Volume 61, Issue 1, Pages 33-43 (January 2007)

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ABSTRACT

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Imaging of hepatic steatosis and fatty sparing

Received 9 October 2006; accepted 2 November 2006.

Abstract

Radiology has gained importance in the non-invasive diagnosis of hepatic steatosis. Ultrasonography is usually the first imaging modality for the evaluation of hepatic steatosis. Unenhanced CT with or without dual kVp measurement and MRI with in and out of phase sequence can allow objective evaluation of hepatic steatosis. However, none of the imaging modalities can differentiate non-alcoholic steatohepatitis/fatty liver disease from simple steatosis. Evaluation of hepatic steatosis is important in donor evaluation before orthotopic liver transplantation and hepatic surgery. Recently, one-stop shop evaluation of potential liver donors has become possible by CT and MRI integrating vascular, parenchymal, volume and steatosis evaluation. Moreover hepatic steatosis (diffuse, multinodular, focal, subcortical, perilesional, intralesional, periportal and perivenular), hypersteatosis and sparing (geographic, nodular and perilesional or peritumoral) can cause diagnostic problems as a pseudotumor particularly in the evaluation of oncology patients. Liver MRI is used as a problem-solving tool in these patients. In this review, we discuss the current role of radiology in diagnosing, quantifying hepatic steatosis and solutions for diagnostic problems associated with fatty infiltration and sparing.

Keywords: Steatosis, Liver, Fat, Fatty sparing, Fatty infiltration, CT, MRI

Article Outline

• Abstract

• 1. Introduction

• 2. Techniques for the evaluation of steatosis

• 2.1. Ultrasonography (US)

• 2.2. Computed tomography (CT)

• 2.3. Magnetic resonance imaging (MRI)

• 3. Hepatic steatosis

• 3.1. Focal steatosis

• 3.2. Hypersteatosis

• 3.3. Perilesional and subcapsular steatosis

• 3.4. Intracellular lipid containing lesions (intratumoral or intralesional steatosis)

• 3.5. Periportal and perivenular steatosis

• 4. Hepatic fatty sparing

• 4.1. Focal geographic and nodular fatty sparing

• 4.2. Perilesional or peritumoral fatty sparing

• 5. Conclusion

• References

• Copyright

1. Introduction

Hepatic steatosis is characterized by increased triglyceride content of liver due to a variety of causes [1], [2], [3]. Most important factors for the development of steatosis are alcoholism, non-alcoholic steatohepatitis (NASH) and obesity [4]. Focal fatty infiltration and sparing develop secondary to altered liver vascular supply most commonly adjacent to liver capsule [5].

This review discusses methods for detection and quantification of steatosis including ultrasonography, CT and MRI, and radiologic findings of different forms of steatosis (diffuse, hypersteatosis multiple nodules, focal, subcortical, perilesional, intralesional, periportal and perivenular) and fatty sparing (geographic, nodular and perilesional) (Table 1).

Table 1.

Different forms of hepatic steatosis and fatty sparing

	Hepatic steatosis
	1	Diffuse
	2	Multinodular
	3	Hypersteatosis
	4	Focal geographic steatosis
	5	Focal nodular steatosis
	6	Intralesional steatosis
	7	Perilesional steatosis
	8	Subcapsular steatosis
	9	Periportal and perivenular steatosis

	Hepatic fatty sparing
	1	Focal geographic sparing
	2	Focal nodular sparing
	3	Focal segmental or lobar sparing
	4	Perilesional sparing

