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Gastrointestinal Imaging |
1 From the Department of Radiology (A.A.S.I., M.M., A.R., G.A.) and HHT Centre (C.S., A.C.), University Hospital, Policlinico of Bari, Piazza Giulio Cesare 11, 70124 Bari, Italy. Received December 23, 2002; revision requested March 3, 2003; revision received April 18; accepted June 13. Address correspondence to M.M. (e-mail: doc.mauri@libero.it).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Multiphasic multi–detector row helical CT was performed in 70 consecutive patients (29 females and 41 males; mean age, 48.5 years; age range, 15–75 years): 64 considered to have hereditary hemorrhagic telangiectasia and six suspected of having the disease. Scanning delay was achieved by using a test bolus of contrast medium to obtain early arterial phase, late arterial phase, and portal venous phase images. Multiplanar and angiographic reconstructions were then generated. The presence of shunts, hepatic perfusion disorders, telangiectases, other vascular lesions, indirect signs of portal hypertension, and vascular anatomic variants were evaluated by two radiologists in consensus.
RESULTS: Fifty-two of 70 (74%) patients had hepatic vascular abnormalities. Only four of 52 (8%) patients were symptomatic. Arterioportal shunts were present in 27 of 52 (52%) patients, arteriosystemic shunts in eight of 52 (15%), and both shunt types in 17 of 52 (33%). In 34 of 52 (65%) patients, parenchymal perfusion disorders were detected. Telangiectases were found in 33 of 52 (63%) patients. Large confluent vascular masses were identified in 13 of 52 (25%) patients. In 31 of 52 (60%) patients, indirect CT signs of portal hypertension were detected, but only one had clinical signs of this condition. Vascular anatomic variants were detected in seven patients (13%).
CONCLUSION: Multi–detector row helical CT and reconstructions depict the complex hepatic vascular alterations typical of hereditary hemorrhagic telangiectasia.
© RSNA, 2003
Index terms: Computed tomography (CT), angiography, 952.12915, 952.12916, 957.12915, 957.12916 • Computed tomography (CT), three-dimensional, 952.12917, 957.12917 • Shunts, arteriohepatic • Telangiectasia
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The typical manifestations of this disorder are mucocutaneous or visceral angiodysplastic lesions (telangiectases and arteriovenous malformations), which may be distributed widely throughout the cardiovascular system. The skin, lungs, gastrointestinal tract, and brain are the organs involved most frequently (3), while the prevalence of hepatic involvement in patients with HHT ranges from 8% to 31% in various studies (9–11).
Hepatic involvement is characterized by the presence of intrahepatic shunts, vascular lesions, and disseminated intraparenchymal telangiectases (11,12). Although patients with liver involvement are generally asymptomatic, cardiac failure, portal hypertension, portosystemic encephalopathy, cholangitis, and atypical cirrhosis have been reported (10,11,13–16).
Diagnostic imaging has a fundamental role in the identification of hepatic vascular alterations. Ultrasonography (US), especially color Doppler US, is the modality generally used for screening patients for HHT with suspected liver involvement (4,13,14,17).
The possibility of performing angiographic reconstructions with magnetic resonance (MR) imaging and helical computed tomography (CT) have caused these two modalities to take on an important role in the identification and characterization of lesions involving hepatic vascular structures.
To our knowledge, there have been no reports of current helical CT techniques applied to patients with HHT. The purpose of our study was to describe the imaging findings obtained with multi–detector row helical CT of the liver in a large group of patients with HHT.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All patients were asymptomatic except for patient 25, who experienced cardiac failure, and patients 18, 53, and 54, who had episodes of hematemesis. In these three patients, esophagogastroduodenoscopy was also performed. Liver function test results (aspartate aminotransferase, alanine aminotransferase, 
-glutamiltranspeptidase, and serous albumin levels), cholestasis indexes (alkalin phosphatase and hematic bilirubin levels), and coagulation times (prothrombin time and partial thromboplastin time) were within normal ranges in all patients. Patients with renal failure, defined by high serum creatinine levels (>1.3 mg/dL [115 µmol/L]), or with altered hematic electrophoresis (ie, presence of monoclonal gammapathy) were excluded from the study.
