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(Radiology. 2001;220:337-342.)
© RSNA, 2001

Gastrointestinal Imaging

Hemangioma-like Lesions in Chronic Liver Disease: Diagnostic Evaluation in Patients1

Eugenio Caturelli, MD, Maurizio Pompili, MD, Francesca Bartolucci, MD, Domenico A. Siena, MD, Marco Sperandeo, MD, Angelo Andriulli, MD and Michele Bisceglia, MD

1 From the Division of Gastroenterology, Division of Medicine, Department of Anatomy and Histopathology, Ospedale Casa Sollievo della Sofferenza, Istituto di Ricovero e Cura a Carattere Scientifico, Viale Cappuccini, I-71013 San Giovanni Rotondo, Foggia, Italy (E.C., D.A.S., M.S., A.A., M.B.); Department of Internal Medicine, Università Cattolica del Sacro Cuore, Rome, Italy (M.P.); and Department of Radiology and Diagnostic Imaging, Università di Ancona, Italy (F.B.). Received August 4, 2000; revision requested September 20; final revision received January 11, 2001; accepted January 22. Address correspondence to E.C. (e-mail: e.caturelli@tiscalinet.it).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To quantify the risk of misdiagnosis of focal hepatic lesions manifesting at ultrasonography (US) as typical hemangiomas in a population at high risk for hepatocellular carcinoma (HCC) and to identify the most effective approach to their diagnostic evaluation.

MATERIALS AND METHODS: A total of 1,982 patients with newly diagnosed cirrhosis underwent US and serum {alpha}-fetoprotein determinations for early detection of HCC. Focal lesions with typical features of hemangioma were evaluated with confirmatory findings of contrast material–enhanced dynamic or spiral computed tomography (CT) and/or single photon emission CT with technetium 99m-labeled red blood cells and, in the absence of confirmatory imaging findings, US-guided fine-needle biopsy. Patients whose initial US scan depicted no lesions or hemangiomas were enrolled in a US follow-up program. All hemangioma-like lesions detected during follow-up were evaluated, or biopsy was performed.

RESULTS: US depicted hemangioma-like lesions in 44 of 1,982 patients: 22 hemangiomas and 22 HCCs. Hemangioma-like lesions detected during follow-up in 1,648 patients were HCCs (n = 22) or dysplastic nodules (n = 4). Only 85 (22%) of 383 patients with HCC had {alpha}-fetoprotein levels suggestive of the diagnosis. The probability of a diagnosis of HCC (or preneoplastic lesion) is 100% for hemangioma-like lesions depicted on subsequent US scans.

CONCLUSION: If initial US examination of a cirrhotic liver depicts a hemangioma, confirmatory findings of imaging studies are necessary since 50% of hemangiomas in this study were hyperechogenic HCCs. US-guided biopsy can be safely performed, and its findings can be used to confirm the diagnosis.

Index terms: Angioma, 761.3194 • Liver, CT, 761.12112, 761.12115 • Liver, SPECT, 761.12162 • Liver, US, 761.12981 • Liver neoplasms, 761.323


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Hepatic hemangiomas typically appear at ultrasonography (US) as round hyperechoic lesions with well-defined irregular margins; in some cases, there are central zones of decreased echogenicity (1–6). This appearance is considered highly suggestive of hemangioma, and findings with additional studies, such as computed tomography (CT) (7,8), magnetic resonance (MR) imaging (9), and/or single photon emission CT (SPECT) with technetium 99m (99mTc)-labeled red blood cells (RBCs) (10), usually confirm the US diagnosis (11). In a recent article, Leifer et al (12) suggested that these confirmatory findings of studies are unnecessary when the typical US features of hepatic hemangioma are found in patients with a low risk for hepatic malignancy (primary or metastatic).