2. Techniques for the evaluation of steatosis

2.1. Ultrasonography (US)

US is the simplest method for crude estimation of liver steatosis. However, accurate quantification of steatosis is not feasible with the current technology. Steatosis appears bright or hyperechoic relative to adjacent right kidney or spleen [6], [7], [8]. Sensitivity of US increases with increasing degree of steatosis [7], [9]. Mild steatosis is characterized by mild increase in liver echogenicity. Moderate steatosis can be diagnosed with increased liver echogenicity that obscures visualization of hepatic and portal vein wall. However, ultrasonographic evaluation of steatosis does not exactly match histopathologic quantification of steatosis. In case of severe steatosis usually posterior attenuation avoids deep liver parenchyma evaluation. If there is posterior attenuation it may be useful for diagnosing steatosis of ≥30% [10]. Evaluation of steatosis in patients with hepatitis can be difficult due to accompanying inflammation and fibrosis [11], [12]. Fibrosis may also appear hyperechoic, but most of the time fibrosis and fatty infiltration co-exist in cirrhotic patients which is called fatty–fibrotic pattern [9], [13]. When compared to MRI, ultrasonography was found to be insensitive to the diagnosis of minimal degree of steatosis, however MRI and ultrasonography were equally useful in the diagnosis of heavy fat accumulation [14]. Recently, new methods are being evaluated for objective evaluation of steatosis by using artifical neural networks and computerized analysis of liver texture by indices of ultrasonic backscatter [15], [16], [17].

2.2. Computed tomography (CT)

CT can be used for the evaluation of hepatic steatosis. Steatosis results in decreased attenuation of liver, which can be measured by Hounsfield Unit (H) and appears as hypodense liver parenchyma [18], [19], [20], [21], [22], [23], [24]. Enhanced CT has a limited role in the diagnosis of steatosis due to influence of contrast injection rate and timing of analysis on liver attenuation [25], [26]. Comparing attenuation of liver to skeletal muscle has been reported to be more specific compared to liver to spleen attenuation on enhanced CT images [27]. Fibrosis does not cause any effect on the attenuation of liver [9].

Unenhanced CT images are used for qualitative evaluation and spleen is used as the reference organ for comparison. Spleen to liver attenuation ratio or difference between attenuation of spleen and liver can be used for the evaluation of steatosis. Attenuation of spleen is approximately 8–10 HU less than the liver in a normal patient. Piekarsky et al. [19] reported that a liver-to-spleen attenuation difference greater than −10 HU was highly predictive of hepatic steatosis. Iwasaki et al. suggested cut-off value of 1.1 (spleen to liver attenuation ratio) for exclusion of moderate steatosis based on their correlative findings on 194 patients [21]. Some authors also use dual kVp measurements for the evaluation of steatosis and characterization of focal steatosis by using 80 and 140kVp [28], [29], [30], [31]. However, this technique has limitations in patients with hepatic iron overload. Recent introduction of dual source CT may enable wider use of this technique due to ability of this new scanner that allow acquisition of same image with two different kVp simultaneously [32]. Kamel et al. used a comprehensive protocol including unenhanced, arterial phase and venous phase images for the evaluation of liver transplant donors [31]. Park et al. also used CT for the assessment of hepatic steatosis in transplant donors and concluded that unenhanced CT had high performance for diagnosing 30% or more steatosis with 100% specificity and 82% sensitivity [33]. In their study, liver/spleen attenution ratio of 0.8 and difference of 9H between liver and spleen attenuation had similar sensitivity. Use of suggested criteria can be helpful in avoding biopsy in moderately steatotic livers [34]. In another study, Limanond et al. [35] also concluded that unenhanced CT quantified the degree of steatosis relatively well in liver donor patients, but stated that most of the time liver biopsy is necessary to exclude fatty liver, co-existing iron deposition and parenchymal disease. Density histogram analysis has also been proposed for the evaluation of steatosis which requires further studies [36].

2.3. Magnetic resonance imaging (MRI)

MRI appears to be the most sensitive and objective tool for the demonstration and quantification of hepatic steatosis. The sequence used for this purpose is a breathhold T1-weighted gradient-echo in/out of phase sequence [3], [37], [38], [39], [40], [41]. This sequence can be obtained with all types of MR scanners with different Tesla power including 0.5, 1, 1.5 and 3T, but TE values for in and out phases varies according to the magnetic power of the scanner.

