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Macrovesicular Hepatic Steatosis in Living Related Liver Donors: Correlation between CT and Histologic Findings¹

¹ From the Departments of Radiology (P.L., S.S.R., J.S., D.S.K.L.), Pathology (C.L.), Surgery (R.M.G., R.W.B.), and Digestive Diseases (S.S.), David Geffen School of Medicine at UCLA, 10833 Le Conte Ave, Los Angeles, CA 90095-1721. Received September 13, 2002; revision requested November 22; final revision received April 30, 2003; accepted May 20. Address correspondence to S.S.R. (e-mail: SRaman@mednet.ucla.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To assess degree of macrovesicular steatosis with unenhanced computed tomography (CT) and correlate it with histologic findings in potential donors for living related liver transplantation.

MATERIALS AND METHODS: Forty-two candidates underwent unenhanced CT within 4 weeks of core liver biopsy. An experienced liver pathologist, blinded to both CT and surgical findings, retrospectively reviewed biopsy specimens and determined degree of macrovesicular steatosis. A radiologist blinded to histologic grading calculated mean hepatic attenuation in each donor liver by averaging 25 region-of-interest (ROI) measurements on five sections (five ROIs per section). Mean splenic attenuation was calculated with three separate ROI measurements. Liver attenuation index (LAI) was derived and defined as the difference between mean hepatic and mean splenic attenuation. Body mass index (BMI) was determined for each patient. Linear regression analysis was used to correlate degree of macrovesicular steatosis with both LAI and BMI.

RESULTS: LAI correctly predicted degree of macrovesicular steatosis in 38 (90%) of 42 cases. In four of four livers, LAI below -10 HU correlated with greater than 30% macrovesicular steatosis (unacceptable for liver transplantation). In nine of 11 livers, LAI was between -10 and 5 HU and correctly predicted 6%–30% steatosis (relative contraindication). In two of 11 cases, LAI overestimated degree of hepatic steatosis. LAI above 5 HU correctly predicted 0%–5% steatosis in 25 of 27 livers. In two of 27 cases, parenchymal hemosiderin deposition led to an increase in LAI into the normal range, despite mild histologically confirmed steatosis. Degree of histologic macrovesicular steatosis correlated well with LAI (r = 0.92) and marginally with BMI (r = 0.45). Of 27 potential donors with normal livers at CT and acceptable LAI levels, four (15%) were deemed poor donor candidates because core biopsy revealed subtle hepatic necrosis and nonspecific hepatitis.

CONCLUSION: Although unenhanced CT quantifies the degree of macrovesicular steatosis relatively well, it may preclude a liver biopsy only in a small percentage of potential donors with low LAI (unacceptable degree of steatosis). Core liver biopsy is still necessary in the majority of donors with normal LAI to identify those with both fatty liver and coexistent hemosiderin deposition or radiologically occult diffuse liver diseases.

© RSNA, 2004

Index terms: Liver, CT, 761.12111, 761.12115 • Liver, fatty, 761.50 • Liver, transplantation

	INTRODUCTION

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Interest in living related liver transplantation has substantially increased in the United States in recent years, in part because of the shortage of cadaveric liver donors. However, careful donor selection must be performed to minimize risks of complications to both donor and recipient (1–3). Preoperative evaluation of hepatic steatosis, especially the macrovesicular subtype, is critical for donor selection (4–6). Severe macrovesicular steatosis (>60%) in the donor liver has been associated with a greater than 60% risk of primary nonfunction after transplantation. Moderate degrees of macrovesicular steatosis (30%–60%) in donor livers may also result in decreased hepatocyte regeneration and higher rates of graft dysfunction, nonfunction, and ischemic injury (7–9). The clinical importance of microvesicular steatosis is still controversial; however, most authors believe that it has less clinical importance than does the macrovesicular subtype (5,6,10). At our institution, donors with greater than 30% histologically determined macrovesicular steatosis are generally rejected because of these risks.

