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Gastrointestinal Imaging |
1 From the Departments of Radiology (B.S.K., T.K.K., M.G.L., J.H.K., K.W.K., K.B.S., P.N.K., H.K.H.), Pathology (J.S.K.), and Surgery (S.G.L.), Asan Medical Center, University of Ulsan, Seoul, Korea; and Department of Information and Statistics, Daejeon University, Korea (W.K.). Received March 24, 2003; revision requested June 18; final revision received October 28; accepted December 18. Address correspondence to T.K.K., Department of Medical Imaging, Toronto General Hospital, 200 Elizabeth St, Toronto, ON, Canada M5G 2C4 (e-mail: taekyoung.kim@uhn.on.ca).
| ABSTRACT |
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MATERIALS AND METHODS: Forty-eight patients underwent two-phase (hepatic arterial phase and portal venous phase [PVP]) CT at 1, 2, and 4 weeks after LDLT. Images were evaluated for hepatic attenuation difference in areas of hepatic venous congestion, opacification of hepatic and peripheral portal veins in those areas, and changes in findings at follow-up CT. CT findings were correlated with serum bilirubin level. Fisher exact test and mixed model were applied. Histopathologic specimens were obtained in six patients.
RESULTS: Thirty patients (62%) had attenuation difference in segments V and VIII of right lobe transplant at initial CT scanning. Opacification of hepatic or peripheral portal veins was seen in 17 (63%) and 27 (100%) hyperattenuating areas of congestion during PVP and in none and three (19%) of 16 hypoattenuating areas, respectively. At 4-week follow-up CT, attenuation difference decreased in volume in 11 of 16 patients with hypoattenuation during PVP. All 14 patients with hyperattenuation showed no change in volume, but attenuation difference had decreased or disappeared. Histopathologic specimens showed evidence of hepatic venous congestion in all six patients. Hypoattenuation was seen at PVP CT in all three patients with severe hepatic venous congestion at histopathologic examination. Serum bilirubin level was significantly different between patients with hypoattenuation and those with hyperattenuation during PVP (P = .035) and between patients with hypoattenuation and those without attenuation difference (P = .009).
CONCLUSION: Areas possibly related to hepatic venous congestion after LDLT have variable attenuation at CT; decreased enhancement during PVP correlates with increased postoperative serum bilirubin level, which indicates severity of hepatic venous congestion.
© RSNA, 2004
Index terms: Hepatic veins, stenosis or obstruction, 959.1242, 959.99 Liver, blood supply, 957.1242, 959.1242 Liver, CT, 761.12115 Liver, transplantation, 761.458
| INTRODUCTION |
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However, because the hepatic venous outflow from liver segments V and VIII of the right lobe usually drains into the middle hepatic vein, right lobe harvest without the middlehepatic vein may produce varying degrees of hepatic venous congestion in segments V and VIII of the transplanted liver (2,4,5). Similarly, hepatic venous congestion may occur in segments VI and VII of the right lobe graft because of the ligation or anastomotic stenosis of the right inferior accessory hepatic vein (2,6).
Several studies have been performed to evaluate hemodynamic alteration after hepatic venous occlusion (710). To our knowledge, however, investigators in previous studies have not documented findings of acute hepatic venous congestion at two-phase computed tomography (CT) with intravenous contrast material injection in transplanted liver after LDLT with a right lobe graft. Thus, the purpose of the present study was to describe and determine the clinical importance of two-phase CT findings of hepatic venous congestion following LDLT with right lobe graft.
| MATERIALS AND METHODS |
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A total of 48 patients were thus included in this study. There were 43 men and five women with an age range of 1957 years (mean age, 44 years). Of the 48 patients, one man had a history of cardiac disease. He had coronary artery disease, which had been treated by means of percutaneous transluminal angioplasty. This patient had cardiac functional capacity of grade I according to New York Heart Association criteria in preoperative evaluation. The hepatic veins from segments V and VIII of the right lobe graft were either ligated (n = 8) or anastomosed to the sidewall of the inferior vena cava by using an interposition vein graft (n = 40) according to vein sizes. Right inferior accessory hepatic veins were present in 21 grafts and were ligated or anastomosed to the inferior vena cava in four and 17 cases, respectively. In all cases, two-phase CT scanning was performed during the hepatic arterial phase (HAP) and portal venous phase (PVP) at 1, 2, and 4 weeks after surgery.
