk for rupture and hemorrhage. CT angiography is the investigation method of choice, although diagnosis of CA dissection can also be facilitated with Doppler US, digital
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Figure 17. Axial (a) and sagittal (b) thin-section CT angiograms show type B aortic dissection extending down the celiomesenteric trunk, a more important finding than propagation into the CA alone. A thoracic aortic stent was placed for treatment. Six months after stent insertion, the patient remained alive, with ongoing abdominal pain but no evidence of ischemic bowel.
subtraction angiography, and MR angiography (56). The CT finding of an intimal flap is pathognomonic. However, this is not always visible and eccentric mural thrombus in the CA lumen may be the only clue to diagnosis. As with many other subtle CT angiography diagnoses, overreliance on MIP images should be avoided because reconstruction algorithms may “smooth out” and conceal small dissection flaps. Surgical intervention is the most reliable treatment for complications of acute CA dissection, although endovascular therapy with careful assessment of collateral blood supply is also an option (57). Conservative medical treatment may be appropriate for patients with limited dissection, with the aims of preventing thromboembolic complications with anticoagulation and optimization of blood pressure (54).
Upper Gastrointestinal Tract Hemorrhage Upper gastrointenstinal tract hemorrhage accounts for around 75% of gastrointestinal tract hemorrhage (58), with an incidence of approximately 0.1% and a high mortality rate. Arterial hemorrhage of CA origin secondary to peptic ulcer disease is the most common cause. Endoscopic visualization and therapy is the first-line treatment. However, failure of endoscopic therapy to control bleeding is common, and transcatheter arterial embolization provides an effective second-line treatment (ahead of surgical intervention), with a technical success rate greater than 92% (59,60). CT has a sensitivity of more than 90% for detecting the source of gastrointestinal hemorrhage when there is active bleeding, although
the sensitivity of CT decreases to less than 50% for patients with obscure gastrointestinal hemorrhage. However, the validity of these percentages for hemorrhage from the CA is questionable because many studies do not differentiate between upper and lower gastrointestinal tract bleeding in their results (58,61–64). In cases of obscure hemorrhage, alternative strategies, such as capsule endoscopy or radionuclide scanning using technetium 99m–labeled red blood cells, have some usefulness, although obscure hemorrhage rarely has an upper gastrointestinal tract origin. In acute cases, it may be difficult to differentiate clinically between upper and lower gastrointestinal tract hemorrhage. Melena and hematochezia (bright red stool) can occur in the context of hemorrhage from any site in the gastrointestinal tract; hematemesis is a more reliable indicator of an upper gastrointestinal source (58). In cases of an endoscopically identified site of upper gastrointestinal tract hemorrhage that cannot be controlled by endoscopic means, it is common practice to proceed directly to transcatheter arterial embolization without any intervening investigation (65) (Fig 18). However, preprocedural CT to appropriately direct the procedure may be useful for patients who are stable enough, to identify pertinent CA anatomic variants and pathologic conditions that may be causing the bleeding or may make transcatheter arterial embolization more technically challenging (such as severe atherosclerotic disease of the CA) (Figs 19, 20). When performing CT for gastrointestinal hemorrhage, the authors use a triple-phase technique and do not administer positive oral
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Figure 18. Angiographic findings in a patient with hemorrhage that appeared to be originating from the gastric fundus at endoscopy, although it could not be controlled with direct visualization. (a) Image does not show a convincing source of hemorrhage. On the basis of clinical suspicion, embolization of the LGA (arrow) was attempted, but the angulation made cannulation impossible. (b) Image shows covered stent placement across the LGA origin, excluding it from circulation (a useful technique to overcome adverse anatomic structure). This was placed because the patient was in extremis and considered to be ineligible for a surgical approach and no other therapeutic options remained. The authors sometimes use a buddy wire to help overcome adverse tortuosity in CA branches by straightening some of the tortuosity.
Figure 19. Imaging findings in a patient with a bleeding duodenal ulcer that could not be controlled with endoscopic injection. (a) Axial CT angiogram shows pneumoperitoneum (attributed to proximal duodenal perforation caused by the endoscopic procedure) and clot in the duodenum (arrow). (b) Subsequent angiogram shows spasm in the GDA (arrow), indicating the site of hemorrhage. Coils were placed to produce occlusion proximally and distally.
contrast material, to avoid masking foci of hemorrhage (58,66). The technique includes (a) a precontrast phase to discriminate between blood and other areas of attenuation (eg, sutures or tablets) (Fig 21), (b) an arterial phase with focal high attenuation (>90 HU) seen in arterial hemorrhage, and (c) a delayed phase in which the arterial bleeding increases in size and attenuation. It has been reported that arterial and portal venous phases are equally useful in identifying gastrointestinal hemorrhage (67).