In the presence of steatosis signal drop is observed on out of phase images due to phase cancellation of fat and water. This technique has been used for the evaluation of patients prior to living related liver transplantation and has shown promise for non-invasive evaluation of steatosis [42], [43]. Recently, this sequence has been optimized for the quantitative measurement of fat fraction in the liver by applying dual flip angle (20 and 70 degrees) to resolve the ambiguity of the dominant constituent [44]. Qayyum et al. [45] recently compared out of phase gradient echo and fat saturated spin–echo technique and suggested that fast spin–echo may allow quantification of liver fat better than out of phase gradient echo sequence especially in cirrhotic patients. Also, MR spectroscopy has been used in few studies and may be widely used in the future for the quantification of steatosis [46], [47], [48].

3. Hepatic steatosis

A variety of clinical disorders is associated with diffuse steatosis including obesity, malnutrition, diabetes mellitus, steroid use, alcoholic liver disease, pregnancy and hepatitis [1], [2], [3], [4], [5], [6]. Major two causes of hepatic steatosis are alcoholic liver disease and non-alcoholic steatohepatitis (NASH). Latter cause has emerged recently as a distinct clinical entity, which is characterized by inflammation and fibrosis associated with steatosis [4], [49], [50]. Although differentiation of NASH and simple steatosis is currently based on liver biopsy findings, CT findings of hepatomegaly, portal lymph nodes and increased caudate lobe to right lobe ratio and splenomegaly have been found more frequently in patients with NASH [51], [52].

Hepatic steatosis can induce changes in the Doppler waveform of hepatic arteries and hepatic veins. Hepatic artery resistance index was found to be decreased with increasing severity of steatosis [53]. Hepatic vein Doppler waveform can be monophasic and biphasic in patients with fatty infiltration of liver independent of the degree of steatosis [54].

For comprehensive evaluation of potential liver donors CT and MRI protocols are being used [31], [55], [56]. These one-stop shop methods allow evaluation of hepatic fat content, vascular (arterial and venous) variations, parenchymal pathologies and volume of right and left liver lobes. Steatosis is graded mild (less than 30%), moderate (between 30 and 60%) and severe (more than 60%) by histologic examination. For living-related liver transplantation mild degree of steatosis is acceptable [57]. Although a recent report suggests use of moderately steatotic livers for transplantation, it is not generally accepted in most of the institutions [58]. MRI appears to be the most useful test for preoperative evaluation of liver donors in terms of steatosis (Fig. 1). But finding of posterior attenuation on ultrasonography and use of ratio or difference of liver and spleen attenuation on CT can be useful in diagnosing steaosis of greater than 30% and may obviate liver biopsy in these patients [10], [33], [34]. However, no standardization is present regarding technical parameters and the way of measuring steatosis.

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Fig. 1. Radiologic appearance of diffuse steatosis. (A) CT image shows diffuse hypodensity of liver compared to spleen. (B and C) In and out of phase T1-weighted gradient echo images show diffuse signal drop on out of phase image consistent with steatosis.

Hepatic steatosis can be diffuse, heterogenous, focal, perilesional, subcapsular, intralesional and perivascular (Table 1; Fig. 2). Diffuse form can be in the form of multiple nodules and can mimic metastatic disease [59], [60] (Fig. 3).

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Fig. 2. Heterogenous steatosis can cause diagnostic problems. (A) CT image shows a patient with diffuse steatosis in left lobe and heterogenous steatosis in right lobe. (B) US image shows diffuse heterogenous increased echogencitiy. (C and D) MR images show diffuse heterogenous signal drop on out of phase images consistent with steatosis. Note normal traversing vascular structures within the heterogenous steatosis without distortion.

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Fig. 3. A patient with multiple hyperechoic lesions and ovarian cancer underwent liver MRI. (A and B) Out of phase images show multiple lesions with signal drop compared to in phase images consistent with multinodular steatosis.

