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AJR 2003; 180:1347-1350
© American Roentgen Ray Society

Original Report

Fat Sparing of Surrounding Liver From Metastasis in Patients with Fatty Liver: MR Imaging with Histopathologic Correlation

Jae-Joon Chung1, Myeong-Jin Kim, Joo Hee Kim, Jong Tae Lee and Hyung Sik Yoo

1 All authors: Department of Diagnostic Radiology and Research Institute of Radiological Science, Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemun-gu, Seoul 120-752, Korea.

Received May 28, 2002; accepted after revision October 21, 2002.

 
Address correspondence to J.-J. Chung.


Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of our study was to evaluate the characteristic MR imaging findings and histopathologic correlation of peritumoral fat sparing of liver metastasis in patients with fatty liver.

CONCLUSION. Out-of-phase spoiled gradient-echo MR imaging was useful in detecting and characterizing the peritumoral fat sparing of liver metastasis in patients with fatty liver that was isointense to surrounding hepatic parenchyma on unenhanced in-phase spoiled gradient-echo, T2-weighted inversion recovery, and contrast-enhanced nonsuppressed spoiled gradient-echo MR imaging.


Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Fatty liver (hepatic steatosis, fatty metamorphosis) is the result of excessive accumulation of triglycerides within hepatocytes, which is associated with a variety of clinical disorders [1, 2]. Although it is most commonly a diffuse process, fatty liver is frequently nonuniform, patchy, or focal [3]. Diffuse fatty liver can obscure metastases or dilated bile ducts [2].

Conversely, focal areas of uninvolved (spared) normal liver are frequently seen on sonography, CT, or MR imaging [4]. Focal fat sparing generally shows a geographic shape in typical locations such as along the gallbladder fossa adjacent to the interlobar fissure, in the medial segment of the left lobe adjacent to the porta hepatis, or in a subcapsular location [5, 6, 7].

Hepatic masses in a diffusely fatty liver may not be easily discerned on CT and sonography, with reported decreased sensitivity and specificity of lesion detection [8]. In such cases, MR imaging may be the modality of choice for the detection and characterization of both fatty liver and coexistent hepatic masses.

We recently encountered peritumoral fat sparing of a solitary liver metastasis in patients with a diffusely fatty liver that was pathologically confirmed at surgery. To our knowledge, no report has appeared in the literature about the histopathologic correlation with the MR imaging findings of peritumoral fat sparing of liver metastasis in patients with fatty liver. We evaluated the characteristic MR imaging findings and histopathologic correlation of peritumoral fat sparing of liver metastasis in patients with fatty liver.


Materials and Methods
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 Materials and Methods
Results
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The medical records of all patients who had hepatic metastases and a diffusely fatty liver between August 2000 and March 2002 were cross-referenced with the histopathologic records. The patients had been referred for MR imaging as their initial examination of the hepatobiliary system or as the follow-up examination of focal hepatic lesions shown on prior imaging such as sonography, CT, or MR imaging.

Patients were included in our study if they had undergone segmentectomy or lobectomy resection of the hepatic metastasis and the surrounding fatty liver; had undergone both MR imaging and surgery within 1 month; and had undergone no intervening therapeutic intervention, including systemic chemotherapy or chemoembolization, between the time of MR imaging and the histopathologic examination. The clinical records of all patients were checked for evidence of chemotherapy or other treatments.

After reviewing the medical records, we selected eight patients who met the criteria of fatty liver, a single liver metastasis, MR imaging of the liver, and surgery. Among them, six patients showed the peritumoral fat sparing on both out-of-phase spoiled gradient-echo MR images and histopathology, but the other two patients did not. One patient had a primary colorectal carcinoma, and the other had a primary gastric cancer.

Six patients (three men and three women; age range, 32–75 years; mean age, 51 years) with peritumoral fat sparing of liver metastases revealed on MR imaging were studied to compare the MR imaging findings with the histopathologic findings. The hepatic metastases originated from the following primary tumors: colorectal carcinoma (n = 4), ileal carcinoid (n = 1), and breast cancer (n = 1). All six patients had a single liver metastasis. All four patients with metastasis from colorectal carcinoma had nonmucinous adenocarcinoma.