A number of other benign conditions and lesions (eg, focal fatty changes, adenomas, focal nodular hyperplasia, lipoma) can, in fact, mimic hemangioma at US, and such manifestations are even more common for malignant liver lesions, including hepatocellular carcinomas (HCCs) (13–15) and metastases (16). Differential diagnosis of a hemangioma-like lesion (HLL) is, therefore, somewhat more complicated in a patient who is at high risk for hepatic malignancy, and additional imaging studies are generally performed to exclude the possibility of hyperechoic HCC (11). Reliable diagnosis is sometimes impossible even with contrast material–enhanced CT, MR imaging, or SPECT with 99mTc-labeled RBCs, particularly when the lesion is small and targeted biopsy is necessary to obtain a diagnosis (17).

We recently completed a prospective study of a large population of patients with cirrhosis enrolled in a follow-up screening program for early detection of HCC. All HLLs observed at US at patient enrollment or during subsequent follow-up examinations were evaluated with confirmatory findings of imaging studies and/or US-guided fine-needle biopsy (FNB). The purpose of our study was to quantify the risk of misdiagnosis of these lesions in a population at high risk for HCC and to identify the most effective approach to their diagnostic evaluation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Prior approval of the study was obtained from the Medical Ethics Commission of the Ospedale Casa Sollievo della Sofferenza, San Giovanni Rotondo, Foggia, Italy. Informed consent was obtained from all participating patients after the nature of all procedures had been fully explained. During the 7 years between January 1992 and December 1998, we enrolled 1,982 patients (1,287 men, 695 women; mean age, 67.1 years; age range, 28–81 years) with newly diagnosed cirrhosis in a follow-up program for early detection of HCC.

The majority had clinical diagnoses (hepatosplenomegaly, ascites, spider angioma, portosystemic collateral vessels), blood chemistry levels (decreased albumin and total serum cholesterol levels; increased serum {gamma}-globulin levels; prolonged prothrombin time; increased aspartate aminotransferase, alanine aminotransferase, and total bilirubin serum levels; low platelet count), and US findings (nodular liver surface; caudate lobe hypertrophy; coarse liver tissue pattern; and/or signs of portal hypertension, ie, dilated portal, splenic and mesenteric veins, spontaneous portosystemic shunts) that were consistent with cirrhosis.

In 42 patients, however, the diagnosis was based on the results of a liver biopsy performed to evaluate chronic hepatitis. The cirrhosis was related to hepatitis C viral infection in 1,725 (87%) patients, hepatitis B in 108 (5%), both hepatitis C and B viruses in 32 (2%), and ethanol consumption in 75 (4%). Thirteen (1%) patients had hemochromatosis, ten (0%) had primary biliary cirrhosis, and in 19 (1%) patients, the cause of the cirrhosis could not be determined.

Preliminary Screening
Prior to enrollment, each patient underwent abdominal US with a real-time scanner (SSA-250A; Toshiba Medical Systems, Tokyo, Japan) and a 3.75-MHz convex probe, and the serum {alpha}-fetoprotein (AFP) level was determined to identify any preexistent lesions. When a solid focal liver lesion with a hypoechoic, mixed, or bull’s-eye appearance was observed, together with a serum AFP level of more than 200 ng/mL (200 µg/L), HCC was diagnosed (18), and the patient was scheduled for treatment. In the absence of AFP levels suggestive of a diagnosis, nodules with the characteristic US appearance of HCC were evaluated with US-guided FNB after verification of satisfactory coagulation (platelet counts, >40,000 per cubic millimeter [40 x 109/L]; prothrombin activity, >40%; or international normalized ratio, <2). A freehand technique (19) was used with a cutting needle (Histocut; Sterylab, Rho-Milan, Italy). This approach usually provides sufficient pathologic material with only one puncture for both histologic and cytologic studies (20). When the biopsy findings revealed HCC, the patient was excluded from the follow-up study and was scheduled for treatment.

When the initial US findings revealed a focal liver lesion with the typical characteristics of hemangioma (ie, diameter, <3 cm; well-defined, irregular margins; hyperechogenicity with or without small central areas of hypoechogenicity), the patient underwent contrast-enhanced dynamic CT (X Peed; Toshiba Medical Systems). After automated power injection of a 150–200-mL bolus of 60% iodinated nonionic contrast material (iopamidol, Iopamiro 300; Bracco, Milan, Italy) at a rate of 3 mL/sec, 10-mm-thick transverse sections were acquired at 10-mm intervals. This method was used for all CT examinations performed during the first 4 years of the study, whereas multiphasic helical CT was used during the last 3 years (1996–1998).