Hemorrhage from Solid Organs Bleeding from CA branches may also occur from arteries supplying the spleen, pancreas, or liver, usually in the context of inflammation (typically acute pancreatitis) (Fig 22), neoplasm (Fig 23, Movie 2), or most commonly trauma (Figs 24– 26). The spleen and liver are the most commonly injured abdominal viscera in blunt abdominal trauma (68,69). Selective use of splenic artery embolization instead of surgery is associated with a substantial reduction in the laparotomy
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Figure 20. Imaging findings in a patient for whom upper endoscopy was unable to control bleeding from a lesser curvature peptic ulcer. (a) Reformatted axial MIP CT angiogram shows hemorrhage from an LGA (black arrow) originating directly from the aorta. Note the contained perforation (white arrow) and blood and surgical clips in the dependent stomach (arrowhead) (migrated from the bleeding site and not to be confused with bleeding from the splenic artery). (b) Angiogram shows transcatheter arterial embolization. The LGA was easily selectively cannulated and embolized to occlusion with coils. This case highlights the usefulness of preprocedural CT, with the anatomic variant readily identified.
Figure 21. Axial CT images in a patient with Mirizzi syndrome. Delayed phase images (a, b) and corresponding nonenhanced images obtained before contrast material injection (c, d) show biliary stents in situ and a rounded area of attenuation (arrow in a and c), a finding consistent with a gallstone. The delayed phase images show dense layering (arrow in b) in the duodenum. This feature was missed by the reporting radiologist; there was no clinical concern about upper gastrointestinal tract hemorrhage at the time. The patient subsequently developed melena, and endoscopy performed 1 day after CT showed active bleeding. The patient was successfully treated with transcatheter arterial embolization of the GDA. These images highlight the usefulness of imaging before contrast material injection.
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Figure 22. Imaging features in a patient with acute-on-chronic alcoholic pancreatitis who previously underwent transcatheter embolization of the splenic artery. (a) Reformatted coronal MIP CT angiogram shows a GDA pseudoaneurysm inside a pseudocyst (note the deviation of the GDA). (b) Angiogram shows the pseudoaneurysm after embolization of the GDA both proximally and distally; the angiographic results are satisfactory.
Figure 23. Imaging findings in a patient with hemorrhage into a hepatoma in the left lobe of the liver. (a) Angiogram shows that initial attempts to access the left hepatic artery through the CA were unsuccessful. (b) Angiogram shows that the left lobe of the liver received arterial supply from both the left hepatic artery (originating from the CA) and the left lobe branches from a replaced right hepatic artery (arrow) (originating from the SMA). These latter branches were considered to be the source of hemorrhage and were accessed by manipulating a microcatheter through the replaced right hepatic artery from the SMA. (c) Angiogram shows successful occlusion with coils and particles.
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Figure 24. Imaging findings in a patient with abdominal pain 10 days after percutaneous liver biopsy. (a) Coronal portal venous phase CT image shows a large hepatic pseudoaneurysm. (b) Angiogram shows the pseudoaneurysm after embolization, with the distal proper hepatic artery and right hepatic artery occluded by coils. (c) Repeat angiogram obtained 3 days later, after a decrease in hemoglobin level and further abdominal pain, shows continued bleeding; thererfore, a covered stent (arrow) was placed to divert flow from the common hepatic artery to the GDA, with good angiographic results.
Figure 25. Digital subtraction angiogram shows posttraumatic pseudoaneurysms (arrows) arising from branches of the splenic artery after an automobile collision. Note also the acute rib fracture (*). Embolization of the splenic artery was performed proximally with coils and a vascular plug.
and splenectomy rate, with no negative effect on survival (70). Endovascular treatment of splenic hemorrhage has the added benefit of avoiding subsequent asplenism. Iatrogenic hepatic arterial injuries have increased in incidence because of the increase in popularity of endoscopic, laparoscopic, and percutaneous procedures (including biopsy and drainage), instead of the traditional laparotomy (71). Major hemorrhage is reported in approximately 1% of cases of acute pancreatitis (72), affecting branches of the CA, including the splenic artery, GDA, and LGA (73).
Aneurysm VAAs include true aneurysms, which involve all three layers of the arterial wall, and pseudoaneurysms (see “Upper Gastrointestinal Tract Hemorrhage” and “Hemorrhage from Solid Organs”), which do not involve all three layers. VAAs may
occur in the CA (Fig 27), SMA, inferior mesenteric artery, renal arteries, and any of their branches. Although renal artery aneurysms are relatively common VAAs (74,75), they are often considered to be distinct entities because of their different clinical manifestations and associations and will not be considered further in this article. VAAs are rare (incidence at autopsy,
