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Gastrointestinal Imaging |
1 From the Department of Diagnostic Radiology and the Research Institute of Radiological Science, Yonsei University College of Medicine, YongDong Severance Hospital, 146-92, Dokok-Dong, Kangnam-Ku, Seoul 135-270, South Korea. Received April 27, 1999; revision requested June 14; final revision received January 10, 2000; accepted January 27. Address correspondence to J.S.Y. (e-mail: yjsrad97@yumc.yonsei.ac.kr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Dynamic MR images obtained in 94 patients with 167 hemangiomas were retrospectively reviewed for peritumoral enhancement. Tumor volume was estimated by using the longest dimension on nonenhanced images. Speed of intratumoral contrast material enhancement was determined with early nonequilibrium phase images and was categorized as rapid (>75% of tumor volume), intermediate (25%–75% of tumor volume), or slow (<25% of tumor volume).
RESULTS: Thirty-two of the 167 hemangiomas (19%) had temporal peritumoral enhancement, which was more common in hemangiomas with rapid enhancement (20 of 49 [41%]) than in those with intermediate (12 of 62 [19%]) and slow (0 of 56 [0%]) enhancement (P < .001). The mean diameter of the hemangiomas with peritumoral enhancement was not significantly different from that of hemangiomas without peritumoral enhancement (P > .05). Hemangiomas with rapid enhancement (mean diameter, 16 mm ± 8), however, were significantly smaller than those with intermediate enhancement (mean diameter, 33 mm ± 34) (P < .001).
CONCLUSION: Temporal peritumoral enhancement on dynamic MR images of hepatic hemangiomas correlates well with the speed of intratumoral contrast material enhancement and was most commonly encountered in rapidly enhancing small lesions. There was no statistically significant relationship, however, between peritumoral enhancement and tumor volume.
Index terms: Liver, MR, 761.121415, 761.121416 • Liver neoplasms, MR, 761.121415, 761.121416, 761.12143 • Magnetic resonance (MR), contrast enhancement, 761.12143 • Shunt, arterioportal, 761.453
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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20 mm in diameter) show homogeneous enhancement on early phase images (1,7,11,12). Previously, these small hemangiomas were considered to be atypical and rare (13,14). Rapidly enhancing small hemangiomas, however, are often encountered in daily practice. In addition, we have found a distinctive feature in hepatic hemangiomas during multiphase dynamic contrast-enhanced MR imaging: temporal enhancement in the hepatic parenchyma around the hemangioma. This feature is considered to be identical to an imaging finding previously described at two-phase dynamic incremental CT: early parenchymal enhancement in the area adjacent to the hemangioma (1). To our knowledge, however, this feature has not been carefully evaluated with dynamic MR imaging. The purpose of this retrospective study was to determine whether the presence of temporal parenchymal enhancement around hemangiomas correlates with the rapidity of intratumoral contrast material enhancement, tumor volume, or both during multiphase dynamic MR imaging.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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-fetoprotein level. Patients were also excluded if MR imaging was the only imaging examination performed. Thus, 94 patients (51 men and 43 women aged 33–90 years; mean age, 47.5 years) with 167 hepatic cavernous hemangiomas were included in this study. Hemangioma was diagnosed on the basis of a combination of typical findings at MR imaging, ultrasonography (US), labeled red blood cell scintigraphy, and hepatic angiography or the absence of an increase in tumor size for at least 12 months. At US, a hyperechoic, well-delimited lesion with faint acoustic enhancement was considered to be a hemangioma. At angiography, a lesion was considered to be a hemangioma if contrast material pooled within the lesion to produce a characteristic "cotton wool" appearance and if the contrast material was retained well beyond the venous phase. At labeled red blood cell scintigraphy, a defect seen during the early phases that showed prolonged and persistent "filling in" on delayed scans was considered to be a hemangioma.
At MR imaging, a lesion was considered to be a hemangioma if it was well demarcated and notably hyperintense on heavily T2-weighted images and if it had the following patterns of enhancement on contrast-enhanced dynamic images: (a) peripheral discontinuous nodular enhancement on arterial phase images with progressive and centripetal enhancement; and (b) immediate homogeneous contrast material enhancement that persisted for at least 5 minutes after the administration of contrast material.