MR imaging was performed with a 1.5-T MR imaging system (Signa MR/i; General Electric Medical Systems, Milwaukee, WI). MR imaging included T1-weighted breath-hold in-phase (TR/TE, 140/4.5) and out-of-phase (140/2.2) axial spoiled gradient-echo (flip angle, 80°; section thickness, 8 mm; intersection gap, 20%) and T2-weighted axial inversion recovery (5110/76; inversion time, 150 msec) images. Axial spoiled gradient-echo MR images were also acquired immediately (18 sec) after IV bolus injection of 0.1 mmol/kg of gadopentetate dimeglumine (Magnevist;

Schering, Berlin, Germany) based on body weight at 45 sec, at 90 sec with fat suppression, and at 5–10 min. From these seven sets of images, the unenhanced in-phase and out-of-phase spoiled gradient-echo MR images and the contrast-enhanced early (18-sec) and late (90-sec) fat-suppressed spoiled gradient-echo MR images were reviewed to evaluate the location and exact size of the tumor, the shape and size of the peritumoral fat-sparing area, and the signal drop of the peritumoral area on out-of-phase spoiled gradient-echo MR images.

An experienced hepatic pathologist who was unaware of the MR imaging findings evaluated the resection specimens. The histopathologic examination involved the following: evaluation of the metastasis, including the histologic type and differentiation; and evaluation of the tumor border surrounding the metastasis, including compressed hepatic parenchyma, atrophy of hepatic cords, indirect evidence of shunting such as the absence of fatty infiltration adjacent to the tumor, and portal venous occlusion by tumor emboli.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
All hepatic metastases of the six patients showed low signal intensity on unenhanced in-phase spoiled gradient-echo MR images with diffuse and slightly high signal intensity of surrounding hepatic parenchyma due to infiltration of fat. There was no difference of signal intensity between the peritumoral fat-sparing zone and the surrounding hepatic parenchyma on unenhanced in-phase spoiled gradient-echo, T2-weighted inversion recovery, or contrast-enhanced nonsuppressed spoiled gradient-echo MR imaging. However, marked signal drop of surrounding liver parenchyma in all cases was shown on unenhanced out-of-phase spoiled gradient-echo MR images, which showed a nondecreased, high-signal-intensity area of peritumoral zone because of no or little fat deposition.

After the administration of contrast media, three metastatic tumors from colorectal carcinoma and one metastatic tumor from breast cancer showed mild to moderate peripheral rim enhancement on early contrast-enhanced spoiled gradient-echo MR images. The remaining two tumors showed negligible rim enhancement. In all six patients, the mild signal drop of surrounding liver parenchyma was seen with a minimal peritumoral high-signal-intensity zone on late fat-suppressed contrast-enhanced spoiled gradient-echo MR images, which was not noted on early contrast-enhanced spoiled gradient-echo images without fat suppression. On the axial images, peritumoral high-signal-intensity lesions had a wedge shape (Figs. 1A, 1B and 1C) in three patients and a polygonal shape (Figs. 2A, 2B, 2C and 2D) in three patients.



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  		Fig. 1A .—75-year-old woman with liver metastasis from colon cancer. On unenhanced in-phase spoiled gradient-echo MR image, 3.1 x 2.2 cm mass is noted in segment VII of liver without peritumoral signal-intensity change. Liver shows diffusely increased signal intensity on in-phase spoiled gradient-echo MR image because of fatty infiltration.

 


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  		Fig. 1B .—75-year-old woman with liver metastasis from colon cancer. On unenhanced out-of-phase axial spoiled gradient-echo MR image, 5.5 x 3.8 cm wedge-shaped high-signal-intensity lesion (large arrowheads) surrounding low-signal-intensity tumor (small arrowheads) is seen in segment VII of liver that is well contrasted by diffusely decreased signal intensity of remaining fatty liver parenchyma.

 


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  		Fig. 1C .—75-year-old woman with liver metastasis from colon cancer. On histopathologic photomicrograph, fat-sparing zone (solid line) is well depicted between tumor mass (T) and fatty liver parenchyma (F). (H and E, x20)

 


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  		Fig. 2A. —37-year-old woman with liver metastasis from ileal carcinoid. On unenhanced in-phase spoiled gradient-echo MR image, 2.5 x 1.8 cm well-defined mass is noted in segment VIII of liver dome without peritumoral signal-intensity change. Liver shows diffusely increased signal intensity on in-phase spoiled gradient-echo MR image because of fatty infiltration.