Macrovesicular hepatic steatosis, the most common cause of low-attenuating liver at computed tomography (CT), is linked to a variety of causes that include obesity; hyperlipidemia; and alcohol, steroid, and chemotherapeutic drug use. Although preoperative hepatic core biopsy is currently the standard method for accurate quantification and characterization of macrovesicular steatosis, it is invasive, is associated with risk, and contributes to overall cost and morbidity (11–15). Various unenhanced CT techniques have been proposed to help noninvasively determine the degree of hepatic macrovesicular steatosis (16–18). However, because of ethical considerations in obtaining specimens from a disease-free population, no study of a correlation between findings at unenhanced CT and the histologic degree of hepatic steatosis has been performed in normal subjects. Body mass index (BMI) has also been used to predict degree of macrovesicular steatosis although results vary (19). The purpose of our study was to assess degree of macrovesicular steatosis with unenhanced CT and correlate it with histologic findings in potential donors for living related liver transplantation.

	MATERIALS AND METHODS

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Patients
This study was approved by our institutional review board, which did not require informed consent. Between July 1993 and April 2002, 113 potential donors were evaluated for living related liver transplantation at our institution. Of these candidates, 50 potential donors underwent both unenhanced CT and core liver biopsy with a 16-gauge needle. Because of the potential for rapid change in the degree of hepatic steatosis, we included only those donors who underwent both CT and liver biopsy within 4 weeks of each other. Of the 50 potential donors, 42 satisfied our criteria and eight were excluded because the time between CT and liver biopsy exceeded the maximum 4-week interval. In eligible candidates, the mean age was 37.4 years, with a range of 21–57 years. These included 29 men (mean age, 36.7 years; SD, 9.66; range, 21–57 years) and 13 women (mean age, 39 years; SD, 7.39; range, 29–49 years). There were no statistically significant differences between both sex distributions (P = .45).

CT Imaging
In 15 donors, CT was performed with a single–detector row helical scanner (CT/i; GE Medical Systems, Milwaukee, Wis); in 27 donors, CT was performed with a multi–detector row helical scanner (LightSpeed Qx/i; GE Medical Systems). Contiguous transverse images were acquired through the liver with 10-mm collimation during a single breath hold without intravenous contrast agent administration prior to donor hepatic CT angiography. The unenhanced CT images were retrospectively reviewed with a picture archiving and communication system workstation (Radstation; UCLA) by a radiologist (P.L., S.S.R., D.S.K.L.) blinded to pathologic and surgical findings. For each case, the hepatic attenuation was measured by means of a random selection of 25 circular regions of interest (ROIs) on both lobes on five transverse sections at different hepatic levels (five ROIs per section). For each ROI, we selected the largest possible ROI and avoided areas of visible hepatic vascular and biliary structures to represent liver parenchymal attenuation. Our ROIs ranged from 200 to 400 mm². The ROI values were averaged as a mean hepatic attenuation. To provide an internal control, the mean splenic attenuation was also calculated by averaging three random ROI values of splenic attenuation measurement on three transverse sections at different splenic levels (one ROI per section). The largest possible ROI (size range, 200–400 mm²) was also selected to represent splenic parenchymal attenuation. The liver attenuation index (LAI), derived from the difference between mean hepatic attenuation and mean splenic attenuation, was used as a parameter for prediction of the degree of macrovesicular steatosis.

BMI Data
We assessed the utility of BMI, defined as donor weight (in kilograms) divided by height (in square meters), in the prediction of the degree of histologically determined steatosis. The BMI was available in 37 (88%) of 42 potential donors.