The helical scans were obtained with a commercially available scanner (X Press/GX; Toshiba Medical Systems) after injection of 150 mL of iopamidol. The latter was administered via the antecubital vein with an automated power injector at a rate of 3.0–3.5 mL/sec. By using the double-pass technique, the entire liver was scanned in a craniocaudal direction (image thickness, 5 mm; table speed, 5 mm/sec; pitch of 1.0–1.5; length of each pass, 25–30 seconds). The arterial and portal venous phases began 25–30 and 50–60 seconds, respectively, after initiation of the infusion of contrast material.

When the results of the CT study were unequivocally indicative of hemangioma (7,8), no additional studies were performed on the lesion in question, and the patient was enrolled in the follow-up program for early detection of HCC. If the CT scan was inconclusive for hemangioma or revealed features suggestive of HCC, SPECT with a gamma camera (901/A; Toshiba Medical Systems) and 99mTc-labeled RBCs was performed. In the absence of findings that would confirm the diagnosis of hemangioma (10), a US-guided FNB was performed to evaluate the histologic and cytologic characteristics of the lesion (as described previously). Patients with HLLs that ultimately proved to be HCC were scheduled for treatment, while those with final diagnoses of hemangioma were entered into the follow-up program, which will be described next.

Follow-up Screening
All patients without evidence of solid focal lesions at enrollment and those whose preexistent lesions had proved to be hemangiomas were invited to take part in the follow-up program for early detection of HCC on the basis of both abdominal US findings and the serum AFP determination at 4-month intervals. The diagnostic protocol for HCC-like lesions detected during the entire follow-up was the one used during the initial screening.

In contrast, two different approaches were used for HLLs detected during the follow-up study. During the first 4 years of the study (January 1992 through December 1995), all newly detected HLLs were evaluated according to the same protocol used during the preliminary screening. In light of the results obtained, this protocol was modified, and, as a result, all new HLLs detected between January 1996 and December 1998 were immediately evaluated with US-guided FNB without resorting to the use of contrast-enhanced dynamic or spiral CT or SPECT with 99mTc-labeled RBCs (ie, the same protocol used for HCC-like lesions that were not associated with increases in serum AFP suggestive of the diagnosis).

Regardless of the US characteristics of the nodule in question, FNB was always repeated if the first specimen collected was inadequate for a definitive diagnosis. None of the biopsies were associated with complications. All pathologic diagnoses (histologic or cytologic or both) of HCC were considered definitive, and the patients were excluded from further follow-up and were scheduled for appropriate treatment.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Preliminary Screening
Table 1 summarizes the results of preliminary screening of the 1,982 patients with cirrhosis in terms of the prevalence and actual nature of focal lesions with the characteristic features of hemangioma (Figs 1, 2). Forty-one of the 44 patients with HLL had single lesions, and each of the remaining three patients had two lesions. The diameters of the HLLs ranged from 8 to 31 mm (mean, 23 mm). None of the HLLs were associated with increased serum AFP levels, and all 44 patients underwent contrast-enhanced CT.


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  		TABLE 1. Results of Preliminary Screening of 1,982 Patients with Newly Diagnosed Cirrhosis: Prevalence and Final Diagnosis of HLLs

 


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  		Figure 1. Preliminary transverse abdominal US scan in a patient with recently diagnosed hepatic cirrhosis. A small (2-cm-diameter) well-defined, hyperechoic lesion (arrowheads) with irregular margins is evident in the second hepatic segment. The final diagnosis was hemangioma.

 


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  		Figure 2. Preliminary subcostal oblique abdominal US scan in a patient with recently diagnosed hepatic cirrhosis. A 1-cm-diameter HLL (arrowhead) can be seen in the eighth hepatic segment. The final diagnosis was HCC.