 


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  		Fig. 2B. —37-year-old woman with liver metastasis from ileal carcinoid. On unenhanced out-of-phase axial spoiled gradient-echo MR image, 4.5 x 3.5 cm polygonal high-signal-intensity lesion (large arrowheads) surrounding low-signal-intensity tumor (small arrowheads) is seen in segment VIII of liver, which is contrasted with diffusely decreased signal intensity of remaining fatty liver parenchyma.

 


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  		Fig. 2C. —37-year-old woman with liver metastasis from ileal carcinoid. On early contrast-enhanced spoiled gradient-echo MR image without fat suppression, metastatic tumor is well enhanced because of primary hypervascular ileal carcinoid tumor. Polygonal fat sparing is not differentiated from surrounding fatty liver parenchyma.

 


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  		Fig. 2D. —37-year-old woman with liver metastasis from ileal carcinoid. On histopathologic photomicrograph, fat-sparing zone (solid line) is well visualized between tumor mass (T) and fatty liver parenchyma (F). (H and E, x20)

 

The histopathologic results of hepatic metastases in four patients with colorectal carcinoma were moderately differentiated nonmucinous adenocarcinomas with mild to moderate fibrotic tumor stroma. A rim of peritumoral fat sparing and mild compression of hepatic parenchyma were histopathologically confirmed between the tumor mass and the surrounding fatty liver in all patients. Atrophy of the hepatic cords and tumor emboli causing occlusion of the portal vein were not shown in these metastatic tumors. The histopathologic results also revealed the rim of peritumoral fat sparing and mild compression of surrounding hepatic parenchyma in the remaining two patients, who had ileal carcinoid and breast cancer. Tumor emboli causing occlusion of the portal vein were not found in these specimens.


Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Focal fat sparing in a diffusely fatty liver is caused by decreased portal flow from the small intestine or by an arterioportal shunt [1, 5, 7]. Although they are not exactly understood in most cases, the known causes of focal fat sparing in fatty liver are aberrant gastric venous drainage into segment IV of the liver [6], systemic venous drainage by the cystic and capsular veins, and arterioportal shunt [5, 9]. The arterioportal shunt can lead to the localized dilution or reduction in portal blood flow, causing a compensatory increase of arterial flow into the involved territory [5]. MR imaging is the modality of choice for differentiating focal sparing from tumorous tissue in patients with inconclusive sonographic or CT findings [10]. The imaging features that are characteristic of focal fat sparing include a wedge shape, lack of mass effect, and the presence of a normal vascular structure [4].

The round shape of peritumoral fat sparing may be caused by direct compression of the adjacent hepatic parenchyma by the metastatic mass itself, adding to the decreased portal venous flow from the tumor emboli or the external compression of the portal vein. We can assume that the hematogenous metastatic tumor emboli involving the portal vein branch may have a role in peritumoral fat sparing, compared with primary hepatic tumors, because we have not found any case of peritumoral fat sparing in the primary hepatic tumors such as hepatocellular carcinoma, hemangioma, or focal nodular hyperplasia.

One cause of peritumoral fat sparing in our patients might be the microinvasion of portal venules by the hematogenous tumor emboli, causing decreased perfusion of portal venous flow, even though the microinvasion of portal venules by the tumor emboli was not histopathologically proven in our study. However, one of three patients with a polygonal peritumoral high signal intensity on axial spoiled gradient-echo MR imaging showed the wedge shape on out-of-phase reconstructed coronal spoiled gradient-echo MR imaging, which may suggest the possibility of occlusion of the portal branches by the tumor emboli causing the fat sparing in the involved territory.

In our study, the focal fat-sparing zone was isointense to the surrounding liver parenchyma on unenhanced in-phase spoiled gradient-echo, T2-weighted inversion recovery, and early contrast-enhanced spoiled gradient-echo MR images without fat suppression. On late contrast-enhanced spoiled gradient-echo MR images with fat suppression, the mild signal drop of surrounding liver parenchyma was visualized only with a minimal peritumoral high-signal-intensity zone. The degree of signal drop of hepatic parenchyma on contrast-enhanced fat-suppressed spoiled gradient-echo MR images was less than that of liver on unenhanced out-of-phase spoiled gradient-echo images because the hepatic parenchyma was diffusely enhanced using gadopentetate dimeglumine. Therefore, unenhanced out-of-phase T1-weighted MR imaging was the most useful modality in the detection of the peritumoral fat-sparing area but not in the detection of metastatic tumor itself.