Imaging
All examinations were performed with a four–detector row helical CT scanner (MX 8000; Marconi Medical Systems, Cleveland, Ohio) with the following parameters: section thickness of 2.5 mm, pitch of 1.25, increment of 0.6 mm, rotation time of 0.5 seconds, 120 kVp, and 250 mAs. Multiphasic CT scans were acquired through the region of clinical interest with the patients in supine position, starting at the hepatic dome (location determined with the scout digital radiograph) and proceeding in a caudal direction to the lower margin of the kidneys.
Nonionic contrast medium (iopromide, Ultravist 370; Schering, Berlin, Germany) was injected into the cubital vein through a 16–18-gauge needle with an automatic injector (MK-IV; Medrad, Pittsburgh, Pa) by using the following parameters: 2 mL administered per kilogram of body weight at a flow rate of 4 mL/sec with a maximum amount of 150 mL. The scanning delay was determined by using a test bolus (20 mL at 4 mL/sec) of contrast medium, and a series of single-level CT scans was acquired with low radiation dose (120 KVp, 10 mA).
A region of interest (10–20 mm2) was placed over the abdominal aorta below the celiac trunk origin, and CT scans were acquired every second from 10 to 40 seconds. The time to peak aortic enhancement was used to determine the scanning delay for the first arterial phase images. The scanning time of the early arterial phase (arterial scanning) was between 8 and 10 seconds, depending on patient size. Scanning in the late arterial phase (arteriolar or parenchymal scanning) was performed after an interscan delay of 5 seconds for table movement. The average scanning delay was 20 seconds (range, 11–37 seconds) for the first arterial phase and 37 seconds (range, 28–54 seconds) for the late arterial phase. Scanning in the portal venous phase was performed 20 seconds after the end of the second arterial phase. Complete CT scanning lasted no more than 10 minutes in all cases. Gastrointestinal contrast medium was not administered.
Image Evaluation
The acquired data were retrospectively transferred to a second workstation (Kayak XU800; Hewlett Packard, Palo Alto, Calif) equipped with dedicated reconstruction software (VITREA 2.6; Vital Images, Minneapolis, Minn). The application programs used for assessment of hepatic involvement were the multiplanar reformatting, three-dimensional maximum intensity projection (MIP), and volume rendering programs, which allowed us to generate multiplanar (transverse, coronal, and sagittal) and angiographic reconstructions. Overall image postprocessing was performed by radiologists and lasted 20 minutes. Two radiologists (G.A. and A.A.S.I., with 28 and 12 years of experience, respectively, in interpretation of abdominal CT images), who were not directly involved in the examination and were blinded to all clinical and radiologic data, reviewed the transverse images and reconstructions on the workstation and reached a consensus interpretation.
The radiologists evaluated the presence and type of shunts. Three types of intrahepatic shunts between the major vessels of the liver are possible (19): arterioportal (hepatic artery to portal vein), arteriosystemic (hepatic artery to hepatic vein), and portosystemic venous (portal vein to hepatic or systemic veins). In accordance with the literature (19–21), early and prolonged enhancement of the portal vein during the early arterial phase, which frequently becomes isoattenuating with the aorta, was considered an indirect sign of the presence of hepatic artery to portal vein shunts (arterioportal shunt). Opacification of the hepatic veins during the early arterial phase was considered an indirect sign of the presence of hepatic artery to hepatic vein shunts (arteriosystemic venous shunt). Evidence of dilated portal veins communicating with the large systemic or hepatic vein during the portal venous phase was considered a sign of intrahepatic communication between the portal and hepatic veins (portosystemic venous shunt).
The radiologists also evaluated the presence of parenchymal perfusion disorders, which consisted of hyperattenuating segmental or subsegmental areas, and the presence of vascular lesions. Round highly enhanced lesions with a diameter of less than 10 mm and a prevalently peripheral arrangement were considered parenchymal hepatic telangiectases, and enhanced lesions with a diameter of more than 10 mm were considered large confluent vascular masses. The term large confluent vascular masses, which to our knowledge has not been mentioned before in the literature, was a term we introduced to depict the aspects of these lesions and the probable underlying formation process. In the evaluation of these vascular lesions, a comparison was made between transverse scans and MIP and multiplanar reformatted images and was based on the number of and conspicuity of improvement of the telangiectases subjectively as detected by observers.
