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Focal Liver Lesions: Pattern-based Classification Scheme for Enhancement at Arterial Phase CT¹

¹ From the Department of Radiology, Stanford University Medical Center, Stanford, Calif (M.N.M., E.W.O., R.B.J., R.L.L., C.F.B.); the Radiology Service (114), Veterans Affairs Palo Alto Health Care System, 3801 Miranda Ave, Palo Alto, CA 94304 (M.N.M., E.W.O.); and the Department of Radiology, University of California Davis, Sacramento (K.A.J.). Received November 9, 1998; revision requested January 5, 1999; final revision received August 31; accepted September 15. Address correspondence to M.N.M. (e-mail: ninomurcia@forsythe.stanford.edu).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To present our early experience with a classification scheme for categorizing focal liver lesions on the basis of the enhancement patterns that they exhibit in the arterial phase of computed tomography (CT) and to determine whether particular enhancement patterns suggest particular diagnoses.

MATERIALS AND METHODS: The authors reviewed arterial phase CT images in 100 consecutive patients with focal liver lesions, excluding simple cysts. The enhancement pattern of the dominant or representative lesion in each patient was classified into one of five categories—homogeneous, abnormal internal vessels or variegated, peripheral puddles, complete ring, or incomplete ring—by three radiologists blinded to the proved diagnosis. Lesions without enhancement were recorded separately. Agreement was reached by consensus in all cases. Standards of reference included findings at histologic examination, correlative imaging, or clinical and imaging follow-up.

RESULTS: Ninety-two percent of the 100 lesions demonstrated arterial phase enhancement. Patterns associated with positive predictive values of 82% or greater and specificity of 80% or greater included abnormal internal vessels or variegated (hepatocellular carcinoma), peripheral puddles (hemangioma), and complete ring (metastasis).

CONCLUSION: The appearance of hepatic lesions in the arterial phase of enhancement has potential use in the determination of specific diagnoses. The classification scheme used in this study may be a useful tool for the interpretation of arterial phase CT studies.

Index terms: Angioma, 761.3194 • Liver, focal nodular hyperplasia, 761.3198 • Liver neoplasms, CT, 761.12112, 761.12114, 761.12115 • Liver neoplasms, diagnosis, 761.32, 761.33 • Liver neoplasms, secondary, 761.33

	Introduction

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With helical computed tomographic (CT) technology, images can be obtained rapidly during the different phases of hepatic parenchymal enhancement. Previous studies have demonstrated improved detection of focal hypervascular liver lesions with this dual-phase technique in comparison with conventional imaging during the portal venous phase alone (1–5). Additionally, recent studies have reported the value of this technique in establishing the diagnosis of focal hepatic lesions on the basis of their appearances during the different phases of enhancement (6,7). The purpose of this study was to present our early experience with a classification scheme for categorizing focal liver lesions on the basis of the enhancement patterns that they exhibit in the arterial phase of CT and to determine whether particular enhancement patterns suggest particular diagnoses.

	MATERIALS AND METHODS

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Patients
Arterial phase CT images were analyzed retrospectively in 100 consecutive patients (42 women and 58 men; age range, 25–84 years; mean age, 57 years) with focal hepatic lesions, excluding simple cysts; adequately enhanced arterial phase images; and an established diagnosis. Adequately enhanced arterial phase images were defined as those exhibiting heterogeneous (moiré) enhancement of the spleen. Scans without adequate enhancement, as determined by consensus, were excluded. Patients were referred for CT evaluation of clinically suspected primary or secondary hepatic neoplasms, further evaluation of abnormalities found on ultrasonographic (US) studies obtained for a variety of indications, or further evaluation of hepatic abnormalities found on imaging studies obtained at other institutions.

Lesions
Only one lesion per patient was analyzed. In patients with multiple lesions, the dominant lesion (on the basis of size) or a representative lesion (when no dominant lesion was apparent) was analyzed. Forty patients had a single lesion: 23 hepatocellular carcinomas (HCCs), seven metastases, five focal nodular hyperplasias (FNHs), five hemangiomas. Sixty patients had multiple lesions: 46 metastases, eight HCCs, four hemangiomas, one cholangiocarcinoma, one abscess. The maximal dimension of the lesions ranged from 1.0 to 16.5 cm (mean, 4.9 cm) for metastases, 1.0–14.3 cm (mean, 5.2 cm) for HCC, 2–10 cm (mean, 4.6 cm) for hemangiomas, and 2.2–7.7 cm (mean, 4.9 cm) for FNH.

