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AJR 2005; 184:S82-S85
© American Roentgen Ray Society


Case Report

Fluid-Fluid Levels in Cavernous Hemangiomas of the Liver: Baffled?

Sangeet Ghai, Marcus Dill-Macky, Stephanie Wilson and Masoom Haider

Division of Abdominal Imaging, University Health Network, Mount Sinai Hospital, University of Toronto, Princess Margaret Hospital 3-923, 610 University Ave., Toronto, Ontario, Canada, M5G 2M9.

Received March 14, 2004; accepted after revision June 1, 2004.

 
Address correspondence to M. Dill-Macky (Marcus.Dill-Macky{at}uhn.on.ca).


Introduction
Top
Introduction
Case Report
Discussion
References
 
Cavernous hemangioma is the most common benign tumor of the liver. The imaging appearances and characteristic enhancement patterns identifying these lesions are well described on sonography, CT, and MRI. The presence of a fluid-fluid level within a hemangioma is an unusual variant that has been rarely described [1-3]. Extremely slow flow has been postulated as the cause of this phenomenon. We present a case of fluid-fluid levels in multiple liver hemangiomas and offer an explanation for their appearance, with an analogy observed in the penis on MRI.


Case Report
Top
Introduction
Case Report
Discussion
References
 
A 34-year-old woman with vague abdominal pain was discovered to have multiple liver lesions on sonography and was referred to our institution for further characterization. A multiphasic MDCT was performed. Unenhanced scans revealed multiple (~ 50) well-defined, low-density lesions compared with the surrounding liver, ranging in diameter from 0.6 to 3 cm. Sixteen of the lesions contained a single fluid-fluid level. Arterial phase images depicted subtle peripheral enhancement in a minority (< 5) of lesions, none of which contained a fluid-fluid level. Portal phase imaging depicted progressive peripheral nodular enhancement typical of hemangiomas in most of the lesions (30 of 50). Enhancement in those with fluid levels was of a peripheral nodular type; however, the progression of enhancement was relatively delayed (Figs. 1A, 1B and 1C). Perflutren liquid microsphere-enhanced (Definity, Bristol-Myers Squibb) sonography with pulse inversion (DE-PII) and a multiphasic gadolinium-enhanced MRI were also performed to increase diagnostic confidence.



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Fig. 1A. 34-year-old woman with vague abdominal pain. Multiphase axial MDCT images were obtained at level of right adrenal gland. Precontrast image depicts multiple lesions with fluid-fluid levels (arrows).

 


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Fig. 1B. 34-year-old woman with vague abdominal pain. Multiphase axial MDCT images were obtained at level of right adrenal gland. Arterial phase image detects subtle peripheral nodular enhancement in some lesions (arrows).

 


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Fig. 1C. 34-year-old woman with vague abdominal pain. Multiphase axial MDCT images were obtained at level of right adrenal gland. Centripetal progression is identified on portal phase image typical of hemangiomas (arrows).

 

Sonography showed multifocal liver lesions that could be grouped into three distinct populations. Most had the typical homogeneous hyperechoic appearance of a hemangioma. Others had an atypical pattern, consisting of an isoechoic or hypoechoic lesion compared with the liver, with an echogenic border. The third group revealed a distinct fluid-fluid level that correlated with some, although not all, of the lesion with fluid-fluid levels on CT (Fig. 2). Sonography did not identify fluid-fluid levels in these lesions after decubitus positioning of the patient for 5 min. DE-PII revealed progressive peripheral nodular enhancement diagnostic of hemangiomas in all lesions on imaging delayed up to 7 min (Fig. 3).



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Fig. 2. 34-year-old woman with vague abdominal pain. Sagittal sonogram centers on dominant segment VIII hemangioma (straight arrow) that is also depicted in Figures. 1A, 1B, 1C, 3, and 4. Three distinct populations of hemangiomas are identified: a typical echogenic lesion (straight arrow), atypical hypoechoic lesion with echogenic border (curved arrow), and lesion containing fluid-fluid level (gray arrow). CT and MRI (Figs. 1A, 1B, 1C and 4) identified fluid-fluid level in segment VIII hemangioma (straight arrow) that was occult on sonography because of background echogenicity of lesion.