 
The latter examination findings supported definitive diagnoses of hemangioma in 12 patients. In the remaining 32 patients, the CT results indicated possible HCC in 14 (including all three with two lesions) and were inconclusive in the remaining 18. These 32 patients underwent SPECT with 99mTc-labeled RBCs, which revealed hemangioma in 10 patients (all with single lesions). In the remaining 22 patients, no areas of increased uptake were observed at SPECT with 99mTc-labeled RBCs, and FNB was thus performed. Neither CT nor SPECT with 99mTc-labed RBCs depicted lesions that were not seen at US screening.

The biopsy findings showed HCC in 19 of the 22 patients. In the remaining three patients, findings in the first specimen were nondiagnostic, but HCC was diagnosed on the basis of findings of a second FNB specimen. There were no complications during or after the biopsies.

Follow-up
Table 2 shows the results of our follow-up study. Nineteen of 22 patients with hemangiomas agreed to take part in the follow-up study along with 1,816 others whose preliminary screening had revealed no focal liver lesions or focal liver lesions that were not HCC. Of the 1,835 patients who were enrolled in the follow-up, 187 (none of whom had initial diagnoses of hemangioma) were excluded from the final analysis because they had missed all three of the scheduled examinations for 1 or more years. The final evaluation was, thus, based on a total of 1,648 patients (1,059 men, 589 women; mean age, 65.2 years; age range, 28–81 years) who had been examined at least twice a year for 1 or more years (mean number of follow-up examinations per patient, 17.8; range, 14–21; mean length of follow-up, 51.6 months; range, 6–84 months). In this group, the cause of cirrhosis was attributed to hepatitis C virus in 1,464 (88.8%) patients, to hepatitis B virus in 82 (5%), to both viruses in 24 (1%), to ethanol use in 48 (3%), and to hemochromatosis in ten (1%); seven (0%) patients had primary biliary cirrhosis, and in the remaining 13 (1%) patients, the cause of cirrhosis was not identified.


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  		TABLE 2. Results of Follow-up Screening of 1,648 Patients with Newly Diagnosed Cirrhosis with No Evidence of HCC at Baseline: Prevalence and Final Diagnosis of HLLs

 
During the first 4 years of the follow-up program, 149 patients manifested new solid focal liver lesions, which were classified as HLLs in 12 (8%) (Fig 3). All of these HLLs were single lesions with diameters of 8–26 mm (mean, 17 mm), and none were associated with increases in serum AFP levels. All 12 patients underwent contrast-enhanced CT; findings indicated HCC in seven and were inconclusive in the remaining five. Findings at SPECT with 99mTc-labeled RBCs were negative for hemangioma in all 12 of these patients. Neither CT nor SPECT with 99mTc-labeled RBCs depicted lesions that were not seen at US screening in this group of patients too. The final diagnoses were based on findings at US-guided FNB, which showed that 10 patients had HCCs and the other two had dysplastic nodules. Again, there were no complications during or after the biopsies.



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  		Figure 3. Follow-up subcostal oblique abdominal US scan in a patient with cirrhosis whose initial scan depicted no focal lesions. A 1-cm-diameter HLL (arrowhead) is evident in the seventh hepatic segment. The final diagnosis was dysplastic nodule.

 
During the last 3 years of the follow-up program (January 1996 through December 1998), we performed FNB on all HLLs when they were detected at US because of the high percentage of HLLs that ultimately proved to be HCCs. Of the 138 solid focal liver lesions detected during this period, 14 (10%) were HLLs. All of the latter lesions occurred singly, with a mean diameter of 19 mm (range, 9–28 mm), and none were associated with serum AFP levels of more than 200 ng/mL (200 µg/L). Findings at the initial FNB revealed HCC in nine of 14 cases and dysplastic nodules in two others. In the remaining three cases, HCC was diagnosed on the basis of findings of a second biopsy. As shown in Table 2, all of the HLLs that were depicted during the US follow-up proved to be malignant (22 cases) or premalignant (four cases) (Fig 3) lesions. A {chi}2 test was performed that showed that the differences in the proportions of HCC diagnosed in the two periods of follow-up were not statistically significant.

