J Med Ultrasonics (2012) 39:61–68 DOI 10.1007/s10396-011-0339-2
ORIGINAL ARTICLE
Sonographic characterization of 271 hepatic hemangiomas with typical appearance on CT imaging Hiroaki Ito • Fumio Tsujimoto • Yasuo Nakajima • Gaku Igarashi • Takanori Okamura • Masaru Sakurai • Sachihiko Nobuoka • Takehito Otsubo
Received: 11 September 2011 / Accepted: 31 October 2011 / Published online: 12 January 2012 The Japan Society of Ultrasonics in Medicine 2012
Abstract Purpose Hepatic hemangioma is the most frequent benign solid tumor that requires differentiation from hepatic malignancy on ultrasonography. Useful ultrasound findings are therefore required for diagnosis. Subjects and methods The following factors were investigated for 271 masses diagnosed as hepatic hemangioma by contrast-enhanced computed tomography (CT) in 188 patients: hepatic subsegment location, shape, maximum diameter, internal echo level, hyperechoic rim, posterior echoes, marginal hypoechoic band (halo), lateral shadow, blood flow signal in the central portion of the mass, and underlying liver disease. Results Hepatic masses were classified by internal echo pattern as homogeneous hyperechoic (35.0%), homogeneous hypoechoic (22.9%), isoechoic (5.2%), mixed hyperechoic (22.1%), or mixed hypoechoic (14.8%)
masses. Twelve masses were isoechoic, and could be recognized by the hyperechoic rim. Posterior echo enhancement was present in 66 masses. There were no cases of posterior echo attenuation. A halo was present in six masses, with the underlying condition being fatty infiltrated liver in two masses; a hypoechoic region with a small amount of fat deposit was present around the mass, and this resembled a halo. This finding was termed a ‘‘pseudohalo.’’ There were no masses in which a lateral shadow was observed. In terms of blood flow signals in the central portion of the mass, pulsatile flow was present in only one mass. Conclusions Important ultrasonographic findings of hepatic hemangioma are characterized as the absence of lateral shadow (100%) and no attenuation of posterior echoes (100%), while the presence of a hyperechoic rim is useful for detecting isoechoic hemangioma. Keywords Ultrasonography Hepatic hemangioma Pseudohalo Hyperechoic rim CT
H. Ito (&) T. Otsubo Department of Gastroenterology and General Surgery, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa 216-8511, Japan e-mail:
[email protected] F. Tsujimoto G. Igarashi S. Nobuoka Department of Laboratory Medicine, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa 216-8511, Japan Y. Nakajima Department of Radiology, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa 216-8511, Japan T. Okamura M. Sakurai Department of Ultrasonography Center, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa 216-8511, Japan
Introduction Hepatic cavernous hemangioma (hemangioma) is the most common nonepithelial benign tumor and is frequently encountered on ultrasonograms. The incidence of hepatic hemangioma in the general population varies in published reports from 0.4% to 7.3% [1–3]. Hepatic hemangioma does not change in size over time, and treatment is not considered necessary [4, 5]. Nevertheless, in rare cases, hemangiomas located on the inferior surface of the liver may enlarge, causing subjective symptoms such as abdominal pressure, and are associated with a risk of rupture; Kasabach–Meritt syndrome may be present, and in such cases surgical treatment is indicated [4, 5]. Recent
123
62
improvements in diagnostic imaging technology have led to a rapid increase in the number of cases discovered by chance while still asymptomatic, and noninvasive ultrasonography (US) in particular is regarded as exceptionally useful for diagnosis of hemangioma [5, 6]. Gandolfi et al. [4] categorized hemangiomas in terms of internal echoes as hyperechoic, mixed echoic, and hypoechoic types, and they reported the frequency of each of these types among 158 masses in 128 patients with hemangioma to be 84.8% hyperechoic, 13.4% mixed echoic, and 1.8% hypoechoic. Soejima et al. [7] and Jeong et al. [8] classified internal echo patterns into four types (hyperechoic, mixed echoic, hypoechoic, and isoechoic) and argued that these are related to the size of the mass. Hemangioma is difficult to distinguish from malignant tumors, particularly hepatocellular carcinoma and metastatic liver cancer. In many cases, it is not possible to differentiate hemangiomas based on the internal echo patterns alone [7–12]. Itai et al. [11] reported one case that was difficult to distinguish from hepatocellular carcinoma, as findings similar to the linear hypoechoic band surrounding the mass, characteristic of hepatocellular carcinoma, are also present in hemangioma. In the present study, 271 masses in 188 patients with confirmed diagnosis of hepatic hemangioma on contrastenhanced computed tomography (CT) were categorized using a more detailed classification of ultrasonographic findings. This is the first description reporting whether the echo level in hepatic hemangioma is related to underlying liver disease or the shape of the mass.
