11 Visceral Arteries

Diseases of the mesenteric arteries and celiac trunk are difficult to diagnose clinically due to a lack of specific symptoms. Frequently they are misidentified or diagnosed too late. The most common diseases are atherosclerosis, thrombosis, embolism, tumors, and inflammatory processes involving the visceral vessels. The diseases are classified as primary or secondary⁷:

•Primary diseases include giant-cell arteritis and panarteritis nodosa.

•Secondary diseases may be caused by extrinsic tumor compression, tryptic digestion in pancreatitis, or radiation-induced changes.

Symptoms depend on the degree and acuteness of hemodynamic changes. Moreover, there is a relatively large range of anatomic variance marked by varying degrees of compensation by collaterals. Slowly developing occlusions may remain asymptomatic, whereas an acute occlusion is usually a life-threatening event.

Despite significant advances in interventional therapy (thrombus aspiration, local thrombolysis, stenting of stenosis, etc.) and surgical options (bypass, intraoperative thrombolysis, intraoperative angiography, retrograde stenting), the mortality from acute intestinal ischemia continues to be high. The main reason for this is a frequent delay in diagnosis.⁸

▶ Angiography. Originally, contrast angiography was the only procedure available for the diagnosis of acute intestinal ischemia. Its early use could reduce mortality from over 90% to 53%. Angiography can also enable endovascular treatment of stenosis and occlusion. Another indication for angiography is in the localization and embolization of bleeding sites. Advantages of angiography are its ability to provide large-scale, nonsuperimposed views of the vascular tree, detect and evaluate caliber changes, and supply additional hemodynamic information. However, its use as a screening tool to investigate chronic abdominal pain or equivocal auscultation findings is obsolete. Today, it is most commonly used as an adjunct to computed tomography (CT).

▶ Computed tomography. Multislice computed tomography with contrast (CT) is considered the procedure of first choice in patients with no signs of peritonitis. It can detect thrombus in the mesenteric vessels (arterial and venous) and pneumatosis intestinalis or air in the portal vein as evidence of acute intestinal ischemia.^{8 ,​ 9} CT is not a suitable screening tool for investigating equivocal findings because of its radiation exposure, contrast nephrotoxicity, and possible contrast allergy.

However, CT is the imaging modality of first choice in patients with an acute abdominal pain. The plain abdominal radiograph is still ranked theoretically ahead of CT for the detection of free air or bowel obstruction, but only if the film can be obtained without delay. Time delay is also of concern for ultrasound in case of suspected acute mesenteric ischemia; additionally, the image quality is often drastically impaired by bowel gas, making ultrasound not a screening tool in the acute setting.¹⁰ This is not true for chronic mesenteric ischemia or unclear mild abdominal symptoms, where ultrasound is generally used prior to CT as a screening procedure and may even establish a diagnosis, making it unnecessary to proceed with CT.¹¹

▶ Ultrasound. Ultrasound imaging of the mesenteric vessels has been practiced since the mid-1980s.^{12 – 15} At that time, the main trunks of the large intestinal vessels could be visualized and evaluated with B-mode and “conventional” duplex ultrasound. These techniques were not widely used initially, however. Color duplex sonography (CDS) offered the decisive advantage of more rapid vascular imaging, making it useful in screening for diseases of the intestinal vessels and for the follow-up of interventional procedures and bypass surgery. Several studies have established criteria for the sonographic diagnosis of ≥ 50% and ≥ 70% stenosis of the superior mesenteric artery (SMA) and celiac trunk.¹⁰

Use of the ultrasound contrast agent Lumason^® has further expanded the applications of contrast-enhanced ultrasound (CEUS). It has increased sensitivity in the evaluation of intraluminal thrombi, intimal flaps, and acute mesenteric artery occlusion. CEUS can also be used to evaluate end-organ perfusion (see Chapter 17: Contrast-Enhanced Ultrasound (CEUS) in Intestinal Diseases). It is noninvasive and can be used at bedside in critically ill patients without the disadvantages of CT noted above.¹⁷

The mesenteric arteries and veins comprise a pathophysiologic and functional unit. For didactic reasons, however, we will initially limit our attention to diseases of the visceral arteries and their sonographic findings. For ontogenetic reasons the mesenteric veins are discussed in the next chapter (see Chapter 12) along with the other abdominal veins and diseases of the mesosplenoportal axis.