 



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Fig. 3. 34-year-old woman with vague abdominal pain. Sagittal sonograms center on dominant segment VIII hemangioma (straight arrow) after perflutren liquid microsphere (Definity, Bristol-Myers Squibb) is injected using contrast-specific, (low mechanical index) pulse-inversion imaging technique. Same lesion is also depicted in Figures 1A, 1B, 1C, 2, and 4. Progressive and persistent centripetal nodular enhancement (arrows) typical of hemangiomas is shown on 3 min (A) and 5 min (B) delayed images.

 




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Fig. 4. 34-year-old woman with vague abdominal pain. T2-weighted fat-saturated MR images were obtained at level of right adrenal. Supine (A) and right lateral decubitus (B) positions show gravity-dependent shifts in fluid-fluid level orientation in hemangiomas (arrows).

 

MRI was performed in the supine and right lateral decubitus positions to evaluate "mobility" of the fluid-fluid levels. All lesions were cerebrospinal fluid-bright on T2-weighted sequences. Sixteen lesions showed fluid-fluid levels. All fluid-fluid levels changed orientation to realign horizontally when moving the patient to the right lateral decubitus position from a supine position when imaged after a 15-min delay (Fig. 4). Enhancement after administration of gadolinium was typical for hemangiomas in all lesions, showing progressive nodular centripetal enhancement that persisted on imaging delayed up to 3 min from injection. Sixteen lesions showed incomplete centripetal progression on delayed imaging up to 3 min. All of these lesions had fluid-fluid levels on precontrast imaging.


Discussion
Top
Introduction
Case Report
Discussion
References
 
Fluid-fluid levels may be seen where fluid-like material of different densities are contained within a compartmentalized space. This has been described in the imaging literature in complicated cysts, abscesses, chronic hematomas, biliary cystadenomas, tumors with liquefactive necrosis or hemorrhage, and necrotic metastases [3]. Fluid-fluid levels within hemangiomas are very rare [1-3].

CT and especially MRI easily show these fluid-fluid levels. To our knowledge, we are the first to describe the same features on sonography. Stagnant or the slow flow of blood likely results in sedimentation of RBCs within the serum, producing the fluid-fluid levels. The superior fluid layer consists of serum and the inferior layer, unclotted sedimentary RBCs [1, 4]. On CT, the superior layer is of fluid attenuation, while the inferior layer has a higher attenuation due to the density of the packed cells. On MRI, T2-weighted sequences depict the superior fluid layer as high (fluid) signal intensity while the inferior layer is of relatively low signal intensity compared with the liver, because of the high cellular content. On T1-weighted imaging, the serum has low signal intensity and the sedimentary packed cells, intermediate signal intensity compared with the liver.

Itai et al. [1] describe more than 10 hemangiomas in three patients with fluid-fluid levels on CT, which were occult on sonography in the two patients who were scanned. CT did not reveal positional changes in the levels, and no evidence of enhancement was seen on dynamic CT. The authors postulate hemolyzed blood as the possible cause of this phenomenon. Obata et al. [2] report multiple fluid-fluid levels in a giant cavernous hemangioma. Typical peripheral nodular enhancement was observed on CT, but only on delayed 15-min scanning. Autopsy revealed no evidence of thrombosis or hemolysis within the hemangioma. Extremely slow flow within the hemangioma, resulting in separation of the blood cells and serum, was proposed as the mechanism for fluid-fluid level formation. We have shown changes in fluid-fluid level orientation on MRI when altering the patient's position. In addition, we have shown on DE-PII, CT, and MRI relatively delayed progressive enhancement of the lesions with fluid-fluid levels typical of hemangiomas. Thus, we concur with the theory that this subcategory of hemangioma has a relatively slow inflow of blood. As a result, a sedimentation effect is the likely cause of the fluid-fluid levels.

Sonography is considered more sensitive for the detection of fluid-fluid levels in liver lesions than CT [5]. In hemangiomas, multiple internal interfaces within the lesion result in the typical hyperechoic appearance. On sonography, fluid-fluid levels in this setting would be relatively more difficult to detect because of the resulting reduction in contrast resolution from the increased background echogenicity (Fig. 2). CT and MRI, however, are not affected by the number of interfaces within a lesion, relying on different physical properties to achieve contrast. We believe this may explain the observed discrepancy of fluid-fluid level detection between sonography and CT or MRI.

