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Original Research |
1 Department of Radiology and Research Institute of Radiology, Asan Medical
Center, University of Ulsan College of Medicine, 388-1, Pungnap-2 dong,
Songpa-ku, Seoul 138-736, Korea.
2 Department of Surgery, Asan Medical Center, University of Ulsan College of
Medicine, Seoul, Korea.
Received July 5, 2007;
accepted after revision October 7, 2007.
Address correspondence to K. W. Kim
(kimkw{at}amc.seoul.kr).
Abstract
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SUBJECTS AND METHODS. Doppler sonography examinations were prospectively performed in 54 patients within 24 hours after living donor liver transplantation with a modified right lobe graft in which large (> 5 mm) middle hepatic vein (MHV) tributaries were reconstructed. The number, flow direction, and waveform of the MHV tributaries; the echogenicity of the surrounding parenchyma; and the flow direction of the corresponding portal branch were evaluated. Hepatic venous congestion was diagnosed when there was no color flow or a monophasic waveform of an MHV tributary. The sensitivity of Doppler sonography for the detection of MHV tributaries was assessed using donors' preoperative CT scans and surgical records as references. The diagnostic values of Doppler sonography for hepatic venous congestion were assessed using recipients' postoperative CT scans as references. Differences in prevalence of Doppler sonography findings between the group with hepatic venous congestion and the non–hepatic venous congestion group were assessed.
RESULTS. Doppler sonography enabled us to identify 90% (155/173) of all and 98% (129/131) of the large MHV tributaries. The sensitivity and specificity of Doppler sonography for hepatic venous congestion were 90% (28/31) and 77% (96/124), respectively, for all and 88% (15/17) and 85% (95/112), respectively, for large MHV tributaries. Parenchymal hyperechogenicity was more commonly seen in the hepatic venous congestion group (65%, 20/31) than in non–hepatic venous congestion group (6%, 7/124) (p < 0.01). All five MHV tributaries with reversed flow were seen in the non–hepatic venous congestion group. All five portal branches with hepatofugal flow were seen in the hepatic venous congestion group.
CONCLUSION. Doppler sonography provides a reliable noninvasive surveillance tool for hepatic venous congestion in a modified right lobe graft during the early postoperative period after living donor liver transplantation.
Keywords: Doppler sonography • hepatic venous congestion • hepatocellular carcinoma • living donor liver transplantation • modified right lobe graft
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The paramedian sector of the anterior segment of a right lobe graft is inherently prone to congestion because the middle hepatic vein (MHV), a major draining vein of the right lobe anterior segment paramedian sector, is usually left in the donor for his or her safety [3, 4]. Because the establishment of optimal hepatic venous outflow is the key to a successful outcome of living donor liver transplantation [3], there has been emerging interest in hepatic venous congestion in the paramedian sector of the right lobe graft after living donor liver transplantation. Recently, various methods of surgical reconstruction of the MHV using an interposition vein graft have been advocated to achieve optimal hepatic venous outflow of the paramedian sector in living donor liver transplant recipients using a modified right lobe graft [5–9]. Although the indication for reconstruction of the MHV is still debated [10–13], in our institution the MHV tributaries in the anterior segment of the modified right lobe graft are routinely reconstructed if they are larger than 5 mm in diameter. However, compared with the recent surgical interest and investigations designed to prevent hepatic venous congestion in the paramedian sector of right lobe grafts or in modified right lobe grafts after living donor liver transplantation, relatively little attention has been given to postoperative radiologic surveillance for hepatic venous congestion in this area.
Doppler sonography is generally regarded as the primary technique for vascular sur veillance after living donor liver trans plantation. However, there may be some concern regarding the value of Doppler sonography for the diagnosis of hepatic venous congestion in the paramedian sector of a right lobe graft or in a modified right lobe graft because the MHV tributaries have smaller diameters than the right hepatic vein (RHV). Although it has been shown that hepatic venous congestion may produce various abnormalities on Doppler sonography after living donor liver transplantation using a modified right lobe graft [14], the value of Doppler sonography for the diagnosis of hepatic venous congestion in the paramedian sector of a right lobe graft or in a modified right lobe graft after living donor liver transplantation has not been determined.
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Patients
Among 78 consecutive patients who underwent liver transplantation at our
hospital during the 4-month period between December 2004 and March 2005, 74
patients underwent living donor liver transplantation and four patients
underwent whole-liver transplantation from deceased donors. Of the 74 living
donor liver transplantation patients, 11 patients with dual grafts and nine
patients with left lobe grafts were excluded, and the other 54 consecutive
patients who underwent living donor liver transplantation using modified right
lobe grafts, in which MHV tributaries larger than 5 mm in diameter were
reconstituted using an interposition vein graft, were included in our
study.