3.1. Focal steatosis

Focal fatty infiltration usually appears geographic but may be nodular and mass like and can cause pseudotumor appearance (Fig. 4) [7], [61], [62], [63], [64]. In most cases both focal sparing and focal steatosis have characteristic locations, such as the gallbladder fossa, the medial segment near the falciform ligament, the subcapsular region and the porta hepatis (Fig. 5). Focal fatty infiltration or sparing are due to anomalous small veins entering liver which are communicating with pancreaticoduodenal, cholecystic and gastric venous system or other veins coursing through the surface of the liver such as superior and inferior sappey veins, and capsular veins [5]. Imaging features of focal fatty liver or focal sparing include typical location, wedge-shape or geographic configuration, absence of mass effect, coursing of normal vascular structures through the fatty area, and enhancement on CT and MRI indistinguishable from that of normal liver allows differentiation from other lesions demonstrating intralesional steatosis. Decrease in the portal flow can induce fatty infiltration in the normal liver parenchyma [65], [66]. Conversely, localized decreased intrahepatic portal flow can cause focal sparing in a diffusely steatotic liver at the sites of venous return from systemic veins [67]. Therefore, hepatopedal flow outside the main portal vein can cause various parenchymal changes in the liver, such as focal fatty infiltration and focal fatty sparing.

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Fig. 4. Focal nodular steatosis can mimic focal liver lesions. (A and B) Axial in and out of phase MR images show a nodular lesion at the dome of liver consistent with focal nodular steatosis. Note presence of signal drop (arrow) on out phase images.

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Fig. 5. Focal steatosis can be geographic or nodular in shape. (A) Most common area of focal steatosis occurs adjacent to falciform ligament which is seen hypondense on CT. (B) Note geographic area of signal drop on out of phase MR images in the right lobe consistent with geographic steatosis.

3.2. Hypersteatosis

Hypersteatosis has been initially described by Basaran et al. [68] to describe areas of relatively more steatotic areas of liver in patients with diffuse liver steatosis (Fig. 6). This entity may cause diagnostic problems in oncology patients as it may appear as a hypodense lesion on CT in a steatotic liver.

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Fig. 6. Focal hypersteatosis is seen as a relatively more steatotic area in a steatotic liver. (A and B) Liver MRI shows diffuse signal drop on out of phase images compared to in phase images. Note focal area in segment 4 (arrow) demonstrating more signal drop compared to rest of liver consistent with hypersteatosis.

3.3. Perilesional and subcapsular steatosis

Perilesional steatosis can occur around metastases of insulinoma and thought to represent local effect of insulin in the liver parenchyma. It appears as bright echogenic rim on ultrasonography and as a hypointense rim on out of phase T1-weighted gradient echo MR images around metastatic lesions [69]. Peripheral steatosis has also been reported around focal nodular hyperplasia by Eisenberg et al. [70]. Also in diabetic patients receiving insulin through peritoneal dialysis, characteristic subcapsular steatosis can be observed due to local action of insulin at the surface of the liver [69], [71], [72].

3.4. Intracellular lipid containing lesions (intratumoral or intralesional steatosis)

Fat within the lesions can be in the form of macroscopic lipid and intracellular lipid. Lesions with intracellular lipid are seen as areas of focal steatosis on out of phase images. These lesions are hepatic adenoma, hepatocellular carcinoma, regenerative nodules and rarely focal nodular hyperplasia [68], [73], [74] (Fig. 7). However, post-contrast imaging characteristics of these lesions allow differentiation from areas of focal steatosis.

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Fig. 7. Focal liver lesions can contain intracellular lipid. (A) Axial out of phase MRI images shows a lesion with signal drop in a patient with hepatitis. (B) T2-weighted image shows hyperintensity of lesion consistent with hepatocellular carcinoma.

3.5. Periportal and perivenular steatosis

Perivascular fatty infiltration is a recently described entity, which is mostly seen in alcoholic patients [75]. Periportal fatty infiltration and perivenular fatty infiltration around hepatic veins can be observed alone or in combination. Imaging findings include hypodense areas along the portal and/or hepatic veins on CT which demonstrates signal drop on out of phase T1-weighted MR images. Interestingly, fatty infiltration around portal vein can be segmental which has been reported back in 1993 [76].

4. Hepatic fatty sparing

4.1. Focal geographic and nodular fatty sparing

Hepatic fatty sparing occurs because of a similar mechanism leading to the formation of focal steatosis which is altered liver hemodynamics caused by small veins entering liver (Fig. 8) [5], [7], [66], [77], [78], [79].