All 19 of the patients with hemangioma who entered the follow-up program were included in the final analysis. During follow-up (mean for these patients, 49 months; range, 24–84 months), none of their lesions showed any change in size, which is considered typical of hemangioma (21,22), and none of the patients had any marked increases in serum AFP level or new focal lesions at US. Only 85 (22%) of 383 patients with HCC had AFP levels suggestive of the diagnosis. The probability of a diagnosis of HCC (or preneoplastic lesion) is 100% for hemangioma-like lesions depicted on subsequent US scans.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
REFERENCES
 
Diagnostic evaluation of HLLs is of crucial importance in patients with chronic liver disease and/or cirrhosis in whom an early and definite diagnosis of HCC is essential for treatment and prognosis (23,24). HCC, which is a major risk for these patients, may manifest with a variety of features at US, including hyperechogenicity (13–15,25). The latter pattern has been attributed to a number of factors that are thought to increase echogenicity within the tumor (13–15,26). Necrosis and interstitial fibrosis, which often appear as the HCC nodule grows, can transform an initially hypoechoic tumor into one that is hyperechoic (14,27). Increased echogenicity can also be the result of intratumoral fatty changes and/or dilated sinusoids. This pattern is somewhat less common than the one previously described, but it is more likely to cause diagnostic problems in a screening program like ours because the hyperechogenicity is already present when the HCC nodule is small. In these cases, the appearance at US is that of a small echoic lesion that is indistinguishable from the typical hepatic hemangioma (14) (Fig 2).

The prevalence of hepatic hemangioma in the general population is high (from 4% to 7.3%) (28), and, as our findings show, an HLL detected at the first US examination of a patient with cirrhosis may well be an actual hemangioma (as were 50% of the HLLs in our series). In high-risk patients of this type, however, the possibility of a malignant lesion must be excluded with at least two additional imaging studies. The choice of the methods to be used for the latter purpose are, to some extent, based on institutional preferences and resources. When our study began in 1992, we chose to perform contrast-enhanced dynamic CT as the initial confirmatory study because of its proven value in distinguishing hemangiomas from HCCs (7,8,29). It is also capable of depicting additional lesions that may not have been seen at hepatic US (although this did not occur in any of the cases included in the present study).

In the few cases in which we were unable to make a reliable diagnosis on the basis of CT findings, SPECT with 99mTc-labeled RBCs was used to correctly identify all other hemangiomas in this series, confirming its well-known accuracy in this setting (10). Our experience with spiral CT during the last 3 years of the study was equally positive. Although comparison of the two tomographic techniques is beyond the scope of this article, it is well known that the spiral technique offers substantial advantages in this setting (29,30). MR imaging with the use of heavy T2 weighting and dynamic enhancement with a gadolinium-based contrast agent is also a sensitive tool for the diagnosis of hepatic hemangiomas (9), and recent publications (31,32) indicate that contrast-enhanced MR imaging techniques are at least equivalent to helical CT in the detection of HCC nodules (sensitivity, 81%–94%).

In the 22 cases in which hemangioma had been excluded on the basis of imaging study findings, US-guided FNB was performed to obtain a pathologic diagnosis. This approach is both safe and reliable (33,34), even for the diagnosis of small HCC nodules (17,20). Moreover, in contrast to all imaging techniques (35), US-guided FNB provides almost absolute specificity so that treatment can be initiated promptly (15,23). In our study, FNB findings confirmed the diagnosis of HCC in all 22 patients (in 19 patients at the first attempt and in the remaining three at the second attempt). This experience indicates that, once the diagnosis of hemangioma has been excluded, HLLs depicted on the initial US scan of a cirrhotic liver are very likely HCCs.

The risk of HCC is even greater when an HLL is detected in a patient who has been undergoing US screening for some time. Our experience indicates that in a mean follow-up of approximately 41/2 years, approximately 17% of a high-risk cirrhotic population will develop new sonographically detectable liver lesions. Our close follow-up program allowed early detection of small HCCs (mean diameter, 18 mm) and four dysplastic lesions.

