AIM: To assess the value of contrast-enhanced ultrasound (CEUS) in diagnosing splenic artery complications (SACs) after acute pancreatitis (AP).

METHODS: One hundred and eighteen patients with AP were enrolled in the study. All patients were examined by CEUS and contrast-enhanced computed tomography (CECT). CECT was accepted as a gold standard for the diagnosis of SACs in AP. The diagnostic accuracy of splenic CEUS and pancreatic CEUS was compared with that of CECT. Splenic infarction was the diagnostic criterion for splenic artery embolism and local dysperfusion of the splenic parenchyma was the diagnostic criterion for splenic arterial stenosis. The incidence of splenic sub-capsular hemorrhage, splenic artery aneurysms, and splenic rupture was all lower than that of SACs.

RESULTS: Nine patients were diagnosed as having SACs after AP by CECT among the 118 patients. The patients with SACs were diagnosed with severe acute pancreatitis (SAP). Among them, 6 lesions were diagnosed as splenic artery embolism, 5 as splenic artery aneurysms, and 1 as splenic arterial stenosis. No lesion was diagnosed by pancreatic CEUS and 5 lesions were diagnosed by splenic CEUS. By splenic CEUS, 4 cases were diagnosed as splenic artery embolism and 1 as splenic arterial stenosis. The accuracy of splenic CEUS in diagnosis of SACs in SAP was 41.7% (5/12), which was higher than that of pancreatic CEUS (0%).

CONCLUSION: Splenic CEUS is a supplementary method for pancreatic CEUS in AP patients, which can decrease missed diagnosis of SACs.

Contrast-enhanced ultrasound (CEUS) has become an important imaging method to evaluate the degree of severity and predict the prognosis of diseases[1]. Acute pancreatitis (AP) can be examined by CEUS to identify the necrosis range of the pancreas, which is related to treatment and prognosis. Splenic artery complications (SACs) have a low morbidity in AP. Although SACs are rare complications in AP and most patients present few clinical symptoms, it may lead to a severe outcome. Rupture of splenic artery aneurysms is frequent and sometimes occurs as the first symptom, and sometimes it is fatal[2]. So, it is of great clinical significance to determine the diagnostic accuracy of CEUS for SACs in AP. However, the sensitivity of gray scale ultrasound and color Doppler ultrasound is low, and few studies have reported on CEUS[3]. In this article, we discussed the diagnostic value and accuracy of splenic CEUS for SACs in AP.

The 118 patients were diagnosed with AP by CECT; among them only 9 patients (including 12 lesions) were diagnosed as having SACs. Among the 118 patients, there were 38 patients with mild AP and 80 with severe AP (SAP). All SACs patients were from the SAP group. Six cases were diagnosed as splenic artery embolism; 5 cases as splenic artery aneurysms and 1 case as splenic arterial stenosis by CECT. Three patients had splenic artery embolism with splenic artery aneurysms found by CECT. In the splenic CEUS group, SACs were found in 5 cases, including 4 cases of splenic artery embolism (Figure 1) and 1 case of splenic arterial stenosis (Figure 2). And in the pancreatic CEUS group, all lesions of SACs were misdiagnosed (Table 2). The diagnostic accuracy of splenic CEUS for SACs in AP was 41.7% (5/12), which was obviously higher than that of pancreatic CEUS (0%, 0/12).

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Figure 1 A 22-year-old man with splenic artery embolism. A: Enhanced-contrast computed tomography showing splenic artery embolism (dotted arrow), and the lesion of splenic infarction (solid arrow); B, C: Gray scale ultrasonography and color Doppler ultrasonography of the spleen showed no obvious lesion of splenic infarction; D: Some regions with no enhancement appeared in the splenic arterial phase (solid arrow) on contrast enhanced ultrasound (CEUS); E: A wedge-shaped splenic infarction with no enhancement was displayed in the splenic venous phase (solid arrow) on CEUS.

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Figure 2 A 26-year-old woman with splenic arterial stenosis. A: Enhanced-contrast computed tomography showing splenic arterial stenosis (dotted arrow) and a focal splenic parenchyma region showed low enhancement (solid arrow); B, C: Gray scale ultrasonography and color Doppler ultrasonography showed no obvious lesions in the spleen; D: No obvious lesion was displayed in the splenic arterial phase on contrast enhanced ultrasound (CEUS); E: Some regions of focal dysperfusion of the splenic parenchyma showed low enhancement in the splenic venous phase (dotted arrow).