The final diagnoses were established at histopathologic examination of surgical or percutaneous biopsy specimens or on the basis of the clinical course and results from follow-up imaging studies (Table 1). Hepatocellular carcinomas were diagnosed in 31 (31%) patients: in 30 at histopathologic examination and in one on the basis of clinical history, elevated -fetoprotein level, and progression of disease depicted on follow-up CT studies obtained during 10 months. Cholangiocarcinoma was diagnosed in one patient at histopathologic examination. Hemangioma was diagnosed in nine (9%) patients: at histopathologic examination in two and on the basis of the characteristic appearance of these lesions on follow-up studies in five (magnetic resonance [MR] imaging in two, US in three, and CT in one). FNH was diagnosed in five (5%) patients: on the basis of technetium 99m sulfur colloid scanning in four and 10-month follow-up MR study in one. Abscess in one patient was confirmed on the basis of positive blood cultures and the response to treatment.

CT Technique
All scans were obtained with a helical CT scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, Wis). An initial nonenhanced scan was acquired with 10-mm section thickness at 20-mm intervals through the liver. After a 20-gauge intravenous cannula was inserted, a total of 150 mL of nonionic contrast medium with 300 mg of iodine per milliliter (Omnipaque; Nycomed, Princeton, NJ) was administered at 4–5 mL/sec. Beginning 25 seconds after initiation of the contrast material injection, a 30-second breath-hold arterial phase helical CT scan was acquired with section thickness of 7 mm and pitch (usually 1.0–1.6) sufficient to cover the entire liver within the breath-hold period. A breath-hold portal venous phase scan was obtained 60–70 seconds after initiation of the injection. Images were reconstructed at 7-mm intervals with use of standard soft-tissue (window width, 400 HU; level, 40 HU) and liver (window width, 150 HU; level, 50–80 HU) display settings.

Image Analysis
The liver and soft-tissue images for each patient were reviewed by three radiologists (R.B.J., E.W.O., M.N.M.) blinded to the final diagnosis. For each patient, the arterial phase enhancement pattern of the dominant or representative lesion was determined relative to the surrounding liver parenchyma and classified into one of five patterns. The "homogeneous" pattern was defined as diffuse uniform enhancement with no more than 10% central low attenuation with any evident vessels having normal contour and branching (Fig 1). The "abnormal internal vessels or variegated" pattern was defined as either visible internal vessels that were irregular in contour and branched in a distorted fashion unlike normal progressive anatomic arborization or randomly distributed hyperattenuating and hypoattenuating regions (Fig 2). The "peripheral puddles" pattern was defined as discrete well-defined peripheral enhancing globules with attenuation equal to that of enhancing arterial structures (Fig 3). The "complete ring" pattern was defined as circumferential ring enhancement surrounding a predominant central region with low attenuation (Fig 4). The "incomplete ring" pattern was defined as noncircumferential ring enhancement (Fig 5). Lesions with no appreciable enhancement on the arterial phase images were recorded separately. Agreement regarding the classification of all lesions was reached by consensus. Disagreements were resolved by majority opinion. The enhancement patterns included in the classification scheme were defined a priori and were based on the authors' previous experience in reviewing abdominal CT scans and enhancement patterns described in the literature (3,6,7).

View larger version (109K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Homogeneous pattern. Transverse arterial phase CT scan of FNH (arrows) with diffuse uniform enhancement.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Abnormal internal vessels or variegated pattern depicted on transverse arterial phase CT scans. (a) HCC with visible internal vessels (arrow) that are irregular in contour. (b) HCC (arrows) with randomly distributed hyper- and hypoattenuating regions.

View larger version (150K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Abnormal internal vessels or variegated pattern depicted on transverse arterial phase CT scans. (a) HCC with visible internal vessels (arrow) that are irregular in contour. (b) HCC (arrows) with randomly distributed hyper- and hypoattenuating regions.

View larger version (111K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Peripheral puddles pattern. Transverse arterial phase CT scan of a hemangioma with peripheral enhancing globules (arrows) with attenuation similar to that of the aorta.

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Complete ring pattern. Transverse arterial phase CT scan of metastases from a small-bowel carcinoid depicts ring enhancement (arrows) with well-defined smooth inner margins surrounding central regions of low attenuation.

View larger version (157K): [in this window] [in a new window] [Download PPT slide]   Figure 5. Incomplete ring pattern. Transverse arterial phase CT scan of a metastasis from an adenocarcinoma of the breast depicts partial ring enhancement (arrow).