11.2 Anatomy, Variants, and Collaterals

The abdominal organs and gastrointestinal tract derive most of their blood supply from the three unpaired visceral branches of the abdominal aorta: the celiac trunk, SMA, and inferior mesenteric artery. These vessels develop from an initially unpaired, stepladder-like vascular system through partial fusion and regression of the embryonic segmental arteries (Fig. 11.1). Disturbances in this complex developmental process lead to numerous variants of origin, position, and course, which may be misleading for the examiner.^{18 ,​ 19} They are briefly discussed below.

11.2.1 Celiac Trunk and Its Branches

The celiac trunk is a short arterial trunk that arises from the aorta at the level of the T12–L1 vertebrae, just below the aortic aperture in the diaphragm. It initially runs downward from the aorta, or occasionally may run horizontally or curve upward, and in 65% to 75% of cases it divides into three branches: the left gastric artery, common hepatic artery, and splenic artery (Fig. 11.2). In 5% to 10% of cases a fourth branch is formed by an additional pancreatic artery or an atypical origin of the dorsal pancreatic artery. In rare cases the celiac trunk may be absent or may have a common origin with the SMA, forming the celiacomesenteric trunk.^{18 ,​ 20}

The left gastric artery is the first branch of the celiac trunk in 90% of the population. It runs between the layers of the lesser omentum and anastomoses with the right gastric artery on the lesser curvature side of the stomach. It also anastomoses with branches of the right gastroepiploic artery and the short gastric arteries. In 2.5% of cases the left gastric artery arises directly from the abdominal aorta.

The splenic artery is the largest-caliber branch of the celiac trunk, measuring 6 to 10 mm in diameter. It runs a partly tortuous course along the superior border of the pancreas to the splenic hilum, though in some cases it runs below or within the body of the pancreas. Its average length is 13 cm. The splenic artery supplies the head and tail of the pancreas, the greater curvature and fundus of the stomach, and the omentum via the greater and dorsal pancreatic arteries and smaller arteries. At the splenic hilum it divides into an inferior and superior main branch, each of which supplies the splenic parenchyma via four to six segmental arteries.

Variants are numerous. In up to 20% of cases the liver receives some or all of its blood supply from the SMA. Local anatomy may be complicated by numerous accessory arteries arising directly from the celiac trunk, from the left gastric or splenic artery, or by branches that cross to the contralateral hepatic lobe (see Fig. 15.1). Vessels in the liver capsule, gallbladder, and small arteries in the porta hepatis can provide additional sources of collateral supply.^{18 ,​ 20}

The gastroduodenal artery runs behind the duodenum and anterior to the pancreas. It divides into the right gastroepiploic artery and into the anterior and posterior superior pancreaticoduodenal arteries, forming a pancreatic arcade that anastomoses with the territory of the SMA. They supply the head of the pancreas, pylorus, portions of the duodenum, as well as jejunal branches in some cases.²¹

11.2.2 Superior and Inferior Mesenteric Arteries

The SMA arises from the aorta 0.5 to 2 cm below the celiac trunk at the level of the L2 vertebra. It runs downward, passing behind the pancreas and posterior to the splenic vein. After descending for approximately 4 cm, it gives off the inferior pancreaticoduodenal artery and the middle and right colic arteries. The jejunum and ileum receive their blood supply from the jejunal and ileal arteries, which interconnect to form numerous arcade-like anastomoses (Fig. 11.2, Video 11.1). The ileocolic artery is the terminal branch of the SMA and supplies the proximal ascending colon, cecum, terminal ileum, and appendix.

Numerous preformed vessels can supply collateral blood flow to the bowel in response to a slowly developing arterial occlusion (Fig. 11.3). The arc of Riolan (Riolan arcade) is a well-known anastomosis that connects the left colic artery to the first branch of the ascending limb of the SMA—generally the middle colic artery. The main collateral pathway in response to an occlusion or high-grade stenosis of the celiac trunk is usually the gastroduodenal artery with the pancreatic arcades.