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Fig. 8. Focal geographic fatty sparing occurs due to small veins entering liver. (A) Axial CT image shows a vein in the segments 2 and 3 communicating with gastric venous system in a patient with lung cancer and occluded superior vena cava. (B and C) Venous phase CT images of the former patient and another patient show areas of sparing appearing hyperdense relative to steatotic liver in left lobe. (D and E) Out of phase MRI and CT images show focal sparing (arrow) adjacent to gallbladder fossa and liver capsule, respectively.

On ultrasonography focal fatty sparing appears as a hypoechoic lesion in a steatotic liver. On CT it appears as hyperdense areas within diffusely hypodense liver parenchyma. MRI allows characterization of these lesions by using in and out phase T1-weighted gradient echo sequence. Interestingly, areas of fatty sparing are not visible on other pre-contrast and post-contrast MRI sequences. Most of the time MRI is requested for characterization of focal lesion in an oncology patient with hepatic steatosis. If MRI scanning protocol does not include in and out of phase sequence, MRI examination can be interpreted as normal, which can lead to confusion in the patients and their doctors. Although most of the time fatty sparing is geographic in shape sometimes it can be nodular and atypical in location, which can cause diagnostic problems [80]. In such situations MRI can allow confident non-invasive diagnosis which can obviate biopsy. Focal fatty sparing can also occur around or distal to a tumor and sometimes can mask a tumor on CT (Fig. 9). According to Grossholz et al. [81] focal sparing adjacent to a space occupying lesion can be peripheral, segmental or lobar, depending on the relationship between the tumor and major portal vessels.

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Fig. 9. Steatosis and sparing can cause diagnostic problems in oncology patients. (A) Axial CT image obtained 2 month prior to MRI shows hyperdense areas in a steatotic liver. (B and C) Axial in and out of phase images show multiple metastatic lesions in a steatotic liver. Note that metastasis in segment 7 (arrow) was not visible on CT image because both metastasis and fatty sparing appear hyperdense.

4.2. Perilesional or peritumoral fatty sparing

Perilesional sparing has been initially described by Itai et al. [82] in 1996 around various lesions including hemangiomas, metastases and hepatocellular carcinoma on CT imaging in patients with steatosis. Gabata et al. [83] used in and out of phase MRI imaging to characterize areas of perilesional sparing around metastatic lesions. Later, Chung et al. [84] confirmed these peritumoral fatty sparing by histopathologic analysis in patients with metastases. In 2005, Marti-Bonmati et al. [85] studied hepatic lesions with peritumoral sparing and found that 51% of the metastases and 18.5% of hemangiomas and 2% of hepatocellular carcinomas had perilesional sparing in their cohort. They suggested that perilesional sparing mainly represented decrease in portal flow due to either by compressed or atrophic hepatocyte cords in expanding metastases or arterioportal perfusion abnormalities in hemangiomas. We observed similar appearance around focal nodular hyperplasia (Fig. 10).

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Fig. 10. Perilesional fatty sparing appears as a hyperintense rim on out of phase images around focal benign or malignant liver lesions. (A and B) Axial in and out of phase images show a lesion with hyperintense rim in segment 7 (arrow) consistent with perilesional steatosis. (C) Arterial phase T1-weighted post-contrast MRI image shows homogeneous enhancement and central scar consistent with focal nodular hyperplasia. (D) Perilesional steatosis can also be seen around metastatic lesions.

5. Conclusion

In conclusion, cross-sectional imaging plays an important role in the diagnosis of hepatic steatosis. MRI appears to be the most sensitive test for the diagnosis and quantification of steatosis. CT and ultrasonography are also widely used for the diagnosis of steatosis. However, multicenter trials and standardization of radiologic techniques (CT, MRI and ultrasonogarphy) and parameters are needed in order to objectively assess the role of radiology in the quantitative assessment of steatosis. MRI also plays a great role in solving diagnostic problems caused by various forms of hepatic steatosis and fatty sparing on CT and ultrasonography.

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Department of Radiology, Hacettepe University School of Medicine, Ankara 06100, Turkey

Corresponding author. Tel.: +90 312 3051188; fax: +90 312 3112145.

PII: S0720-048X(06)00445-1

doi:10.1016/j.ejrad.2006.11.005

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