	RESULTS

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Enhancement Patterns and Corresponding Diagnoses
The arterial phase enhancement features and final diagnoses of the 100 focal hepatic lesions are summarized in Table 2. Twenty-three lesions demonstrated the homogeneous pattern of enhancement: 13 (57%) HCC, five (22%) FNH, four (17%) metastasis, and one (4%) hemangioma. Ten lesions demonstrated the abnormal internal vessels or variegated pattern of enhancement: nine (90%) HCCs and one (10%) metastasis. Seven lesions demonstrated the pattern of peripheral puddles: six (86%) hemangiomas and one melanoma metastasis (Fig 6). Forty-nine lesions exhibited the complete ring pattern: 40 (82%) metastasis, seven (14%) HCC, one (2%) cholangiocarcinoma, and one (2%) abscess. Three lesions exhibited the incomplete ring pattern: two (67%) hemangiomas and one (33%) metastasis. Eight lesions demonstrated no enhancement: six (75%) metastasis and two (25%) HCC.

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 6. Melanoma metastasis (arrows) exhibits the peripheral puddles pattern. Transverse arterial phase CT scan demonstrates peripheral enhancing globules with attenuation similar to that of the aorta. This appearance is similar to that of the hemangioma in Figure 3.

Table 4 summarizes the arterial enhancement patterns exhibited by metastases. The primary lesions for 13 of the 53 metastases are commonly considered hypervascular, including carcinoid, breast carcinoma, pancreatic neuroendocrine tumor, melanoma, and renal cell carcinoma. The most frequently observed enhancement patterns in these lesions were complete ring in six and homogeneous in three. Enhancement patterns among the remaining four lesions were abnormal internal vessels or variegated in one carcinoid, peripheral puddles in one melanoma, incomplete ring in one breast carcinoma, and no enhancement in one breast carcinoma. The primary lesions for the remaining 40 metastases are commonly considered hypovascular. The most frequently observed enhancement pattern in this group was the complete ring in 34.

	DISCUSSION

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Ninety-two of the 100 lesions included in this study exhibited appearances that met criteria for classification into one of the five enhancement categories; the remaining eight (8%) lesions exhibited no enhancement in the arterial phase. Three arterial phase enhancement patterns were associated with PPVs that exceeded 82% for particular diagnoses, including the abnormal internal vessels or variegated pattern as suggestive of HCC, the peripheral puddles pattern as suggestive of hemangioma, and the complete ring pattern as suggestive of metastases. Accordingly, in our early experience, these arterial phase enhancement patterns can be considered suggestive of these diagnoses.

An ideal imaging sign for the purpose of differentiating one diagnosis from another is one that exhibits both high PPV, meaning that the likelihood of a particular diagnosis is great when the sign is present, and high specificity, meaning that the likelihood of the sign being present in the absence of the particular diagnosis is small. All three arterial phase enhancement patterns associated with PPVs of 82% or greater also were associated with a specificity of 80% or greater: the abnormal internal vessels or variegated pattern for the diagnosis of HCC, the peripheral puddles pattern for the diagnosis of hemangioma, and the complete ring pattern for the diagnosis of metastasis. These three arterial phase enhancement patterns, with both high PPV and high specificity, are likely to be the most clinically useful.

The abnormal internal vessels or variegated pattern indicated HCC with a PPV of 90% and a specificity of 98%. We required lesions in this category to have either abnormal internal vessels or randomly distributed components of both hyperattenuation and hypoattenuation. Our definition for abnormal internal vessels required vessels to be irregular in contour or to branch erratically, findings that reflected neovascularity associated with malignancy in angiographic studies (11). This definition would not include the central feeding vessels described by Van Hoe and colleagues (6) within a small proportion of FNHs, because the arterial supply to such lesions does not exhibit abnormal contours or abnormal arborization (11). Concerning variegated enhancement, hyperattenuation was required specifically in our series, rather than just heterogeneity as described in the mosaic pattern in portal venous phase imaging (12–14), to confer specificity for HCC, which often is hyperattenuating in the arterial phase (1,3,4). This enhancement feature may reflect the presence of viable tumor interspersed with necrosis, as suggested by previous authors (12,15).