Histologic Analysis
All the histologic specimens were obtained by an experienced hepatologist during the living related liver transplantation preoperative evaluation. The specimens were obtained from a single biopsy of the right lobe by using a large 16-gauge biopsy needle (Klatskin; Becton Dickinson, Franklin Lakes, NJ), which provided the adequate hepatic specimens (at least 25 different portal triads for each specimen). An experienced liver pathologist (C.L.), blinded to radiologic and surgical findings, retrospectively reviewed the histologic findings of selected donor livers. The slides for histologic review were prepared with methods that included hematoxylin-eosin staining for routine histologic analysis and quantification of fat content, reticulin staining for identification of hemosiderin deposition and hepatocyte regeneration, and Masson trichrome staining for detection of fibrous tissue. The degree of macrovesicular steatosis was quantified on a percentage scale with estimation of the amount of liver parenchyma that was replaced by macrovesicular steatotic droplets. All estimates were performed twice for an entire biopsy specimen by using low-power microscopy (Olympus BX-40; Olympus America, Melville, NY).

Data and Statistical Analysis
The CT-derived LAI was plotted graphically as a function of the percentage of histologically confirmed macrovesicular steatosis. Ranges of values were evaluated for the LAI in an attempt to discriminate between the different extents of hepatic steatosis. The statistical correlation between LAI at CT and fat measurement at histologic analysis and between BMI and fat measurement at histologic analysis was established by using linear regression analysis.

	RESULTS

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The range of mean hepatic attenuation of potential living related donor livers was between 4 and 69 HU (mean, 55.5 HU). The mean splenic attenuation varied from 34 to 59 HU (mean, 50 HU). The LAI ranged from -47.4 to 22.7 HU (mean, 5.5 HU). The histologic degree of macrovesicular steatosis of potential donor livers ranged from 0% to 80% (mean, 10.7%). The correlation of the LAI with the degree of histologic macrovesicular steatosis of donor livers is demonstrated in Figure 1.

View larger version (20K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Graph demonstrates high degree of correlation between LAI on y axis as a function of percentage of histologically confirmed macrovesicular steatosis on x axis across a range of values.

View larger version (127K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. (a) Unenhanced transverse CT image obtained through the liver in a 30-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 9.3 HU, which represents a normal liver without substantial macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture without detectable macrovesicular steatosis. (Hematoxylin-eosin stain; original magnificiation, x100.)

View larger version (172K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. (a) Unenhanced transverse CT image obtained through the liver in a 30-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 9.3 HU, which represents a normal liver without substantial macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture without detectable macrovesicular steatosis. (Hematoxylin-eosin stain; original magnificiation, x100.)

View larger version (137K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. (a) Unenhanced transverse CT image obtained through the liver in a 46-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 7.4 HU, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture with 10% macrovesicular steatosis (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) Specimen shows moderate degree of hemosiderin deposition (arrows), which masks the degree of histologically confirmed steatosis. (Reticulin stain; original magnification, x200.)

View larger version (185K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. (a) Unenhanced transverse CT image obtained through the liver in a 46-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 7.4 HU, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture with 10% macrovesicular steatosis (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) Specimen shows moderate degree of hemosiderin deposition (arrows), which masks the degree of histologically confirmed steatosis. (Reticulin stain; original magnification, x200.)

View larger version (182K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. (a) Unenhanced transverse CT image obtained through the liver in a 46-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 7.4 HU, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture with 10% macrovesicular steatosis (arrows). (Hematoxylin-eosin stain; original magnification, x100.) (c) Specimen shows moderate degree of hemosiderin deposition (arrows), which masks the degree of histologically confirmed steatosis. (Reticulin stain; original magnification, x200.)

View larger version (131K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. (a) Unenhanced transverse CT image obtained through the liver in a 33-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 9.1 HU, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows widened portal triads at left (arrows), compatible with abnormal zones of hepatocyte regeneration as a subsequent result of hepatic necrosis. Normal portal triads are at right (arrowheads). (Reticulin stain; original magnification, x100.)

View larger version (165K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. (a) Unenhanced transverse CT image obtained through the liver in a 33-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 9.1 HU, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows widened portal triads at left (arrows), compatible with abnormal zones of hepatocyte regeneration as a subsequent result of hepatic necrosis. Normal portal triads are at right (arrowheads). (Reticulin stain; original magnification, x100.)