MR imaging was performed in all 94 patients; hepatic US, in 93; labeled red blood cell scintigraphy, in 44; and angiography, in 10. Eighty-nine patients underwent follow-up examinations. All patients had typical findings of hemangioma on images obtained with at least two imaging modalities, and follow-up examinations with one or more imaging modalities were used to verify the benignity of the lesion. One follow-up MR examination was performed in 30 patients, two follow-up MR examinations were performed in 14, and three follow-up MR examinations were performed in five. One follow-up US examination was performed in 33 patients, two follow-up US examinations were performed in 56, and three follow-up US examinations were performed in four. In patients with rapidly enhancing lesions at dynamic MR imaging, US was not considered to be diagnostic because rapidly enhancing hemangiomas tend to be hypoechoic (15). Instead, labeled red blood cell scintigraphy or hepatic angiography was performed to establish the diagnosis of rapidly enhancing lesions. In addition, all rapidly enhancing lesions had without exception one or more follow-up examinations performed at 3–6-month intervals for at least 12 months since we excluded the cases of rapidly enhancing lesions without follow-up from the study regardless of typical findings of hemangioma on images obtained with at least two imaging modalities.
MR Imaging
MR imaging was performed with a 1.5-T superconducting system (Magnetom Vision; Siemens, Erlangen, Germany) with a phased-array multicoil. All MR images were obtained in the transverse plane during breath-holding. Nonenhanced T1-weighted images were obtained with a multisection fast low-angle shot (FLASH) sequence with and without fat suppression (repetition time, 113–130 msec; echo time, 4.1 msec [113–130/4.1]; flip angle, 80°), and T2-weighted images were obtained with a multishot turbo spin-echo sequence with and without fat suppression (3,540–4,000/138; echo train length, 29). Then, T1-weighted fat-suppressed dynamic FLASH images were obtained 10 seconds (first phase), 35 seconds (second phase), 60 seconds (third phase), and 300 seconds (delayed phase) after the start of a manual injection of a bolus of 0.1 mmol of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany) per kilogram of body weight into the antecubital vein followed by a 10-mL flush with normal saline.
For all pulse sequences, automated shimming was performed for each examination to maximize magnetic field homogeneity. The matrix size was 117–140 x 256; the field of view ranged from 32 to 40 cm, depending on patient size. Flow compensation was used. A total of 12–15 sections were obtained with an 8–10-mm section thickness and a 2-mm intersection gap. In all patients, the liver was imaged with a single acquisition during one breath hold. The acquisition time was 16–19 seconds.
Image Analysis
Temporal enhancement in the hepatic parenchyma around the hemangioma was defined as a contrast-enhanced area adjacent to the tumor, with or without early opacification of vascular structures, that was displayed during the early phase of dynamic MR imaging and disappeared in the delayed phase. The static nonenhanced T1- and T2-weighted images obtained with and without fat suppression were meticulously compared with the dynamic contrast-enhanced images to more clearly define the lesion boundaries and to detect the regions of peritumoral enhancement.
The speed of intratumoral contrast material enhancement was determined with the early nonequilibrium phase images. The early nonequilibrium phase was defined as the earliest phase that showed contrast material enhancement of the hepatic vein. The enhancement speed of all lesions was categorized as follows: rapid, in which more than 75% of the tumor volume enhanced; intermediate, in which approximately 25%–75% of the tumor volume enhanced; and slow, in which less than 25% of the tumor volume enhanced. Lesion diameter was defined as the greatest dimension on the transverse T2-weighted image in which the lesion appeared the largest.
The frequency of temporal enhancement around the hemangioma, the enhancement speed, the size of each hemangioma, and the pattern of temporarily enhancing foci around hemangiomas during dynamic MR imaging were measured and recorded after meticulous review by the authors in conference. Disagreements between the reviewers were resolved by consensus. The prevalence of temporal parenchymal enhancement was assessed in each type of hemangioma according to the enhancement speed. The analysis was directed to the difference in the prevalences of temporal peritumoral parenchymal enhancement according to the rapidity of intratumoral contrast material enhancement.