By splenic CEUS, 4 cases were diagnosed as splenic infarction, including 1 case complicated with sub-capsular hemorrhage, and 1 case of focal dysperfusion of the splenic parenchyma (Table 3). The CEUS imaging of splenic infarction showed that in some regions, no enhancement appeared after contrast agent injection in the splenic artery phase and venous phase, and hence infarcted splenic parenchyma was displayed as a hypoechoic area. The shape of splenic infarction varied from wedge-shaped (3 cases) to round or irregular (1 case).

Sub-capsular hemorrhage is a complication of splenic artery embolism. CEUS imaging of sub-capsular hemorrhage showed an anechoic region under the splenic sub-capsule, which could differentiate better than pancreatic ultrasound, and there appeared an anechoic region and no enhancement after contrast agent injection in the splenic arterial phase and venous phase. There was one case diagnosed by CEUS as splenic infarction in the splenic CEUS group.

The imaging of focal dysperfusion of the splenic parenchyma revealed a region where the degree of enhancement inside the lesion area was lower than that of normal surrounding splenic parenchyma in the arterial and venous phases (especially the venous phase). The region of focal dysperfusion of the splenic parenchyma was displayed as a slightly hypoechoic area on CEUS, which did not appear on pancreatic ultrasound. Hence, a case of SAC was diagnosed by splenic CEUS, and there was no evidence of splenic rupture during his stay in hospital.

Five cases of splenic artery aneurysms were all miss-diagnosed by pancreatic CEUS and splenic CEUS in AP. Because the whole splenic artery is difficult to display by ultrasound, especially the region which is close to the hiluslienis, gray scale ultrasound or CEUS may be necessary to identify the size or the location of splenic artery aneurysms.

AP is a common abdomen emergency and SACs in AP are rarely seen with a low incidence[4]. Due to the low sensitivity of ultrasound in diagnosing SACs, the missed diagnosis of the complications is often ignored[5], even by CEUS[6]. CECT was regarded as the gold standard to evaluate AP, especially the degree of severity[7,8]. CEUS changes the conventional viewpoint that ultrasound can only examine AP roughly[1,9], such as the pancreas size, shape, and peri-pancreatic fluid collection[10]. With the development of contrast agents, corresponding contrast-enhanced software and ultrasound equipment, CEUS is being utilized in more and more diseases, including pancreatic diseases, especially examination of SAP because it can display pancreatic parenchymal necrosis and the degree of necrosis, and the extra-pancreatic acute fluid collection. Previous studies concluded that ultrasound severity index (USSI) has a strong correlation with CT severity index (CTSI) and has been regarded as a substitute for CECT[6,9]. Only a few cases have been reported worldwide about CEUS for SACs compared with CECT for splenic venous complications[11-13]. The reason may be that the splenic artery is located between the tail of the pancreas and the hilum of the spleen with the body of the stomach in front. Gray scale sonography is influenced greatly by meteorism in the gastrointestinal tract, and diagnosis is sometimes difficult[14]. Because the quality of CEUS depends on the gray scale sonography, its quality is consequently affected, and the diagnostic accuracy for SACs is often ignored compared with CT or MRI[15].

Although the whole splenic artery is difficult to be displayed directly by ultrasound, we convert the observational objective to evaluate the lesions of the splenic artery indirectly. The diagnostic criteria for SACs were defined by observing the pattern of images obtained from the splenic CEUS. Blood supply to the spleen is solely from the splenic artery. Any lesions or changes in the splenic artery may result in splenic parenchymal infarction. In AP, splenic parenchymal infarction occurs due to SACs. SACs are infrequent complications with pancreatitis, which mainly occur in chronic pancreatitis and SAP[16]. Mortelé et al[17] found that the incidence of splenic infarction in AP was about 7%, and there was a strong relationship between this complication and the severity of pancreatitis. In our study, 6 cases were diagnosed as splenic infarction by CECT. The incidence of splenic infarction in AP was 5.1% (6/118) and all cases with the complications were SAP. The findings in our study are consistent with the results reported by Mortelé et al.