Subjects This study was approved by the University Ethics Committee (no. 1729). A computer search of CT reports completed between January 2009 and March 2010 helped identify 1200 patients with reports containing the word ‘‘hemangioma.’’ A total of 271 masses, for which masses of the same size and shape and in the same location of the liver could also be identified on US, were studied.
J Med Ultrasonics (2012) 39:61–68
thickness of 0.5–3 mm and beam pitch of 0.282–1.5. Two radiologists interpreted all CT images and reported diagnosis of hepatic hemangioma. Another radiologist reviewed reports with CT images, and selected 1200 cases in which administration of contrast resulted in peripheral nodular enhancement in the early phase, followed by centripetal pattern or ‘‘filling in’’ during the late phase [13–16]. The ultrasound devices used were the Aplio XG, AplioX, and Xario (Toshiba Medical Systems, Tokyo, Japan), the EUB-8500 (Hitachi Medical Corporation, Tokyo, Japan), the HD11 and IU21 (Philips Healthcare, Tokyo, Japan), and the Acuson S-2000 (Mochida Siemens Medical Systems, Tokyo, Japan). Scanners were convextype probes of 3.5–3.75 MHz. All US examinations were performed by an ultrasonographic technician, within 1 year of CT examination between January 2008 and February 2010, and all scans were interpreted by a board-certified radiologist, a Fellow of the Japan Radiological Society and Japan Society of Ultrasonics in Medicine. A mass diagnosed as hepatic hemangioma on CT was judged to be the same lesion as a mass detected on US if it had the same location, shape, and size. Masses detected on CT that could not be detected on US were excluded. All patients were monitored for at least 2 years to confirm absence of any change in mass size or shape. Masses were investigated with regard to the following characteristics: 1. Hepatic subsegment location: categorized according to Couinaud’s hepatic subsegment classification [17]. 2. Shape: classified as circular, elliptical, or irregular. All masses with fine surface irregularities were classed as irregular. 3. Internal echo level and maximum diameter: internal echo level was classified into homogeneous hyperechoic (Fig. 1), homogeneous hypoechoic (Fig. 2), isoechoic (Fig. 3), mixed hyperechoic (Fig. 4), and mixed hypoechoic types (Fig. 5). Masses in which the
Methods The CT devices used were the Aquillion 64, Aquillion 4, Asteion 4, and Aquillion 16 (Toshiba Medical Systems, Tokyo, Japan). The contrast material was iodine 300 or 370 mg/ml, administered at 600 mgI/kg. Iodine 300 mg/ml as contrast material was administered at rate of 2.0–4.0 ml/s, with maximum dose of 150 ml; iodine 370 mg/ml as contrast agent was administered at rate of 1.7–3.3 ml/s, with maximum dose of 100 ml. Imaging was performed with slice
123
Fig. 1 Hyperechoic-type hemangioma: longitudinal US image of the liver showing homogeneous hyperechoic mass with hyperechoic rim (arrow)
J Med Ultrasonics (2012) 39:61–68
Fig. 2 Hypoechoic-type hemangioma: transverse US image of the liver showing homogeneous hypoechoic mass (arrow)
63
Fig. 5 Mixed hypoechoic-type hemangioma: transverse US image of the liver showing mixed hypoechoic mass (arrows). The hypoechoic area in the mass is broader than the hyperechoic area
4.
5.
6. 7. 8. 9. Fig. 3 Isoechoic-type hemangioma: transverse US image of the liver showing isoechoic mass with hyperechoic rim (arrow)
Hyperechoic rim: determined as a narrow, linear hyperechoic band around the margin of the mass (Figs. 1, 3). Isoechoic masses can be recognized by the presence of such a hyperechoic rim. Posterior echoes: classified as enhanced, intermediate, attenuated, or indeterminate. Indeterminate cases were those in which the mass was located on the inferior surface of the liver or touching the diaphragm. Marginal hypoechoic band (halo). Lateral shadow associated with the mass. Blood flow signal in the central portion of the mass: determined using color Doppler velocity mode. Underlying liver disease: patients with high echo levels of hepatic parenchyma and hepatorenal echo contrast were regarded as having fatty infiltrated liver, whereas those without these findings were considered not to have fatty liver. The non-fatty liver group included patients with chronic hepatitis or liver cirrhosis diagnosed clinically or on diagnostic imaging, as well as those with normal liver. The relationship between qualitative features was assessed using v2 test criterion with the statistical software package Statcel 3 in EXCEL.