Histopathologically, with liver metastasis, surrounding liver parenchyma may show compression or atrophy of hepatocyte cords, scattered foci of chronic inflammation replacing lost hepatocytes, and the absence of fatty change. On out-of-phase images, this zone of compressed liver parenchyma bordering on the metastasis appears as a moderately high-signal rim. Peritumoral edema can be ruled out if peritumoral high signal intensity is not shown on T2-weighted MR images.

On unenhanced CT, peritumoral fat sparing with a spherical shape may appear as a hyperattenuating rim surrounding a hypoattenuating tumor. The width of this thin ring or thick irregularly shaped rim is approximately 2–20 mm [11]. The hyperattenuating rim on unenhanced CT is frequently shown as a hyperintense rim on out-of-phase T1-weighted gradient-echo MR imaging in 80% of tumors in the fatty liver (Taupitz M, presented at the Radiological Society of North America meeting, December 1998). Occasionally, wedge-shaped focal fat sparing with configurations related to the intrahepatic distribution of portal vein branches does not immediately suggest a tumor, but the mass at the apex of the spared area should be carefully observed because it can often be small [12]. In such a case, the combination of unenhanced in-phase and out-of-phase spoiled gradient-echo MR imaging may be more helpful than unenhanced CT or contrast-enhanced fat-suppressed spoiled gradient-echo MR imaging in the evaluation of small tumor causing wedge-shaped focal fat-sparing in the liver.

Limitations of our study included the following: a small number of patients had the criteria of fatty liver, single liver metastasis, MR imaging of the liver, and surgery; the number of times that this finding was present in patients with fatty liver and metastatic tumors was not investigated; and the microinvasion of portal venule by the tumor emboli was not histopathologically proven in this study.

In conclusion, out-of-phase spoiled gradient-echo MR imaging was useful in the detection and characterization of the peritumoral fat sparing of liver metastasis in patients with fatty liver that was isointense to surrounding hepatic parenchyma on unenhanced in-phase spoiled gradient-echo, T2-weighted inversion recovery, and contrast-enhanced nonsuppressed spoiled gradient-echo MR imaging.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Semelka RC, Braga L, Armao D, et al. Liver. In: Semelka RC. Abdominal–pelvic MRI, 1st ed. New York: Wiley-Liss, 2002:33 –317
  2. Siegelman ES, Rosen MA. Imaging of hepatic steatosis. Semin Liver Dis 2001;21:71 –80[Medline]
  3. Rampal P, Desmorat H, Bruneton JN, et al. Irregular hepatic steatosis: clinical and imaging study of 6 cases. Gastroenterol Clin Biol 1986;10:43 –48[Medline]
  4. Mitchell DG. Focal manifestations of diffuse liver disease at MR imaging. Radiology 1992;185:1 –11[Abstract/Free Full Text]
  5. Arita T, Matsunaga N, Honma Y, Nishikawa E, Nagaoka S. Focally spared area of fatty livers caused by arteriportal shunt. J Comput Assist Tomogr 1996;20:360 –362[Medline]
  6. Matsui O, Kadoya M, Takahashi S, et al. Focal sparing of segment IV in fatty liver shown by sonography and CT: correlation with aberrant gastric venous drainage. AJR 1995;164:1137 –1140[Abstract/Free Full Text]
  7. Arai K, Matsui O, Takashima T, Ida M, Nishida Y. Focal spared areas in fatty liver caused by regional decreased portal flow. AJR 1988;151:300 –302[Free Full Text]
  8. Kato M, Saji S, Kanematsu M, et al. A case of liver metastasis from colon cancer masquerading as focal sparing in a fatty liver. Jpn J Clin Oncol 1997;27:189 –192[Abstract/Free Full Text]
  9. Semelka RC, Hussain SM, Marcos HB, Woosley JT. Perilesional enhancement of hepatic metastases: correlation between MR imaging and histopathologic findings—initial observations. Radiology 2000;215:89 –94[Abstract/Free Full Text]
  10. Itai Y. Peritumoral sparing of fatty liver: another important instance of focal sparing caused by a hepatic tumor. AJR 2000;174:868 –870[Free Full Text]
  11. Itai Y, Maeda M, Echigo J, et al. Hyperattenuating rim on noncontrast CT of liver: probable peritumoral sparing of fatty infiltration. Clin Radiology 1996;51:406 –410[Medline]
  12. 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 –1395[Free Full Text]

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