The presence of indirect signs of portal hypertension was evaluated: portal venous dilatation was noted when the diameter was larger than 13 mm (22–24). The diameter was measured on transverse CT scans at the level of the largest section of the portal vein, just before the portal bifurcation, by using an automatic software tool. Splenomegaly (longitudinal spleen diameter larger than 130 mm), gastroesophageal varices and other venous collaterals, and ascites were assessed, as was the presence of anatomic variants of the hepatic arterial supply.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Vascular Lesions
Telangiectases were found during the arterial phases in 33 of 52 (63%) patients. In nine cases, the vascular ectasias (Fig 5), which appeared as round formations 5–7 mm in diameter with a prevalently peripheral arrangement and formation of relationships with vascular branches with the same attenuation, were better identified with MIPs and multiplanar reformations in comparison with the transverse CT scans. In 13 of 52 (25%) patients, a total of 27 large confluent vascular masses were detected, with diameters ranging from 1 to 3 cm (Figs 1, 4). In all cases, they were characterized by early enhancement that persisted during both arterial phases.
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Of the four patients with clinical manifestations, isolated arteriovenous shunts were detected in patient 25, who experienced congestive heart failure, while arterioportal shunts alone (patient 54) or those associated with arteriovenous shunts (patients 18 and 52) were recognized in the three patients with hematemesis. CT also showed a dilated portal vein and splenomegaly in these three patients, together with gastroesophageal varices in patient 54. Esophagogastroduodenoscopy was used to confirm the presence of gastrointestinal telangiectases in these three patients and recent bleeding of esophageal varices in patient 54.
Vascular Anatomic Variants
Anatomic variants of the hepatic arterial supply were detected in seven of 52 (13%) patients: A left hepatic artery originating from the left gastric artery was evident in two patients, an accessory right hepatic artery originating from the superior mesenteric artery was recognized in two others, and both abnormalities were present in one (Fig 5). In one patient, a hepatic artery was observed to originate from the superior mesenteric artery, and in the other patient, the left hepatic artery ascended directly from the aorta.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Several imaging methods are available for establishing the affected location and the involvement of different organs. Conventional and color Doppler US is widely used for study of the liver because it is readily available, noninvasive, cost-effective, and capable of demonstrating intraparenchymal shunts and other vascular malformations while allowing qualitative and quantitative analysis of the arterial, venous, and portal flows (26). Essentially, US has assumed a screening and follow-up role (4,14), although the main limitation is low sensitivity and spatial resolution in the detection of small arteriovenous shunts (15).
MR imaging performed with dynamic and angiographic sequences provides information similar to that obtained with CT in the study of hepatic disorders (4,11,27–29). However, only few reports of MR imaging of the hepatic location of this disease have been published in the literature.
Angiography, which was the most useful imaging method for assessment of vascular abnormalities in the past (30–32), nowadays seems to be indicated only in selected cases for hemodynamic measurement in symptomatic patients or for pretransplantation work-up. A therapeutic role of hepatic arterial embolization in the prevention of cardiac failure (32,33) or the reduction of life-threatening portal hypertension (19) has been proposed but is controversial because of its unpredictable results and association with a high risk of fatal hepatic necrosis (34–36).
Helical CT scanners, particularly multi–detector row scanners, which can scan three to seven times faster than can single–detector row scanners, enable us to perform a complete multiphasic study of the hepatic vascular system. In comparison to traditional helical CT, multi–detector row CT also improves the quality of multiplanar and angiographic (MIP and volume rendering) reconstructions and increases the diagnostic accuracy of this imaging method, thanks to the thinner section thickness (37).
In our study, hepatic vascular alterations were found in 74% of patients with an established or suspected diagnosis of HHT. In our experience, hepatic involvement has thus proved to be more frequent than that in reports by other authors (9–11); this is probably related to the higher general sensitivity of the imaging methods in the detection of hepatic alterations, compared with those in use in the past and clinical findings alone. We searched for these hepatic disorders even in patients with limited clinical symptoms and only suspected hepatic involvement but with a family history of HHT, and it is likely that with greater availability and use of multi–detector row CT, more and more patients will be scanned, and the unexpected findings of vascular abnormalities, which are fairly classic for HHT of liver, will be detected.