Results
Fig. 4 Mixed hyperechoic-type hemangioma: longitudinal US image of the liver showing mixed hyperechoic mass (arrows). The hyperechoic area in the mass is broader than the hypoechoic area
internal hyperechoic region was C50% of the area were classified as mixed hyperechoic, while masses in which the internal hyperechoic region was \50% were classified as mixed hypoechoic.
Subjects were 94 men and 94 women; there were no sexbased differences. Ages ranged from 37 to 87 years with average of 60.7 ± 0.92 years. A single mass was present in 137 cases (72.9%), and multiple masses were present in 51 cases (27.1%). The number of masses in patients with multiple masses was 2–7 with average of 2.64 ± 0.15. The maximum diameter of the masses was 3–560 mm with average of 24.7 ± 2.9 mm. The following characteristics were found:
123
64
J Med Ultrasonics (2012) 39:61–68 Table 1 Relationship between underlying liver disease and internal echo pattern in 271 hemangiomas Internal echo pattern
Fatty liver (n = 50)
Non-fatty liver (n = 221)
Homogeneous hyperechoic (%)
11 (22.0)
84 (38.0)
Homogeneous hypoechoic (%)
25 (50.0)
37 (16.7)
Mixed hyperechoic (%)
7 (14.0)
53 (24.0)
Mixed hypoechoic (%)
7 (14.0)
33 (14.9)
Isoechoic (%)
0 (0)
14 (6.3)
5. Fig. 6 US detection numbers and rates of hepatic hemangioma by Couinaud’s liver subsegmentation (n = 271)
6. 1.
2. 3.
4.
Hepatic subsegment location: S1, 2 masses (0.7%); S2, 24 masses (8.9%); S3, 26 masses (9.6%); S4, 29 masses (10.7%); S5, 35 masses (12.9%); S6, 49 masses (18.1%); S7, 66 masses (24.4%); S8, 40 masses (14.8%) (Fig. 6). S7 was the most frequent location, followed by S6, S8, and S5. Shape: 67 masses (42.7%) were circular, 88 (32.5%) were elliptical, and 116 (42.8%) were irregular. Internal echo level and maximum diameter: 95 masses (35.1%) were homogeneous hyperechoic, 62 (22.9%) were homogeneous hypoechoic, 60 (22.1%) were mixed hyperechoic, 42 (15.5%) were mixed hypoechoic, and 12 (4.4%) were isoechoic. The proportion of homogeneous hyperechoic masses was highest for masses of maximum diameter \2 cm, of which 72 (26.6%) were homogeneous hyperechoic, 46 (17.0%) were homogeneous hypoechoic, 32 (11.8%) were mixed hyperechoic, 19 (7.0%) were mixed hypoechoic, and 9 (3.0%) were isoechoic. Among masses of diameter C2 and\5 cm, 21 (7.7%) were homogeneous hyperechoic, 15 (5.5%) were homogeneous hypoechoic, 20 (7.4%) were mixed hyperechoic, 11 (4.1%) were mixed hypoechoic, and 10 (3.7%) were isoechoic. Among masses of diameter C5 cm, 2 (1.0%) were homogeneous hyperechoic, 1 (0.3%) was homogeneous hypoechoic, 8 (3.0%) were mixed hyperechoic, 5 (1.8%) were mixed hypoechoic, and 0 (0.0%) were isoechoic. Among masses of diameter \2 cm, 104/178 (58.4%) were regarded as hyperechoic (including both homogeneous hyperechoic and mixed hyperechoic types). The wax and wane sign [18], in which the internal echo level changed over time, was observed in 2 masses. The chameleon sign [19], in which the internal echo changed due to postural changes, was observed in 1 mass. Hyperechoic rim: a hyperechoic rim was present in 176 masses (64.9%).
123
Underlying liver disease
7. 8.