SACs include splenic artery embolism, splenic artery aneurysms and splenic arterial stenosis[18]. SACs can lead to splenic infarction, sub-capsular hemorrhage, splenic rupture, or splenic aneurysm rupture. Color Doppler ultrasound is less sensitive to display acute infarction because there is no difference between the echo area of infarcted and normal parenchyma[19]. Acute splenic arterial stenosis is the main presentation of SAP. With the development of CEUS, splenic trauma or aortic aneurysm rupture can be diagnosed in clinical practice[20-22]. The microcirculation of the splenic parenchyma can be displayed by CEUS and it is possible to observe the ischemic alteration of the splenic parenchyma. These characteristics guarantee the diagnosis of acute infarction as early as possible and SAPs indirectly. The sensitivity of splenic CEUS for detecting SACs has increased obviously, and the accuracy rate was 41.7% (5/12, including 4 cases of splenic artery embolism and 1 case of splenic arterial stenosis) in diagnosing SACs compared with CECT.

There were no SACs diagnosed by pancreatic CEUS, indicating that pancreatic CEUS is a low sensitive method to diagnose SACs in AP. This finding also demonstrates that splenic CEUS is an indispensable technique in diagnosis of SACs in AP. It is of great clinical significance to optimize methods of diagnosis for AP complications, such as CEUS. Splenic CEUS is a felicitous supplement to overcome the disadvantage of pancreatic CEUS for SAPs in AP.

However, this study of diagnosis for splenic artery aneurysms is not satisfactory. In this study, all cases of splenic artery aneurysms were miss- diagnosed. We finally analyzed the reason for missed diagnosis of splenic artery aneurysms. The longest diameter of splenic artery aneurysms was less than 2 cm and the location was far from the hilum of the spleen so that sonologists could not observe the lesions, even by CEUS. And there were 2 cases of splenic infarction which were miss-diagnosed by splenic CEUS. We retrospectively analyzed the reasons why splenic CEUS missed the diagnosis. The reason was that the splenic infarction in 2 cases was located close to the diaphragm and at the sub-capsular area of the spleen, where ultrasound imaging would be obstructed by the ribs. Sonologists did not notice the missed area, which was just located in the shadow of the imaging. By controlling the quality of ultrasound imaging and avoiding the influence of the ribs, the incidence of missed diagnosis would be decreased.

The ultrasound contrast agent (suspension made of 5 mL normal saline mixed with SonoVue dry powder) was administered by intravenous injection at 1.5-2.0 mL for each pancreatic CEUS examination. Pancreatic CEUS examination generally did not run out of the suspension. Usually the remaining suspension of about 1.0-2.0 mL was sufficient for splenic CEUS examination. Therefore, it is economic to perform the splenic CEUS after pancreatic CEUS examination. Splenic CEUS examination could diagnose not only splenic artery lesions but also any other pathological changes, such as pancreatic pseudocysts in the splenic parenchyma[23,24].

Although CECT is the gold standard in diagnosing AP, ultrasound has an important position in pancreatitis examination[25]. When the patient’s condition is not fit for CECT, such as iodine allergy, unavailability for bedside examination, and cases of renal insufficiency, CEUS is an effective substitute for CECT examination[26,27].

In conclusion, splenic CEUS diagnosis of SACs in AP was better than pancreatic CEUS because it had a higher diagnostic accuracy than the latter. In splenic CEUS examination, the contrast agent can be utilized more effectively and economically. Splenic CEUS can obviously increase the diagnostic accuracy for SACs in AP, which is simple, convenient, efficient, safe, and partly solves the disadvantages of other modalities in diagnosis of SACs in AP. Splenic CEUS is a supplementary method for pancreatic CEUS when AP patients need pancreatic CEUS examination, which can decrease the missed diagnosis of SACs.

The authors are indebted to Professor Qin Xia, Zhong-Wen Huang, and Wen-Fu Tang (Department of Integrated Chinese and Western Medicine of West China Hospital) for providing the cases in this study. We also thank Lin Lan and Xiao-Ying Feng for assistance with the injection of contrast agents.