View larger version (123K): [in this window] [in a new window] [Download PPT slide]   Figure 5a. (a) Unenhanced transverse CT image obtained through the liver in a 51-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 8.4, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows inflammatory cells (arrows) infiltrating the portal triads, compatible with mild hepatitis. (Hematoxylin-eosin stain; original magnification, x200.)

View larger version (159K): [in this window] [in a new window] [Download PPT slide]   Figure 5b. (a) Unenhanced transverse CT image obtained through the liver in a 51-year-old male potential liver donor demonstrates a liver with normal attenuation. LAI is 8.4, which represents a normal liver without marked macrovesicular steatosis. (b) Corresponding histologic specimen shows inflammatory cells (arrows) infiltrating the portal triads, compatible with mild hepatitis. (Hematoxylin-eosin stain; original magnification, x200.)

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 6a. (a) Unenhanced transverse CT image obtained through the liver in a 44-year-old male potential liver donor demonstrates a liver with diffuse decreased hepatic attenuation, which suggests steatosis. Central hepatic vessels cannot be appreciated. LAI is 3.8 HU, which represents 6%-30% macrovesicular steatosis. (b) Histologic specimen shows normal architecture with moderate steatosis of 30%. (Hematoxylin-eosin stain; original magnification, x100.)

View larger version (178K): [in this window] [in a new window] [Download PPT slide]   Figure 6b. (a) Unenhanced transverse CT image obtained through the liver in a 44-year-old male potential liver donor demonstrates a liver with diffuse decreased hepatic attenuation, which suggests steatosis. Central hepatic vessels cannot be appreciated. LAI is 3.8 HU, which represents 6%-30% macrovesicular steatosis. (b) Histologic specimen shows normal architecture with moderate steatosis of 30%. (Hematoxylin-eosin stain; original magnification, x100.)

View larger version (130K): [in this window] [in a new window] [Download PPT slide]   Figure 7a. (a) Unenhanced transverse CT image obtained through the liver in a 43-year-old female potential liver donor demonstrates a liver with markedly decreased attenuation, even lower than the attenuation of the central hepatic vessels. LAI is -47.4 HU, which represents greater than 30% macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture with severe steatosis (80%). (Hematoxylin-eosin stain; original magnification, x100.)

View larger version (162K): [in this window] [in a new window] [Download PPT slide]   Figure 7b. (a) Unenhanced transverse CT image obtained through the liver in a 43-year-old female potential liver donor demonstrates a liver with markedly decreased attenuation, even lower than the attenuation of the central hepatic vessels. LAI is -47.4 HU, which represents greater than 30% macrovesicular steatosis. (b) Corresponding histologic specimen shows normal architecture with severe steatosis (80%). (Hematoxylin-eosin stain; original magnification, x100.)

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
It has been well recognized since the late 1970s that unenhanced CT is useful for detection of hepatic macrovesicular steatosis (16,17). Piekarski et al (16) reported the utility of the difference between liver and spleen CT numbers in the prediction of hepatic steatosis, although no pathologic quantification of hepatic steatosis was provided. We created the term liver attenuation index, or LAI, to describe the difference between the mean hepatic and the mean splenic CT attenuation. We have shown that this simple unenhanced CT–derived calculation provides a reasonable estimate of diffuse hepatic steatosis over a wide range (0%–80%) of histologically confirmed macrovesicular steatosis.