9.
Posterior echo: this was enhanced in 66 masses (24.4%), intermediate in 50 (18.5%), attenuated in none, and indeterminate in 155 (57.2%). Marginal hyperechoic band (halo): there were 6 masses for which a halo was observed. Lateral shadow: there were no masses for which a lateral shadow was observed. Blood flow signal in the central portion of the mass: a pulsatile blood flow signal was observed in the central portion of 1 mass, with maximum velocity (Vmax) of 64.2 cm/s and resistance index (RI) of 0.73. Underlying liver disease: 129 patients with 193 masses had normal livers, 37 patients with 50 masses had fatty infiltrated liver, 16 patients with 22 masses had chronic hepatitis, and 6 patients with 6 masses had liver cirrhosis. Internal echo levels of the 50 hemangiomas in the fatty infiltrated liver group were homogeneous hyperechoic in 11 masses (22.0%), homogeneous hypoechoic in 25 (50.0%), mixed hyperechoic in 7 (14.0%), and mixed hypoechoic in 7 (14.0%), with no isoechoic-type masses. A hyperechoic rim was present in 26 masses (52.0%). Among the 221 masses in the non-fatty liver group, 84 (38.0%) were homogeneous hyperechoic, 37 (16.7%) were homogeneous hypoechoic, 53 (24.0%) were mixed hyperechoic, 33 (14.9%) were mixed hypoechoic, and 14 (6.3%) were isoechoic. A hyperechoic rim was present in 150 masses (67.9%). Homogeneous hypoechoic-type masses were significantly more frequent among the fatty infiltrated liver group when compared with the non-fatty liver group (P \ 0.001) (Table 1).
Discussion In histopathological images, hemangiomas exhibit a sponge-like appearance on the cut surface due to narrow connective tissue interstitium, and because these lesions are not hard tumors. The mass is in contact with the hepatic parenchyma, and no covering is formed on its border, but it
J Med Ultrasonics (2012) 39:61–68
may enclose atrophied liver cells or bile ducts at its margins. The fibrous septa separating it from the vascular lumen are normally thin, but large areas of scarring may be present. Hemangiomas may cause degenerative changes, and although their mechanism of formation is unknown, fresh or organized blood clots are frequently present in the vascular lumen. As blood flow within the mass is slow, it is believed that small blood clots are repeatedly formed and dissolved. With the passage of time, fresh and old blood clots, scarring, and even calcification are observed [20]. In the USA and Europe, hemangioma is regarded as more frequent among women [1, 2]. In our cases, however, no such difference was present. Most hepatic hemangiomas occur singly, with multiple occurrence in approximately 10% of cases [21]. In the present study, 72.9% occurred singly and 27.1% occurred as multiple masses, representing a marked increase in the proportion of multiple occurrence, but this may have been due to the improved diagnostic accuracy with multislice CT scanners having slice thickness of 0.5–3 mm and ultrasound diagnostic devices with harmonic imaging and digital scanners, thereby allowing previously undetectable lesions to be depicted. Among the 50 hemangiomas in the fatty infiltrated liver group, the internal echoes were homogeneous hypoechoic type in 25/50 (50.0%), but among the 221 hemangiomas in the non-fatty liver group, homogeneous hypoechoic type was seen in 37 (16.7%). The homogeneous hypoechoic type was clearly more common in the fatty infiltrated liver group than in the non-fatty liver group, being approximately three times more frequent. One possible reason that hemangiomas may have appeared hypoechoic in the fatty infiltrated liver group is that ultrasound beams were scattered by fatcontaining liver tissue around the hemangioma, making the hemangioma itself appear relatively hypoechoic [22]. In terms of location of the mass by hepatic subsegment, S1 was the least common with only 2 masses, while S7 was most frequent with 66 masses. Hemangioma is regarded as a congenital hamartoma [23] that may appear anywhere within the liver. According to Eddie et al. [24], the ratio of the total volume of S5, S6, S7, and S8 in the right hepatic lobe (997 ± 279 cm3) to that of S2, S3, and S4 in the left hepatic lobe (493 ± 127 cm3) is approximately 2:1. The number of hemangiomas was 190 in the right hepatic lobe and 79 in the left, a right-to-left ratio of 2.4:1, meaning that the ratio of the volume of the right and left hepatic lobes was almost the same as that of the number of hemangiomas in each side. Gandolfi et al. [4] reported that 98 of 99 (99%) small masses of diameter \2 cm were hyperechoic, with 1 of mixed echo type. In the present study, the results were very different, with 104 of 178 (58.4%) masses of diameter \2 cm being hyperechoic. Gandolfi et al. diagnosed hemangioma on US alone, detecting only masses