Hemangiomas are usually congenital, and they are known for their lack of growth over time. As our experience during the first 4 years of our study showed, it is, therefore, highly improbable that a vascular lesion of this type will enlarge to reach detectable dimensions during follow-up. In fact, confirmatory findings of imaging revealed that none of the 12 HLLs we observed during the first 4 years of follow-up (approximately 12 [8%] of 149 of all new lesions detected) were actually hemangiomas, and subsequent US-guided FNB findings demonstrated that 10 were HCCs and the remaining two were preneoplastic lesions. Therefore, in 1996 we decided to forego additional imaging studies for the detection of HLLs emerging during the US follow-up of patients with cirrhosis. As in all other solid lesions observed in this setting, FNB was performed in HLLs as soon as possible. The results of the second part of our study support our decision: All 14 HLLs detected during the second follow-up period (approximately 14 [10%] of 128 of all new lesions) proved once again to be HCCs (12 cases) or preneoplastic lesions (two cases).

It is also important to note that in the present series, biopsy was not performed in hemangiomas. All hemangiomas depicted on the preliminary scans and those detected during the first 4 years of the follow-up were correctly identified by using imaging techniques, and biopsy was performed only when findings of these studies had excluded the vascular nature of the lesion with a high degree of certainty. Although FNB is not generally recommended if a hemangioma is suspected, we regarded the HLLs in which biopsy was directly performed in the latter half of our study as probable HCC rather than suspected hemangioma. This position was supported with findings of our experience during the previous 4 years and was confirmed with the direct biopsy findings. However, US-guided FNB has proved to be safe even when the lesion in question is actually a hemangioma (36–38), and, in some instances, it may allow a specific diagnosis.

Another point to be stressed is the low diagnostic value of the use of the serum AFP level in distinguishing hyperechoic HCC from typical-appearing hemangioma. None of the 48 HLLs that were actually HCCs or preneoplastic lesions (22 detected at the first US examination and 26 detected during follow-up) were associated with a marked increase in serum levels of this marker. Although such increases are highly specific for HCC, the sensitivity of the AFP level is at best approximately 25% (18,39). Indeed, only 85 (22%) of 383 patients in this series whose HCCs manifested with more classic US features had serum AFP levels higher than 200 ng/mL (200 µg/L). Therefore, uniform absence of this marker among our patients with hyperechoic HCC is, perhaps, not surprising. On the other hand, it may be that these tumors represent a particular subset of non–AFP-secreting HCCs.

In conclusion, regular US screening of patients with cirrhosis can reveal extremely small focal liver lesions, the vast majority of which will prove to be HCC. However, if the initial US scan depicts a lesion with the typical features of hemangioma in a patient with cirrhosis, there is a good possibility (approximately 50%) that the lesion is a congenital or preexistent vascular lesion that is unrelated to the chronic liver disease, but the tentative diagnosis of hemangioma should always be confirmed with findings of additional imaging studies, such as spiral CT, SPECT with 99mTc-labeled RBCs, and/or MR imaging. If findings of the latter methods fail to confirm the presence of a hemangioma, the lesion is in all probability a hyperechoic HCC (even if serum AFP levels are within normal limits), and US-guided FNB should be performed as soon as possible. In contrast, HLLs that are detected in cirrhotic livers during the course of screening, that is, after findings on previous scans have already been used to exclude the presence of congenital vascular lesions, should be treated as probable HCCs. In these cases, we believe that the use of immediate FNB without additional imaging studies is the most rapid and effective way to arrive at a reliable diagnosis and, thereby, to initiate prompt treatment.


   ACKNOWLEDGMENTS
 
The authors thank Marian E. Kent for editorial assistance and Matteo Palladino, Department of Scientific Photography, Ospedale Casa Sollievo della Sofferenza, San Giovanni Rotondo, Foggia, Italy, for technical assistance.


   FOOTNOTES
 
Abbreviations: AFP = {alpha}-fetoprotein, FNB = fine-needle biopsy, HCC = hepatocellular carcinoma, HLL = hemangioma-like lesion, RBC = red blood cell

Author contributions: Guarantor of integrity of entire study, E.C.; study concepts and design, all authors; literature research, F.B.; clinical studies, E.C., A.A.; data acquisition, D.A.S., M.S.; data analysis/interpretation, all authors; manuscript editing, E.C., M.P.; manuscript preparation, definition of intellectual content, revision/review, and final version approval, all authors.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
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