The peripheral puddles pattern was associated with hemangiomas in all but one case. Thus, the PPV and specificity of this pattern for hemangioma were 86% and 99%, respectively. The appearance of discrete well-defined peripheral globules isoattenuating with vascular structures has been well established as characteristic of hemangiomas (9,16,17). The only other lesion in our series that exhibited this pattern was a melanoma metastasis; we regard this as atypical, and it may be prudent to consider lesions with this appearance as indeterminate in patients with known melanoma and consider further work-up with MR imaging in such cases.

Lesions with circumferential ring enhancement usually were malignant. When all lesions exhibiting this enhancement pattern were considered, malignancy was predicted with a PPV of 98% (48 of 49) and specificity of 93% (14 of 15). These findings are similar to those in the series of Van Leeuwen and colleagues (7), who found that a hyperattenuating ring in the arterial phase was associated with malignancy in all cases. It is important to bear in mind, however, that not all ring-enhancing lesions are malignant; for example, as noted in one patient in our series, this feature may also be noted with abscesses (18). Lesions with circumferential ring enhancement in our classification scheme were most frequently encountered in metastatic disease. Peripheral enhancement seen in metastases may reflect perfused, viable tumor tissue in the periphery of the lesion and fibrosis or necrosis in the center (7,10,19).

The remaining two enhancement patterns in our categorization scheme, the homogeneous pattern and the incomplete ring pattern, were associated with PPVs too low to be considered clinically useful for the purpose of distinguishing lesions of different histologic origins.

Eight (8%) of the 100 lesions did not exhibit any arterial phase enhancement, including six metastases and two HCCs. This percentage is smaller than that reported in other studies of focal hepatic lesions in general (6,7) and hepatic metastases in particular (5,20,21). Among our metastases, 92% (12 of 13) and 88% (35 of 40) of hypervascular and hypovascular lesions, respectively, exhibited enhancement. We speculate that the higher frequency of enhancement observed in our study may reflect differences in the severity of disease in patients enrolled at different institutions.

An important observation is that overlap can occur between the appearances of benign and malignant lesions. For example, as found in this study and others, the homogeneous pattern can be exhibited by lesions such as HCC, hemangiomas, and FNH (6,7,22,23). Additionally, we found overlap between the peripheral puddles pattern typical of hemangiomas and the enhancement exhibited by one melanoma metastasis. Correlation with portal venous phase images, not the object of this study, may help differentiate lesions that exhibit similar arterial phase enhancement patterns. Likewise, correlation with MR imaging, scintigraphic studies, or biopsy may be required to achieve a definitive diagnosis.

A number of limitations should be considered with this study. First, we focused on visible features exhibited by lesions in the arterial phase, not their detectability or conspicuity. Second, the study was retrospective and limited to patients who underwent dual-phase scanning. Third, it is possible that the results would differ with a larger series. For example, relatively few hemangiomas and hypervascular metastases were included in our study, and further work will be necessary to more fully examine their enhancement patterns. Fourth, we did not examine lesions in the portal venous phase because this was not the focus of the study. In practice, portal venous phase imaging may also contribute useful information. Finally, our thresholds for considering PPVs and specificity to be clinically useful are subjective and based on our own clinical experience.

Our early experience suggests that the peripheral puddles, complete ring, and abnormal internal vessels or variegated enhancement patterns in the arterial phase are associated with the diagnoses of hemangioma, metastasis, and HCC, respectively, with PPV of 82%–90% and specificity of 80%–99%. Thus, the appearance of hepatic lesions in the arterial phase of enhancement has potential use in the determination of specific diagnoses, and the classification scheme presented herein may be a useful tool for the interpretation of arterial phase CT studies.

	Footnotes

 
² Current address: Department of Radiology, Palo Alto Medical Foundation, Calif.

Abbreviations: HCC = hepatocellular carcinoma, FNH = focal nodular hyperplasia, PPV = positive predictive value

Author contributions: Guarantor of integrity of entire study, M.N.M.; study concepts and design, R.B.J., E.W.O., M.N.M., R.L.L.; definition of intellectual content, R.B.J., M.N.M., E.W.O.; literature research, M.N.M., E.W.O.; clinical studies, all authors; data acquisition, R.B.J., M.N.M., E.W.O., R.L.L.; data analysis, E.W.O., M.N.M., R.B.J.; manuscript preparation and editing, M.N.M., E.W.O., R.B.J.; manuscript review, all authors.

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Nino-Murcia, M. Articles by Jain, K. A. Search for Related Content PubMed PubMed Citation Articles by Nino-Murcia, M. Articles by Jain, K. A.