Institutional review board approval and informed consent were not required for this retrospective study.
CT Scanning and Interpretation
CT scans were obtained with a Somatom Plus-4 (n = 35) or Plus-S scanner (n = 13) (Siemens, Erlangen, Germany). Each patient received 100120 mL of iopromide (Ultravist 370; Schering, Berlin, Germany) through an 18-gauge 32-mm-long angiographic catheter inserted in a forearm vein by using a mechanical injector (LF CT 9000; Liebel-Flarsheim, Cincinnati, Ohio) at a rate of 3 mL/sec. Scans were obtained with the following parameters: 20-second acquisition time, 810-mm collimation, 810-mm reconstruction interval, 1:1 table pitch, 210250 mA, and 120 kV. HAP and PVP scans were obtained 30 and 70 seconds after the initiation of contrast material injection. Each spiral acquisition through the liver was accomplished with breath holding.
CT scans were analyzed retrospectively by two experienced abdominal radiologists (B.S.K., T.K.K.) in consensus for the presence and distribution of hepatic attenuation differences in the areas of hepatic congestion, opacification of the hepatic veins and peripheral portal veins in those areas, and changes of these findings on follow-up CT scans. The two reviewers had 5 and 10 years of experience in abdominal imaging. The hepatic attenuation difference related to hepatic congestion at CT was determined by means of typical anatomic distribution that corresponds to the area of middle hepatic vein drainage (defined as where the straight border of the involved hepatic parenchyma intersects the anterior segmental branch of the portal vein and the vertex of the wedge-shaped area of hepatic attenuation difference points to inferior vena cava [7,11]).
We compared the frequency of hepatic attenuation difference according to surgical technique (ligation vs anastomosis) for the hepatic veins from segments V and VIII of the right lobe graft. In addition, we evaluated the fluid collections for location, size, grade of hepatic surface compression (apparent, subtle, or absent), and presence of hepatic attenuation difference because fluid collections can alter hepatic enhancement by compressing adjacent liver parenchyma. To determine the presence or absence of hepatic attenuation difference between normal and congested liver parenchyma, the two radiologists (B.S.K., T.K.K.) interpreted the CT images in consensus with a picture archiving and communication system workstation with Radipia software (HyundaeTech, Seoul, Korea). A 21-inch monitor was used with a resolution of 2,048 x 2,560 bit pixels (BACCO; Dataray, Denver, Colo) with free adjustment of the window width and level.
Histopathologic Findings
Correlative histopathologic findings were available in six patients who underwent percutaneous liver biopsy with an 18-gauge needle to confirm hepatic venous congestion and to evaluate the severity in the areas of hepatic attenuation difference at CT. Liver biopsy was performed only in selected patients who were suspected of having severe hepatic venous congestion on the basis of clinical features and CT findings.
Clinical features suggestive of severe hepatic venous congestion included persistent abnormal liver function tests, hepatic swelling, persistent ascites, and pleural effusion. Biopsy was performed within 2 months (mean interval, 21 days) after LDLT. Each specimen was reviewed by a pathologist (J.S.K.) for the evidence of centrilobular congestion and damage. The pathologist had 10 years of experience in the field of pathology. The diagnosis of hepatic venous congestion was made on the basis of dilatation of central veins and sinusoids. Severity of hepatic venous congestion was graded as mild, moderate, or severe (12,13).
Laboratory Findings
Laboratory findings were reviewed retrospectively in the patients medical records. The serum total bilirubin level was used to evaluate the metabolic capability of the graft. CT findings were correlated with the serum bilirubin level.
Statistical Analysis
The Fisher exact test was used to compare the frequency of hepatic attenuation difference according to surgical technique. Statistical analysis was performed by using a mixed model of SAS software release 8.3 (SAS Institute, Cary, NC) to compare serum bilirubin levels with CT findings because the data were collected repeatedly along the timetable for each subject. A P value of less than .05 indicated a statistically significant difference. Statistical analysis did not adjust for age- and sex-related differences because with the Wilcoxon rank sum test, there were no statistically significant differences between age distributions according to patient sex (mean age in men, 43.7 years ± 7.9 [SD]; mean age in women, 45.6 years ± 7.9; P = .853).
| RESULTS |
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The results of the comparison of frequency of hepatic attenuation difference according to the surgical technique during the PVP are shown in Table 3. There was no statistically significant difference in frequency of hepatic attenuation difference between the groups in which ligation had been performed versus anastomosis to the sidewall of the inferior vena cava for the hepatic veins from segments V and VIII of the right lobe graft (P = .451).