65
exhibiting hyperechogenicity and determining their nature as hemangioma on the basis of 7-year follow-up. Isoechoic and hypoechoic masses were therefore not included among the hemangiomas they studied, giving rise to this difference in results. In terms of the relationship between maximum diameter and internal echo pattern, when the mixed hyperechoic and mixed hypoechoic patterns are jointly regarded as a mixed echo type, this pattern was seen in 51 of 178 masses (28.7%) with diameter\2 cm and in 44 of 93 (47.3%) with diameter C2.1 cm, with a higher proportion of the mixed echo type among masses with larger diameter. The fact that internal echoes become inhomogeneous as the mass increases in size is due to the histopathological presence of blood clots, scarring, and even calcification [20]. Changes in internal echo pattern were recorded among the masses in this study, with the wax and wane sign [18] observed in 2 and the chameleon sign [19] in 1. The internal echo pattern of hemangiomas may change because of differences in ultrasound scattering due to changes in the amount of blood pooling as a result of expansion and contraction of the blood sinuses, causing differences in the echo level [18, 19]. The linear hyperechoic area, known as the ‘‘hyperechoic rim,’’ can be regarded as a border echo resulting from the difference in acoustic impedance between the hepatic parenchyma and the mass [25–27]. Masses possessing a hyperechoic rim accounted for 53/62 (85.5%) of the homogeneous hypoechoic type, 38/40 (95%) of the mixed hypoechoic type, 12/12 (100%) of the isoechoic type, 34/95 (35.8%) of the homogeneous hyperechoic type, and 38/60 (63.3%) of the mixed hyperechoic type, with homogeneous isoechoic hemangiomas in particular being recognizable owing to the presence of this hyperechoic rim. A hyperechoic rim was present in 176/271 (64.9%) of all hemangiomas. Yajima et al. [27] reported that, in some cases, it was impossible to detect masses that later became detectable during ultrasonographic follow-up study. This phenomenon suggests that masses may temporarily become isoechoic, making them impossible to detect. Even if a hyperechoic rim is present, isoechoic hemangiomas may not be detected if this hyperechoic rim itself is not recognized in real time. Even in such cases, however, the hemangioma may be detected if the examiner is able to recognize the hyperechoic rim. Posterior echo enhancement was present in 24.4% (66/ 271) of all masses due to two possible causes: multiple reflection by multiple sinuses or blood flow pooling in the hemangioma itself, or high ultrasound transmission [23]. Posterior echo attenuation was not present in any mass. Therefore, if posterior echo attenuation is present, there is an extremely high possibility that the mass is not a hemangioma.
123
66
Fig. 7 a-1 Right intercostal US: echogenicity of liver parenchyma is markedly hyperechoic, suggestive of hepatic steatosis. Hypoechoic mass with hyperechoic rim (arrows) is surrounded by hypoechoic area. a-2 Right subcostal US: hypoechoic mass with hyperechoic rim (arrows) is noted, which is surrounded by ring-shaped hypoechoic area resembling halo, termed ‘‘pseudohalo.’’ a-3 Right intercostal color Doppler US: hypervascularity is noted in hypoechoic area instead of mass lesion. a-4 Right subcostal color Doppler US:
123
J Med Ultrasonics (2012) 39:61–68
hypervascularity is noted in ring-shaped hypoechoic area, termed ‘‘pseudohalo.’’ b-1 Plain CT. A triangle-shaped hyperdense area is noted in the peripheral portion of the right hepatic lobe. Liver parenchyma is diffusely low in density, representing fatty infiltrated liver. b-2 Contrast-enhanced CT. In the parenchymal phase, a wellenhanced hemangioma (arrow) is noted, smaller than the same area of the known triangle-shaped hyperdense parenchyma (broken line) on plain CT