Other cross-connections are formed by the Bühler’s anastomosis (see Fig. 11.1) and the marginal artery of Drummond, which runs along the mesenteric side of the colon and is supplied by branches of the middle, right, and left colic arteries.

With a complete occlusion of all the main visceral branches, collateral flow can still be supplied from above via intercostal, diaphragmatic, and esophageal arteries. Branches of the internal iliac artery and the inferior and superior hemorrhoidal arteries can deliver blood to the inferior mesenteric artery from below.²² The latter collateral pathway via the inferior mesenteric artery plays a significant role due to the frequent use of aortic stent grafts and associated occlusions and may cause reperfusion leaks in aortic stents used for endovascular aneurysm repair (see Chapter 10).

11.3 Examination Technique

11.3.1 Settings

Using the initial settings described in Chapter 2, the celiac trunk and the origin of the SMA are identified in a longitudinal scan (Fig. 11.4). Then they are imaged in two planes. The patient is scanned in the supine or lateral decubitus position using a 3- to 6-MHz transducer, or a 5- to 8-MHz transducer in children and thin patients, while moderate probe compression is applied. Besides curved-array transducers, trapezoidal or phased-array transducers have also proven useful for scanning the celiac trunk. If the B-mode examination employs tissue harmonic imaging (THI), a 1.5-MHz transducer can be used. The equipment, settings, and technique for CEUS are described in Chapter 2 and Chapter 4.

11.3.2 Patient Preparations

The patient should avoid drinking carbonated beverages on the eve of the procedure and preferably should avoid an evening meal. Next day, the fasted patient is placed in the supine position. The patients are given an antigas medication at some centers.

11.3.3 Color Duplex Sonography

Using the liver as an acoustic window, the celiac trunk and the main trunk of the SMA can be imaged in over 96% of cases when a modern scanner is used. B-mode imaging is followed by color Doppler activation and adjustment, and the celiac trunk and its branches are analyzed (Fig. 11.5). Then the main celiac trunk, common and proper hepatic arteries, splenic artery, and, if possible, the left gastric artery and gastroduodenal artery are identified in longitudinal and transverse scans (Fig. 11.6). All or part of the gastroduodenal artery can be defined in over 80% of cases as a vessel running perpendicular to the proper hepatic artery and anterior to the pancreatic head (Fig. 11.6). Next, the origin of the SMA is identified and traced as far as possible in longitudinal scans. In more than 65% of cases the artery can be traced to the level of the jejunal branches and ileocolic artery (Fig. 11.7).

Evaluation of the inferior mesenteric artery begins by defining the aortic bifurcation. From there the aorta is traced cephalad in contiguous transverse scans, applying gentle transducer pressure, until the proximal trunk of the inferior mesenteric artery is visualized on the left side of the aorta approximately 3 cm above the bifurcation. The transducer is then rotated to a longitudinal orientation and the inferior mesenteric artery can usually be traced over a length of 3 to 4 cm (Fig. 11.8). For an optimum examination, the color gain and threshold should be adjusted just below the level at which color noise pixels appear. Artifacts due to peristalsis can be reduced by applying careful compression.

The length of the ultrasound examination depends on the clinical question. If acute intestinal ischemia is suspected, a few minutes should be allowed for ultrasound scans at the most so that necessary contrast-enhanced CT, with its therapeutic implications, will not be delayed. Ultrasound can quickly detect acute mesenteric ischemia due to an acute arterial or venous thrombotic occlusion, pneumatosis intestinalis, or air in the portal vein so that further therapeutic steps can be initiated. Besides acute thromboembolic occlusion, other possible conditions such as nonocclusive mesenteric ischemia (NOMI) can be diagnosed with CTA.^{9 ,​ 23} If free intra-abdominal fluid is found and a ruptured visceral artery aneurysm is suspected, angiography with possible embolization would be indicated in a hemodynamically stable patient and open surgery in an unstable patient.