Vascular shunts were found in all 52 patients with hepatic involvement. Arterioportal shunts, the most common type, which are typically found with high frequency in patients with cirrhosis and hepatocellular carcinoma or benign hepatic neoplasms (19), were identified in 52% of patients. Isolated arteriosystemic shunts were recognized in 15% of patients, although in other disorders they have rarely been found and are generally associated with benign and malignant neoplasms (19,38). Both of these shunts coexisted in 33% of our patients. A multiphasic liver study with a double arterial phase has been proposed for the assessment of hypervascular hepatocellular carcinoma (39–41), although discordant results have been obtained. Instead, the advantage of supplying a clear temporal separation among the arterial, arteriolar, and venous phases with different enhancing patterns of parenchyma, arteries, and portal and hepatic veins could help to detect hypervascular alterations other than hepatocellular carcinoma, such as shunts or arterial anomalies, thus reducing the risk of misdiagnosis (42). In our study, all arterioportal and arteriosystemic shunts were detected during the early arterial phase, while the late arterial phase was less diagnostic for the shunt type, and portal venous phase CT scans showed no abnormalities.
In the absence of shunts, the portal veins were not completely filled with contrast medium in the early arterial phase, so they were not enhanced or were only slightly hyperattenuating, and the hepatic veins were not enhanced. In the late arterial phase, the hepatic parenchyma, portal veins, and sometimes hepatic veins began to be well enhanced, which impeded definite detection of this kind of hepatic vascular alteration. No intrahepatic spontaneous portosystemic venous shunts were detected in our group of patients. Likewise, few cases have been reported in the literature, and they are generally associated with cirrhosis (21,43) and rarely seen in patients with HHT (15,44).
The existence of arteriosystemic or arterioportal intrahepatic shunts that are not correlated with other pathologic conditions (ie, neoplasia, cirrhosis, trauma) should raise the suspicion of HHT, even if patients are asymptomatic for visceral involvement or have no family history of the disease. In these patients, the presence of other diagnostic criteria should be analyzed, and investigation should eventually be extended to their family members.
Abnormal parenchymal perfusion was recognized in 65% of patients, all with arterioportal shunts, and was referable to the transient hepatic parenchymal enhancement phenomenon (or transient hepatic attenuation differences) (16,45,46). These hepatic perfusion disorders appear during the arterial phases as hyperattenuating parenchymal areas that become isoattenuating on portal venous phase images. Such areas of transient enhancement, which are usually peripheral and wedge shaped with straight margins and lobar, segmental, or subsegmental distribution (46), reflect a change in the normal dual blood supply of the liver and are frequently associated with arterioportal shunts. Decreased portal venous flow due to the presence of shunts determines a preferential redistribution of arterial flow to a hepatic lobe or segment, which therefore appears enhanced (16,47). Thus, the evidence of transient hepatic parenchymal enhancement should be interpreted as another indirect sign of the presence of an arterioportal shunt.
The disorders of angiogenesis control mechanisms typical of HHT could explain the occurrence of other lesions, such as vascular abnormalities in the liver parenchyma: telangiectases and large confluent vascular masses were detected in 63% and 25% of our patients, respectively. Although the number and size of these vascular lesions seemed to increase in the late arterial phase, recognition and differentiation of these lesions from the vascular branches were easier during the first arterial phase, when they were more conspicuous because of lesser enhancement of the portal and hepatic veins and the hepatic parenchyma. Round enhanced formations a few millimeters in diameter with a prevalently peripheral arrangement were considered to be telangiectases and are perhaps analogous to those that can be found in the nose, skin, and gastrointestinal tract. These small vascular spots were more readily recognizable on the reconstructed multiplanar reformatted and MIP images, which enhance the difference in attenuation between hepatic parenchyma and vascular structures. Large confluent vascular masses appear as larger vascular pools with early and persistent enhancement during the arterial phases after contrast medium injection. Presumably, they are large areas of multiple telangiectases that coalesce or large shunts that are directly visible.