Statistical analysis was performed by using the 
2 test and the Cochran-Armitage trend test, with P values less than .05 considered to indicate a statistically significant difference. The mean size differences among lesions with slow, intermediate, and rapid enhancement were analyzed, and statistical significance was determined by using the one-way analysis of variance test for multiple comparisons. In addition, differences in mean size between hemangiomas with and hemangiomas without peritumoral enhancement were analyzed by means of the Student t test, with P values less than .05 considered to indicate a statistically significant difference. The difference in the pattern of peritumoral enhancement according to lesion size and enhancement speed was also evaluated (but was not statistically evaluated). In lesions with peritumoral enhancement, we evaluated whether lesion size was related to enhancement speed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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20 mm) with peritumoral enhancement, the subcapsular wedge enhancement pattern was most common, occurring in 10 of the 14 hemangiomas (71%). All 14 of these small lesions with peritumoral enhancement were unexceptionally rapid-type hemangiomas (Table 3, Fig 4). In the 18 large lesions (diameter, >20 mm) with peritumoral enhancement, the prevalence of segmental and/or lobar enhancement was 39% (seven of 18 lesions) (Table 3). In rapidly enhancing hemangiomas with peritumoral enhancement, subcapsular wedge enhancement was the most common pattern, occurring in 14 of 20 lesions [70%]). Hemangiomas with intermediate enhancement accompanied by peritumoral enhancement showed subcapsular wedge (five of 12 lesions [42%]) (Fig 5) or segmental and/or lobar (five of 12 lesions [42%]) enhancement patterns with the same frequency (Fig 3d, Table 3); all of these lesions were larger than 20 mm.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In our study, temporal parenchymal enhancement adjacent to hemangiomas at dynamic MR imaging was most frequently associated with rapidly enhancing small lesions. Therefore, it could be presumed that a rapidly enhancing small hemangioma has hyperdynamic status with large arterial inflow, rapid tumoral enhancement, and, consequently, large and rapid outflow, which seems to result in early opacification of the draining vein and peritumoral enhancement. The hyperdynamic status of the rapidly enhancing small hemangioma can be differentiated from a "true" transvasal arterioportal shunt associated with malignant lesions and could result from portal vein invasion and arterioportal flow through the vasa vasorum, with the arterial inflow into the tumor (the blood flow supplying the tumor) often bypassing the intratumoral vasculature.
Although peritumoral enhancement was most frequently encountered in small hemangiomas with rapid enhancement, the mean size of hemangiomas with temporal peritumoral enhancement was larger than that of lesions without any peritumoral enhancement. This can be explained by the fact that most large hemangiomas with intermediate enhancement were included in the group with peritumoral enhancement and that the slowly enhancing hemangiomas, which were almost without exception small or medium, were included in the group without peritumoral enhancement. The inclusion of large hemangiomas with intermediate enhancement in the group with peritumoral enhancement resulted in an increase in the mean lesion size in that group. Conversely, inclusion of the small hemangiomas with slow enhancement in the group without peritumoral enhancement resulted in a decrease in the mean lesion size in that group. Consequently, among all lesions with peritumoral enhancement, small hemangiomas with rapid enhancement were most frequently encountered. If only the hemangiomas with intermediate enhancement are considered, however, the larger hemangiomas were more frequently associated with peritumoral enhancement.
In addition to the fact that the size of hemangiomas with peritumoral enhancement differed according to the speed of intratumoral enhancement, the differences in the pattern of peritumoral enhancement could also be attributable to differences in the mechanism that causes peritumoral enhancement. The subcapsular wedge enhancement pattern was frequently associated with rapidly enhancing small lesions, whereas the segmental and/or lobar enhancement pattern was almost always associated with large hemangiomas with intermediate enhancement.
In contrast with the hyperdynamic status for rapid enhancement, compromised portal vein branches from the mass effect of larger hemangiomas could be associated with peritumoral enhancement by means of compensatory arterial inflow, with segmental and/or lobar distribution. When this is the case, there should be no early opacification of portal vein branches as draining vasculature. Consequently, it is predictable that the larger the lesion, the more prevalent the segmental and/or lobar enhancement pattern. Similarly, it is possible that subcapsular wedge enhancement without early opacification of the draining vein results from a compromise of the peripheral small branch of the portal vein.