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Biopsy results showed evidence of hepatic venous congestion in all six patients (severe in three, moderate in two, and mild in one). Four biopsy specimens in which there were three severe grades and one moderate grade of hepatic venous congestion also showed centrilobular damage (Fig 6). Hypoattenuating areas were seen at PVP CT in all three patients with severe hepatic venous congestion at histopathologic examination. Among the two patients with moderate hepatic congestion, one patient with centrilobular damage showed hypoattenuation with a surrounding hyperattenuating area, and the other showed hyperattenuation at PVP CT. In one patient with mild hepatic venous congestion, a hyperattenuating area was seen at PVP CT.
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| DISCUSSION |
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CT yields important information about the transplanted liver. The CT finding of hepatic attenuation difference that corresponds to the area of middle hepatic venous drainage has been considered to indicate hepatic venous congestion. Our study shows that the CT appearance of hepatic attenuation difference is variable and probably depends on severity and duration of hepatic venous congestion on the basis of the facts obtained from the opacification of hepatic veins and peripheral portal veins, follow-up CT, histopathologic examination, and serial serum total bilirubin level.
In our experience, the congested area of liver transplant has been seen most commonly as hypoattenuation at HAP CT. This result was different from that of previous studies, which showed that the arterial flow increases in the segment of hepatic vein occlusion at CT during hepatic arteriography (7). Because the area was always seen as hypoattenuating before the injection of contrast material, we assumed that hypoattenuation of the congested area of liver transplant during the HAP might be caused by lymphatic edema and increased interstitial fluid as a result of congestion (15) and that arterial hyperperfusion might have made a minor contribution to the enhancement.
Also, while the results of previous experimental studies showed that complete occlusion of the hepatic vein produces an increase in the sinusoidal pressure and reverses the pressure gradient between the sinusoid and portal vein and thereby produces hypoattenuation at CT during arterial portography (7,8), in our experience, the congested area showed variable findings at PVP CT. It was most commonly seen as diffuse hyperattenuation and was also commonly seen as hyperattenuation surrounding a hypoattenuating area.
Although the cause of hyperattenuation during the PVP is not clearly understood, opacification of the hepatic vein branches is commonly seen, and the peripheral portal branches are invariably enhanced in the hyperattenuating area. These findings suggest that hyperattenuation of the congested area on PVP CT images is not caused by complete hepatic venous obstruction but is most likely caused by partial obstruction. We assume that if partial hepatic venous obstruction induces insufficient increase in the sinusoidal pressure to reverse the pressure gradient between the sinusoid and portal vein, there might be a somewhat decreased but persistent inflow of portal venous blood and that the stasis and the accumulation of contrast material in the hepatic sinusoid might effect diffuse homogenous enhancement in segments V and VIII of the transplanted liver during the PVP. The area showed no shrinkage in volume, and the attenuation differences decreased or disappeared at 4-week follow-up CT. It is assumed to be caused by the reestablishment of hepatic vein drainage through the intrahepatic collateral vessels. Clinically, the transplants had a good prognosis, and no additional management was required.
On the other hand, hypoattenuating congested areas indicated severe hepatic venous congestion. There was a low incidence of enhancement of hepatic vein branches or peripheral portal branches in the hypoattenuating congested areas, and the areas had usually become atrophied by the time of 4-week follow-up CT. In histopathologic specimens obtained in six patients, these areas showed severe distention of the central vein and vascular sinusoids of centrilobular zone and centrilobular damage. Some reports showed that advanced and prolonged hepatic congestion could induce fibrosis in the centrilobular regions, resulting in cirrhotic change (12,13).