In patients with chronic intestinal disease, the search for stenoses and possible subsequent functional evaluation may take 15 minutes or more. If stenosis is found, all three intestinal vessels should be analyzed along with the flow direction in the pancreatic arcade.

11.3.5 Contrast-Enhanced Ultrasound

The combination of CDS and CEUS can significantly improve accuracy in the diagnosis of nonstenotic changes such as thrombi, dissections, intimal flaps, and mesenteric artery occlusion. End-organ perfusion can also be investigated by contrast-enhanced imaging with Lumason^®: hyperperfusion is found in acute or chronic inflammation, hypoperfusion in ischemia.^{17 ,​ 24} Perfusion defects will be seen in patients with a hepatic or splenic infarction.

CEUS is a noninvasive bedside procedure that can eliminate the need for further CT examination in some critically ill patients (e.g., in intensive care unit [ICU]).²⁵

11.4 Normal Findings and Variants

11.4.1 Normal Findings

The celiac trunk has a palm-frond-like appearance when viewed in a transverse color Doppler scan (see Fig. 11.5). The common or proper hepatic artery and the splenic artery can be traced into the liver and spleen, respectively, appearing as vessels perfused by pulsatile, antegrade flow (see Fig. 15.2). The Doppler spectrum resembles that of the internal carotid artery. This similarity results from the low resistance in the distal vascular bed, which permits continuous antegrade blood flow even in diastole (Fig. 11.6, Fig. 15.4 b and c). In patients with little or no stenosis, the values shown in Table 11.1 are found in the region of the celiac trunk.²⁰ The flow velocities measured during expiration are significantly higher than the inspiratory velocities.²¹

By rotating the transducer, the operator can trace the gastroduodenal artery down to the pancreas and its division into the anterior and posterior superior pancreaticoduodenal arteries. Normal flow in the gastroduodenal artery is directed inferiorly (Fig. 11.6).

The left gastric artery can be traced along the inferior surface of the hepatic left lobe in a modified longitudinal scan (Fig. 11.6). Usually only the proximal segment can be visualized, but in some cases the vessel can be traced to its possible anastomosis with the left hepatic artery. Its Doppler spectrum, like that of the gastroduodenal artery, shows greater pulsatility with very little diastolic flow.

The SMA arises from the anterior or anterolateral surface of the aorta. By varying the probe alignment as needed, the operator can trace the main trunk of the artery for up to 8 cm (Fig. 11.7). The Doppler waveform shows continuous, distally directed systolic flow with a steep upstroke and rapid downstroke. In the fasted patient, a notch occurs in the late systole, indicating a brief reverse-flow component encoded in the opposite color. Flow may cease in the late diastole (Fig. 11.9). Postprandial spectra will show an increased peak systolic velocity (PSV) and a disproportionate rise of end-diastolic velocity. This reflects the physiologic hyperemia that is induced by digestion. Analogous spectral changes are found after the administration of glucagon.

Normal values for the SMA in patients with little or no stenosis are shown in Table 11.1. The maximum flow velocity in the SMA rises continuously after a meal, reaching a peak value (134 ± 14% of the baseline value) after a period of 41 ± 4 minutes.²⁸

The inferior mesenteric artery can be imaged in over 92% of patients when modern equipment is used in conjunction with the examination technique described above.²⁹ Its main trunk normally shows homogeneous color filling during systole (Fig. 11.8). Doppler spectra show a flow pattern similar to that of the SMA: high velocity in systole and little or no flow in diastole. The values listed in Table 11.1 are found in normal patients.²⁹ In occlusive disease of the celiac and superior mesenteric arteries or the iliac artery, values in the inferior mesenteric artery are still normal (up to 189 ± 58 cm/s).³⁰

11.4.2 Variants

Variants such as an isolated origin of the hepatic artery from the aorta (Fig. 11.10) or the common hepatic artery and right hepatic artery arising from the SMA (Fig. 15.2) are easily detected with CDS under favorable scanning conditions (see Chapter 15). The detection of these variants is helpful, for example, in planning interventions such as intrahepatic chemotherapy.