The reason why peritumoral enhancement was not associated with a slowly enhancing hemangioma could be explained in terms of tumoral hypovascularity. In contrast with the hyperdynamic state of rapidly enhancing hemangiomas, which have a large amount of inflow and outflow, slowly enhancing hemangiomas without peritumoral enhancement may be in a hypodynamic state, with a lack of inflow and outflow. Although hemangiomas with intermediate enhancement may have tumoral inflow as large and rapid as that of hemangiomas with rapid enhancement, it may take more time to completely fill the intratumoral vascular spaces because these hemangiomas are significantly larger than those with rapid enhancement.
Consequently, regardless of the amount of tumoral inflow, the outflow of contrast-enhanced blood through a tumor will be delayed owing to the large tumor volume, and the peritumoral enhancement produced by transtumoral arterioportal communication could be delayed and not seen during the arterial phase. In addition, this enhancement may not be discernible on the portal venous phase images owing to the masking effect caused by the increased signal intensity of background liver. Thus, the reason this distinctive enhancement was most prevalent in rapidly enhancing small hemangiomas is that hemangiomas with rapid enhancement could have a relatively high inflow and fast intratumoral spread of contrast material with respect to the tumor volume.
In any case, the presence of temporal parenchymal enhancement around hemangiomas is enough to attract attention to the various possibilities of local hemodynamic alteration by hemangiomas. The temporal and contrast resolution with MR imaging is superior to that with CT. CT is limited by diminished contrast resolution and a relatively long contrast material injection period and imaging time, which makes detection of small lesions and optimal enhancement difficult. Therefore, we believe that MR imaging is superior to CT in the evaluation of the hemodynamics related to hemangiomas because the distinctive peritumoral enhancement was most commonly associated with rapidly enhancing small lesions. In contrast with our presumption that the peritumoral enhancement around a hemangioma will be more frequently detected at MR imaging than at CT scanning, however, the peritumoral enhancement related to hemangiomas was more infrequent at MR imaging (32 of 167 hemangiomas [19%]) than has been reported at CT (12 of 51 hemangiomas [24%]) (1).
Moreover, we used four-phase dynamic MR imaging, which is a more carefully subdivided protocol, as a dynamic sequence. It is probable that the comparison of our MR imaging results and the CT results by Hanafusa et al (1) was not controlled and that there was an inherent limitation in the patient selection. In addition to the small number of hemangiomas and patients in the previous study on CT (1), each patient (in both the previous study and our study) also represented a select population.
The limitation of our study is that the cause of temporal peritumoral enhancement around hemangiomas displayed at dynamic MR imaging was not histopathologically proved, mainly owing to the benignity of the underlying condition. In fact, it is generally accepted that typical findings at two or more imaging examinations are sufficient for diagnosing hemangioma. Hemangiomas with peritumoral enhancement, however, could create confusion when trying to differentiate them from malignant lesions, even though they had characteristic findings of hemangioma at two or more imaging examinations. Regardless of typical findings of hemangioma with two or more imaging modalities, in cases with peritumoral enhancement or arterioportal shunt, it was difficult to make a confident diagnosis of hemangioma because of the previous understanding that the peritumoral enhancement due to arterioportal shunt was rare in benign lesions. Therefore, if one is familiar with this distinctive feature of hemangioma, then further examinations to verify the diagnosis of hemangioma could be unnecessary.
In summary, temporal parenchymal enhancement adjacent to hemangiomas is not infrequently encountered during dynamic MR imaging, and this distinctive feature is mainly seen in rapidly enhancing small lesions. Therefore, the knowledge that temporal parenchymal enhancement around hemangiomas reflects only local hemodynamic alteration related to the hemodynamic status of hemangiomas could obviate further examinations when making a confident diagnosis of hemangioma.
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, J.S.Y.; study concepts, J.S.Y.; study design, M.G.J.; definition of intellectual content, J.S.Y.; literature research, J.S.Y.; clinical studies, M.G.J.; data acquisition and analysis, M.G.J.; statistical analysis, M.G.J.; manuscript preparation, M.G.J.; manuscript editing, J.S.Y.; manuscript review, K.W.K.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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