Although unenhanced CT provided a reasonable assessment of hepatic steatosis, liver biopsy is still necessary in donors with a normal LAI to identify those with coexistent fat and hemosiderin deposition or radiologically occult disease. In our series, although 36 (86%) of 42 donor livers with normal LAI were histologically normal, in six (14%) of 42 cases, radiologically occult conditions were detected only at histologic analysis; the finding of these conditions prompted a substantial change in clinical management. In two cases, we encountered 10% histologic macrovesicular steatosis coexisting with a mild-to-moderate degree of hemosiderin deposition, which resulted in a spurious elevation of the LAI into the normal range. Although the degree of hemosiderin deposition in these donor livers was not itself a contraindication for liver transplantation, it precluded an accurate noninvasive assessment of macrovesicular steatosis, which would have contraindicated living related liver donation. This phenomenon was recognized in an early report (16) and continues to be a limitation of sole reliance on CT attenuation. In four other cases, living related donor livers without marked macrovesicular steatosis had subtle histologic liver damage that was undetected at clinical examination and with serum markers and multiphasic CT. These subtle pathologic abnormalities include hepatic necrosis with hepatocyte regeneration and/or a mild degree of hepatitis. At further clinical review of these donors, no specific cause of liver damage was uncovered. However, these histologic findings precluded the use of these organs for living related liver transplantation. In our series, if we relied only on CT-derived LAI data in surgical donor candidates, we would miss important subclinical diffuse liver disease in 14% of donor livers, thus increasing the risk of potential posttransplantation complications. We therefore recommend reliance solely on imaging findings, including CT-derived LAI data only to eliminate potential liver donors with moderate-to-severe hepatic steatosis (ie, histologic steatosis > 30% and LAI < -10 HU). Because of the reliability of CT in the detection of steatosis, this group of potential donors may be spared the added risk of hepatic biopsy. Potential living related donors cleared for surgery with otherwise normal CT scans (ie, including LAI levels -10 HU) should undergo core biopsy to exclude clinically and radiologically occult diffuse liver diseases.

The BMI, a gross summary of overall body habitus, was reported as a good predictor of hepatic steatosis in potential living related donors, with a significant correlation (r = 0.49) (19). Although we found a similar correlation in our study between BMI of living related donors and degree of macrovesicular steatosis (r = 0.45), BMI was a much less powerful indicator when it was compared with the CT-derived LAI (r = 0.92). For pretransplantation evaluation of macrovesicular steatosis, BMI should be supplemented with CT evaluation and, if necessary, liver biopsy for an adequate work-up.

Limitations of this study include possible population bias toward a cohort of individuals considering living related liver donation, small sample size, wide range of time between liver biopsy and CT scanning, and variability in assessment of the CT attenuation value with two different CT scanners. Further, the liver biopsy specimens were acquired only from the right hepatic lobe, whereas the mean hepatic attenuation was acquired from 25 ROIs of both hepatic lobes. Although other CT-based methods of assessment for hepatic steatosis (16,17) were not reviewed, the additional information uncovered at liver biopsy would apply to these techniques as well.

In summary, the LAI from an unenhanced CT scan closely predicts a range of histologic macrovesicular steatosis in potential liver donors. We believe the LAI may preclude a liver biopsy only in the small percentage of potential hepatic donors who have low LAI (ie, unacceptable degrees of steatosis). However, to avoid missing subclinical and radiologically occult conditions, a core liver biopsy should be performed in donors cleared with imaging and other noninvasive criteria for living related liver transplantation.

	ACKNOWLEDGMENTS

 
The authors thank Julia Fendrick, BA, for her invaluable assistance in grammatical review and formatting of the manuscript.

	FOOTNOTES

 
Abbreviations: BMI = body mass index, LAI = liver attenuation index, ROI = region of interest

Author contributions: Guarantors of integrity of entire study, S.S.R., D.S.K.L.; study concepts and design, S.S.R., D.S.K.L.; literature research, P.L., S.S.R.; clinical studies, R.M.G., R.W.B., S.S., C.L., P.L.; data acquisition, P.L.; data analysis/interpretation, P.L., D.S.K.L.; statistical analysis, J.S.; manuscript preparation and definition of intellectual content, P.L., S.S.R.; manuscript editing and revision/review, P.L., S.S.R., D.S.K.L.; manuscript final version approval, D.S.K.L.

	REFERENCES

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