Bronchopulmonary Sequestration

Other variants detectable with transabdominal ultrasound are pulmonary malformations supplied by abdominal vessels. An example is bronchopulmonary sequestration, first described by Pryce in 1946.³¹ It is a rare congenital malformation of the lower respiratory tract characterized by a nonfunctioning mass of lung tissue that lacks normal communication with the tracheobronchial tree. It derives its arterial blood supply from the systemic circulation. The sequestration may be intralobar or extralobar, depending on its pleural investment. Sade expanded the classification of bronchopulmonary sequestration in 1974. In most cases the sequestration has a systemic arterial blood supply while venous drainage is via the pulmonary veins in the intralobar form and via systemic veins in the extralobar form. Both forms may exhibit any pattern of anomalous vascular supply and drainage. The parenchyma or bronchi in the aberrant lung segment may be unchanged, and there may be communication with the gastrointestinal tract.³² The combination of an atypical vessel arising from the abdominal aorta or its main branches and passing up to the diaphragm or a history of recurring bronchopulmonary infections should suggest the possibility of bronchopulmonary sequestration (Fig. 11.11).

11.5 Pathologic Findings

Intestinal blood flow is a complex process that is controlled and influenced by mechanical, metabolic, and neural factors as well as numerous vasoactive substances.³³ Intestinal blood flow is dependent on dietary composition. It decreases in response to stress and physical exercise. The arterial blood supply to the bowel may become compromised as a result of stenosis, thrombosis, embolism, tumor compression, volvulus, adhesions, mesenteric vein thrombosis, or severe circulatory insufficiency (nonocclusive disease). Slowly developing processes may be compensated by collateral circulation. Clinically, patients may be asymptomatic or may present with acute or chronic intestinal ischemia. Acute occlusions, deficient collateral circulation, or involvement of two or more vessels can lead to intestinal damage.

Many of these disorders were formerly misinterpreted as inflammatory bowel disease. With the increasing use of endoscopy, endosonography, histology, refined angiographic techniques, multislice computed tomography angiography (CTA), and CEUS, we have been able to differentiate other entities such as ischemic colitis and drug-induced colitis.^{9 ,​ 17 ,​ 23 ,​ 24}

11.5.1 Plaque, Stenosis, and Occlusion

The principal cause of stenosis is atherosclerosis. Narrowing may also result from fibromuscular dysplasia (FMD). At the abdominal level this rare disease may affect, in descending order of frequency, the renal and splenic arteries, the SMA, and the celiac trunk. Other pathologies are extrinsic compression by benign and malignant tumors, the arcuate ligament syndrome, and stenotic changes due to vasculitic diseases.

Atherosclerosis

Atherosclerotic changes in the visceral arteries are found as early as the third decade of life. With further aging, plaques may form that cause luminal narrowing or obstruction. The lesions are classified by their location as involving the origin of the artery, its main trunk, first- and second-order branches, or diffuse involvement of the peripheral branches.

Atherosclerotic stenosis in the proximal portion of the visceral arteries is generally short, circumferential, or eccentric (ostial stenosis in aortic atherosclerosis). Often the only early findings are isolated wall plaques, which at most cause slight flow irregularities. As the degree of stenosis increases, turbulence and flow acceleration occur. Diabetic patients most often present a diffuse pattern of atherosclerosis with the concomitant involvement of peripheral branches. They appear irregular on angiography with no associated collateral circulation.

▶ Findings. Calcified plaques have a sonodense appearance on ultrasound and cast a typical acoustic shadow in accordance with their size and insonation angle. Depending on the degree of narrowing, CDS shows circumscribed flow acceleration that may cause aliasing, turbulence, and possible poststenotic dilatation. In high-grade stenosis, peripheral vascular segments may show waveform damping and/or retrograde flow in the gastroduodenal artery (Fig. 11.12). High-grade stenosis may also produce coarse vibration artifacts that transcend the vessel lumen (Fig. 11.13). This “confetti sign” was described previously for peripheral vessels and the aorta (Video 3.2).

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