J Med Ultrasonics (2012) 39:61–68
In the infiltrated fatty liver group, for 2 masses in 2 patients, peritumoral hypoechoic regions were detected representing fat-spared area, which had a similar appearance to a halo. The fat-spared zone that we termed ‘‘pseudohalo’’ may have been the result of peritumoral arterioportal shunting in fatty infiltrated liver [22, 25, 26] (Fig. 7a-1, 2, 3, 4). In addition, on plain CT, only the hepatic parenchyma surrounding the hemangioma was hyperdense, confirming that there was little fatty deposit in this area (Fig. 7b-1, 2). In the fatty infiltrated liver group, depending on the ultrasound beam direction, a bull’s-eye pattern [28] or a broad halo was visible, appearing like a typical liver metastasis, so recognition of the pseudohalo is important. Lateral shadow was not present in any hemangiomas. Lateral shadow is an acoustic shadow that occurs when a shadow is produced below a smooth-surfaced mass on both sides as a result of refraction and complete reflection of ultrasound waves [29]. The fact that lateral shadow is not present in hemangioma suggests that small marginal irregularities are present. Identification of these irregularities on the margins of hemangiomas and confirmation of the absence of lateral shadow are important findings in the diagnosis of hemangiomas. Konno et al. [30] reported that the proportion of hepatic hemangiomas exhibiting lateral shadow was 9.5%. However, in the present study, a lateral shadow was not observed in any masses. This may have been because compound scanning was performed by recent diagnostic ultrasound devices in the processing of ultrasound images, making it more difficult for lateral shadows to occur. No blood flow signal in the central portion of the mass was detected in 270 of 271 hemangiomas (99.6%) investigated in this study, and pulsatile flow was detected in only 1. Hepatic hemangiomas themselves are composed of numerous sinuses, and because blood flow within these sinuses is extremely sluggish, it is extremely rare for blood flow to be detected in the central portion of the mass by the Doppler method [12, 30, 31]. Numata et al. [31] reported that pulsatile flow was present in 13 of 28 hemangiomas, but blood flow was detected in all peripheral portions of the masses. It is possible that most blood flow signals were detected in the peripheral portion of the masses with or without detection of blood flow artifact in normal hepatic parenchyma owing to the slice thickness of the ultrasound beam. According to Doo et al. [32], a blood flow signal in the central portion of the masses was detectable in 3 of 400 cases (0.75%) scanned by gadolinium-enhanced magnetic resonance imaging (MRI). The absence of a blood flow signal within the mass is therefore one of the most important findings for the diagnosis of hepatic hemangioma [31]. However, hyperechoic early hepatocellular carcinoma without a blood flow signal in the central portion may be considered as a differential diagnosis [7–12].
67
Conclusions • •
•
Confirmation of a hyperechoic rim enabled detection of hemangiomas with isoechoic internal echoes. In patients with underlying fatty infiltrated liver for whom hepatic parenchyma is hyperechoic, the area surrounding the hemangioma appears hypoechoic and resembles a halo, an appearance termed a ‘‘pseudohalo.’’ Posterior echo attenuation and lateral shadow were not present in any cases of hepatic hemangioma, representing important ultrasonographic findings characterizing hepatic hemangioma.