To further explain the imaging appearances, we propose an instructive analogy in the penis. Incidental fluid-fluid levels were noted in the corpora cavernosa on T2-weighted MR images in some patients having pelvic imaging for un-related reasons (Fig. 5). To our knowledge, this has not been previously described in the literature. The normal enhancement of the corpora cavenosa on gadolinium-enhanced MRI has been documented and bears an intriguing similarity to that of a cavernous hemangioma with gradual enhancement on sequential postcontrast MR images. In the penis, however, enhancement progresses in a centrifugal direction from the central cavernosal artery as opposed to the centripetal progression seen in hemangiomas [6]. As with the hemangiomas we describe containing fluid-fluid levels, enhancement is relatively delayed, occurring over 10 to 15 min. The corpus cavernosa consists of an intercommunicating volume (the sinusoidal intracorporeal network) separated by innumerable incomplete septations or baffles rather than multiple separate vessels or a single, large vascular space [7]. Blood flow in such a structure is slow, almost stagnant. As free communication occurs between the cavities, the volume of blood will act as a whole, explaining the appearance of a single sedimentation level across the corpus cavernosa after a period of inactivity by the patient. We propose that hemangiomas with fluid-fluid levels can be explained in an analogous way. We theorize that these lesions contain a large intercommunicating macroscopic space, baffled by a microscopic network of incomplete septations similar to the corpus cavernosa. Soyer et al. [3] describe a case in their series with imaging very similar to ours, in which the lesion underwent surgical biopsy. This showed a single large vascular space containing blood. Cavernous hemangiomas are described pathologically as having larger vascular spaces than capillary hemangiomas, but this is at a microscopic level. Large vascular lakes in these lesions are lined by a single layer of flat endothelial cells and separated by fibrous septa [8]. We can find no pathologic description of a variation of hemangiomas with macroscopic spaces that would correlate with the proposal of a single dilated cavity. The truth in our case will be revealed only with histologic correlation. However, the diagnosis of hemangioma in our patient did not require biopsy.



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Fig. 5. 70-year-old man. T2-weighted axial MR image of penis depicts fluid-fluid levels in corpora cavernosa.

 

In summary, a fluid-fluid level in a hemangioma is an unusual and dramatic variant in an otherwise common, benign, and well-described lesion. Our case illustrates typical enhancement characteristics on DE-PII, CT, and MRI that are preserved in these lesions, allowing a confident diagnosis of hemangioma without resorting to biopsy. We propose that this subcategory of hemangiomas consists of an intercommunicating volume "baffled" by incomplete septations, similar to the sinusoidal intracorporeal network of the corpus cavernosa. The relatively low sensitivity of sonography in detecting fluid-fluid levels in these lesions may be explained by the reduction in contrast produced by the background echogenicity of the baffles. The cause of the fluid-fluid levels is undoubtedly sedimenting RBCs in a large, slow-flowing vascular space.


References
Top
Introduction
Case Report
Discussion
References
 

  1. Itai Y, Ohtomo K, Kokubo T, Yamauchi T, Okada Y, Makita K. CT demonstration of fluid-fluid levels in nonenhancing hemangiomas of the liver. J Comput Assist Tomogr1987; 11:763 -765[Medline]
  2. Obata S, Matsunaga N, Hayashi K, Ohtsubo M, Morikawa T, Takahara O. Fluid-fluid levels in giant cavernous hemangioma of the liver: CT and MRI demonstration. Abdom Imaging1998; 23:600 -602[Medline]
  3. Soyer P, Bluemke DA, Fishman EK, Rymer R. Fluid-fluid levels within focal hepatic lesions: imaging appearance and etiology. Abdom Imaging 1998;23:161 -165[Medline]
  4. Vilgrain V, Boulos L, Vullierme MP, Denys A, Terris B, Menu Y. Imaging of atypical hemangiomas of the liver with pathologic correlation. RadioGraphics2000; 20:379 -397[Abstract/Free Full Text]
  5. Federle MP, Filly RA, Moss AA. Cystic hepatic neoplasms: complementary roles of CT and sonography. AJR1981; 136:345 -348[Abstract/Free Full Text]
  6. Kaneko K, De Mouy EH, Lee BE. Sequential contrast-enhanced MR imaging of the penis. Radiology1994; 191:75 -77[Abstract/Free Full Text]
  7. Barreto J, Caballero C, Cubilla A. Penis. In: Sternberg SS. Histology for pathologists, 2nd ed. Philadelphia, PA: Lipincott-Raven Publishers, 1997:1039 -1050
  8. Feldman M. Hemangioma of the liver; special reference to its association with cysts of the liver and pancreas. Am J Clin Pathol 1958;29:160 -162[Medline]

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