Our study findings confirmed that liver involvement tends to be asymptomatic or characterized by nonspecific clinical manifestations: only four of 52 (8%) patients were symptomatic. The heart failure in patient 25 could be attributed to the intrahepatic left-to-right shunt caused by the arteriovenous shunts. The three patients with hematemesis had CT findings of a dilated portal vein and splenomegaly, which would indicate a portal hypertension condition (24), and had endoscopic findings of gastrointestinal telangiectases. Only in patient 54 were the CT signs associated with large gastroesophageal varices, which were confirmed with esophagogastroduodenoscopy. Therefore, in patients with HHT, a dilated portal vein in the absence of other clinical or instrumental findings should not be interpreted as a definite sign of portal hypertension. A portal vein diameter larger than 13 mm is a frequent finding in these patients with hepatic involvement: it was detected in 31 patients alone or associated with splenomegaly, so it may be related to hepatic artery to hepatic vein shunts or hepatic artery to portal vein shunts. In the former, corrected hepatic wedge pressure is normal, while in the latter, it will be elevated. Many of the patients in this study had both shunt types, so only a direct measure of the hepatic wedge pressure would enable us to ascertain the presence of portal hypertension. Our symptomatic patients’ hematemesis episodes could be traced back to variceal bleeding only in one patient, which was certainly a consequence of the portal hypertension, while in the other two cases, it was probably old blood vomited up from large epistaxis or gastric telangiectases.
Vascular anatomic variants were found in only 13% of patients, and in view of this limited incidence, it was impossible to establish whether they were chance findings or abnormalities related to the disease. In the literature, however, anatomic variations of hepatic vasculature are described in these patients (11), so a precise assessment of vascular anatomy is fundamental, especially in candidates for liver transplantation (12,48–50).
The study of hepatic parenchyma in patients with HHT is important from the clinical point of view, because the presence of any vascular alterations, even if usually asymptomatic, could induce serious complications, such as pulmonary hypertension or cardiac failure (10,13–15). Other symptoms, such as portal hypertension, portosystemic encephalopathy, cholangitis, and atypical cirrhosis (11,16), are also certainly related to hepatic vascular lesions. This explains why, in such patients with advanced symptoms, liver transplantation remains the only therapeutic possibility (12,48–50).
The main limitations of the present study are lack of assessment of interreader agreement, absence of angiographic confirmation of CT findings, and lack of radiologic-pathologic correlation based on liver biopsy findings. In general, however, the absence of substantial symptoms does not justify the use of invasive procedures, such as angiography and recourse to liver biopsy, which could be dangerous because of the diffuse vascular alterations and are not helpful in establishing the presence of liver disease or classifying its type (12). The major purpose of the present study, which was conducted in a large group of patients with HHT, was to define the hepatic CT findings. The identification of these findings, if corroborated by clinical findings, in the absence of other causes of liver disease will be sufficiently diagnostic of hepatic involvement. Further investigations are required to confirm our findings.
In conclusion, the assessment of hepatic involvement in patients with HHT is important because of the high frequency of HHT and the risk of serious complications. Diagnosis of the condition is based on clinical-historical data, while diagnostic imaging has a fundamental role in the detection of disorders involving various anatomic regions. Because of its ability to acquire multiphasic images of the liver and provide high-quality multiplanar and angiographic reconstructions, multi–detector row helical CT enables detection and characterization of the complex anatomic-pathologic alterations typical of this disease.
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FOOTNOTES |
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Abbreviations: HHT = hereditary hemorrhagic telangiectasia, MIP = maximum intensity projection
Author contributions: Guarantors of integrity of entire study, G.A., A.R.; study concepts, A.A.S.I., M.M., A.C., G.A.; study design, A.A.S.I., M.M., A.C.; literature research, M.M., A.C.; clinical studies, A.C., C.S.; data acquisition, M.M., A.C.; data analysis/interpretation, A.A.S.I., M.M.; statistical analysis, M.M., A.C., C.S.; manuscript preparation, M.M., A.A.S.I.; manuscript definition of intellectual content, A.R., C.S., G.A.; manuscript editing, M.M., A.A.S.I., A.C.; manuscript revision/review, M.M., G.A., C.S.; manuscript final version approval, A.R., G.A., C.S.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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