Persistent hyperbilirubinemia during the 2nd week after surgery was observed in patients with hypoattenuating congested areas. Therefore, it is assumed that severe hepatic venous congestion may induce deterioration of the metabolic capacity of the liver transplant and result in destruction of the hepatic parenchyma. The reduction of viable hepatic parenchyma in graft liver may lead to lower graft survival, probably because of enhanced parenchymal cell injury, and to reduced metabolic and synthetic capacities (16). In this regard, we speculate that the detection of severe hepatic congestion at CT may have a substantial effect on clinical outcome. We believe that these CT findings in patients who underwent LDLT with hepatic venous congestion may be applied to other situations, such as in that of an LDLT donor undergoing extended left lobectomy or in patients undergoing hepatic vein reconstruction after hepatic tumor removal (17).
Severe extrinsic compression of the liver can be included as a rare cause of hepatic hemodynamic alteration (18,19). Fluid collection often occurs after LDLT, from which this focal compression may cause focal increase in tissue pressure at the subcapsular region, resulting in decreased portal perfusion and altering hepatic enhancement. However, some features can aid in differentiation of hepatic attenuation difference caused by extrinsic compression from hepatic venous congestion. Alteration of hepatic enhancement at compressed parenchyma adjacent to a fluid collection can be considered hepatic attenuation difference caused by extrinsic compression. It usually disappears at repeat CT examination after a drainage procedure is performed.
The hepatic attenuation difference in transplanted liver might also be related to differences in the surgical procedure used with the free edge of the transplant and to manipulation of hepatic arterial variants during surgery. The manipulation, cauterization, and retraction of the free edge of the transplant might cause a small region of low attenuation at the surgical margin, which could be suggested by intermittent thin lesion that conforms to the shape of that margin in a nonanatomic distribution (20). Diminished hepatic arterial flow may occur during manipulation of hepatic arterial variants at surgery. A decrease in hepatic arterial flow possibly affects hepatic attenuation difference during the HAP but not during the PVP because it does not cause an increase in portal flow, and the acute obstruction of peripheral arterial flow induces no recognizable flow change of portal blood flow (21).
We recognize that our study has specific limitations. First, definitive proofthat is, pathologic evidencewas not obtained in all patients with hepatic venous congestion. However, we believe that it might not be possible to perform biopsy in all patients from an ethical point of view. Moreover, considering the fact that hepatic attenuation difference in segments V and VIII had typical distribution of middle hepatic venous territory intersected by the anterior segmental branch of the portal vein, we believe that the hepatic attenuation difference represents hepatic venous congestion. Second, our study was only a retrospective analysis. We believe that further prospective blinded studies might be needed to support reliability of data in the retrospective review.
Third, our study design involved only consensus interpretation. It would have been helpful to interpret CT images independently to determine how consistently hepatic attenuation difference can be recognized, and it might have improved reliability of our results. Fourth, a fixed delay time in our study could sometimes have an influence on perception of hepatic attenuation difference caused by individual varying transit times. With an automatic bolus-tracking method or test bolus technique, biphasic helical CT might be optimized for most patients, regardless of individual variability (2225).
In conclusion, two-phase CT of patients with hepatic venous congestion who underwent LDLT may show variable findings of attenuation and morphologic changes of the liver, depending on the severity and stage of the obstruction. Hepatic enhancement patterns that may be related to hepatic venous congestion correlate with postoperative bilirubin levels. Decreased enhancement in the area of middle hepatic venous drainage in segments V and VIII during the PVP suggests the possibility of severe hepatic venous congestion.
| ACKNOWLEDGMENTS |
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| FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, T.K.K., B.S.K.; study concepts and design, T.K.K., B.S.K.; literature research, J.H.K., J.S.K., K.W.K.; clinical studies, S.G.L.; data acquisition, J.H.K., M.G.L., J.S.K., W.K., S.G.L.; data analysis/interpretation, B.S.K., T.K.K., J.S.K.; statistical analysis, W.K.; manuscript preparation, B.S.K.; manuscript definition of intellectual content, J.H.K., M.G.L., P.N.K., K.B.S., K.W.K., H.K.H.; manuscript editing, H.K.H., T.K.K., K.W.K., M.G.L., W.K., J.S.K., K.B.S., P.N.K.; manuscript revision/review, T.K.K., H.K.H., K.B.S., P.N.K., S.G.L., W.K.; manuscript final version approval, T.K.K., B.S.K., J.S.K., H.K.H., M.G.L., K.B.S.
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