References 1. David ML, William DM, Sharlene AT, et al. Follow-up of patients at low risk for hepatic malignancy with a characteristic hemangioma at US. Radiology. 2000;214:167–72. 2. Ng WWC, Cheung YS, Lee KF, et al. Is regular follow-up scan for giant liver haemangioma necessary? Hong Kong Med J. 2007;13:353–8. 3. Itai Y, Ohtomo K, Furui S, et al. Noninvasive diagnosis of small cavernous hemangioma of the liver: advantage of MRI. AJR. 1985;145:1195–9. 4. Gandolfi L, Leo P, Solmi L, et al. Natural history of hepatic haemangiomas: clinical and ultrasound study. Gut. 1991;32:677–80. 5. Kobayashi T, Kawano M, Tomita Y, et al. Follow-up study of hepatic hemangiomas. Nippon Shokakibyo Gakkai Zasshi. 1995;92:41–6. 6. Kudara N, Chiba T, Andoh T, et al. A case of hepatic hemangioma with pedunculated extrahepatic growth simulating submucosal tumor of the stomach. Nippon Shokakibyo Gakkai Zasshi. 2004;101:293–9. 7. Soejima S, Shigei F, Ichihara A, et al. Ultrasonography of hepatic cavernous hemangioma. Kitasato Med. 1987;17:107–19. 8. Jeong SY, Myeong JK, Kim KW, et al. Hepatic cavernous hemangioma: sonographic patterns and speed of contrast enhancement on multiphase dynamic MR imaging. AJR;171:1021–5. 9. The guideline of diagnostic imaging of hepatichemangioma. JRS/ JCS Guideline making committee 2007; p. 1–43. 10. Karhunen PJ. Benign hepatic tumours and tumour like conditions in men. J Clin Pathol. 1986;39:183–6. 11. Itai Y, Ohtomo K, Araki T, et al. Computed tomography and sonography of cavernous hemangioma of the liver. AJR. 1983;141:315–20. 12. Bree RL, Scwab RE, Neiman HL. Solitary echogenic spot in the liver: is it diagnostic of a hemangioma? AJR. 1983;140:41–5. 13. Pa¨iva¨nsalo M, La¨hde S, Jalovaara P. Computed tomography of hepatic haemangiomas: a chance for a definite diagnosis. Bildgebung. 1991;58:29–32. 14. Choi BI, Han MC, Park JH, et al. Giant cavernous hemangioma of the liver: CT and MR imaging in 10 cases. AJR. 1989;152:1221–6. 15. Choi BI, Han JK, Cho JM, et al. Characterization of focal hepatic tumors: values of two-phase scanning with spiral computed tomography. Cancer. 1995;76:2434–42. 16. Hanafusa K, Ohashi I, Himeno Y, et al. Hepatic hemangioma: findings with two-phase CT. Radiology. 1995;196:465–9.
123
68 17. Couinaud C. Distribution De L’artere Hepatique dans Lefole. Acte anat. 1954;22:4–81. 18. Tsujimoto F, Abe T, Murakami Y, et al. Temporal changes of internal echoes in hepatic hemangiomas. J Jpn Radiol Soc. 1989;49:574–82. 19. Otake K, Asai H, Ikeoka N, et al. The changing of the ultrasonographic image of hepatichemangioma (‘‘Chameleon’’ sign) by changing position. Jpn J Med Imaging. 1991;10:120–5. 20. Goodman ZD. Benign tumors of the liver. Neoplasms of the liver. Heidelberg: Springer; 1987. p. 105–25. 21. Kasai Y. Hepatic hemangioma. J Jpn Surg Assoc. 1979;34: 897–901. 22. Kim KW, Kim MJ, Lee SS, et al. Sparing of fatty infiltration around focal hepatic lesions in patients with hepatic steatosis: sonographic appearance with ct and mri correlation. AJR. 2008;190:1018–27. 23. Nichols III FC, van Heerden JA, Weiland LH. Benign liver tumors. Surg Clin North Am. 1989;69:297–314. 24. Abdalla EK, Denys A, Chevalier P, et al. Total and segmental liver volume variations: implications for liver surgery. Surgery. 2004;135:404–10. 25. Grossholz M, Terrier F, Rubbia L, et al. Focal sparing in the fatty liver as a sign of an adjacent space-occupying lesion. AJR. 1998;171:1391–5.
123
J Med Ultrasonics (2012) 39:61–68 26. Chen RC, Li CS, Lii JM, et al. Peritumoral fat-spared area is well correlated with the presence of temporal peritumoral enhancement in hepatic hemangioma in fatty liver. J Magn Reson Imaging. 2005;22:86–91. 27. Yajima Y, Onodera H, Oikawa M, et al. A case of hepatic hemangioma with the shift of internal echo level from echolucent to echogenic type. Jpn J Clin Radiol. 1983;28:891–3. 28. Minami Y, Kudo M. Hepatic malignancies: correlation between sonographic findings and pathological features. World J Radiol. 2010;28:249–56. 29. Steel R, Poepping TL, Thompson RS, et al. Origins of the edge shadowing artifact in medical ultrasound imaging. Ultrasound Med Biol. 2004;30:1153–62. 30. Konno K, Ishida H, Sato M, et al. Liver tumors in fatty liver: difficulty in ultrasonographic interpretation. Abdom Imaging. 2001;26:487–91. 31. Numata K, Tanaka K, Mitsui K, et al. Flow characteristics of hepatic tumors at color Doppler sonography: correlation with arteriographic findings. AJR. 1993;160:515–21. 32. Doo KW, Lee CH, Choi JW, et al. ‘‘Pseudo washout’’ sign in highflow hepatic hemangioma on gadoxetic acid contrast-enhanced mri mimicking hypervascular tumor. AJR. 2009;193:490–6.