The study group of transplant recipients was composed of 39 men (mean age ± SD, 48.4 ± 8.3 years; age range, 23–61 years) and 15 women (48.9 ± 11.8 years; 22–62 years). The most common underlying disease necessitating liver transplantation was liver cirrhosis associated with hepatitis B or C virus (n = 27), followed by hepatocellular carcinoma (n = 19), acute fulminant hepatitis (n = 4), alcoholic liver cirrhosis (n = 2), primary biliary cirrhosis (n = 1), and cholangiocarcinoma (n = 1). The corresponding 54 donors included 38 males (mean age ± SD, 28.9 ± 9.5 years; age range, 16–58 years) and 16 females (30.8 ± 10.0 years; 16–52 years).
Preoperative CT in Donors
In all 54 donors, CT scans were obtained using a 16-MDCT scanner
(LightSpeed 16, GE Healthcare). After unenhanced CT scans were obtained, 150
mL of iopromide (Ultravist 370, Bayer HealthCare) was administered at a rate
of 3 mL/s using a mechani cal injector. Biphasic CT was then per formed during
the hepatic arterial phase (HAP) and the portal venous phase (PVP). By means
of a bolus-tracking method (SmartPrep, GE Healthcare), HAP scanning was
initiated 10 seconds after enhancement of the descending aorta reached 100 H.
PVP scanning was performed at a fixed scanning delay of 72 seconds.
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MHV Reconstruction in Transplant Recipients
During the living donor liver transplantation surgery, MHV reconstruction
was performed using various types of autogenous or cryopreserved cadaveric
veins as interposition vein grafts. MHV tributaries were routinely anastomosed
to the interposition vein graft if they were larger than 5 mm in diameter.
Each MHV tributary was categorized as being large if it was reconstructed or
as being small if it was seen on the donor's preoperative CT examination but
was ligated during surgery.
Prospective Postoperative Doppler Sonography in Recipients
Doppler sonography was routinely performed in all 54 recipients on
postoperative day 1 using a scanner with a 1-4–MHz transducer (Sequoia
512, Acuson). All examinations were performed by a board-certified abdominal
radiologist with 4 years of experience performing Doppler sonography
surveillance for postoperative vascular complications after living donor liver
transplantation. The radiologist was unaware of the donor information.
Patients were placed in the supine position with their heads elevated and
right arms abducted, and the examinations were performed without
breath-holding because these patients were usually short of breath immediately
after surgery. The entire examination was performed under aseptic
conditions.
Sonograms were always obtained using oblique intercostal scanning because it was the only available sonic window during the immediate postoperative period. On gray-scale sonography, the number and diameters of MHV tributaries found and the echogenicity of their territory relative to the posterior segment of the modified right lobe graft were recorded. Color and spectral Doppler sonography examinations of MHV tributaries were performed to assess the presence or absence of blood flow, direction of blood flow, and spectral Doppler waveform and the presence of intrahepatic collaterals. The velocity scale was individually adjusted; when there was no color signal with the velocity scale reduced to ± 8.6 cm/s, it was defined as "no Doppler-detectable blood flow" [15, 16]. When the flow of the MHV tributaries was directed to an interposition vein graft, it was considered normal flow direction. When the flow of the MHV tributaries was directed away from an interposition vein graft, it was considered reversed flow direction.
We classified the hepatic vein wave into one of three patterns—triphasic, biphasic, or monophasic. A triphasic wave consisted of two forward peaks with a short period of reversed flow at the end of the second forward wave. The monophasic wave was defined as the loss of the normal periodic pulsatility of the hepatic vein and a continuous flat wave. The biphasic wave was defined as the loss of reversed flow and obscured two forward flow peaks but preservation of hepatic vein pulsatility. Color and spectral Doppler waves of the portal branch corresponding to each MHV tributary were also obtained to assess the direction of portal flow—that is, hepatofugal or hepatopetal—in those segments.
On Doppler sonography, hepatic venous congestion was diagnosed when there was no Doppler-detectable blood flow or a monophasic waveform in an MHV tributary [14–17].
Postoperative CT and Venography in Recipients
Postoperative CT scans were obtained in all 54 recipients from 1 to 12 days
(mean ± SD, 4.2 ± 2.6 days) after living donor liver
transplantation. The time interval between Doppler sonography and CT was
between 0 and 11 days (3.2 ± 2.6 days). CT scans were obtained using a
16-MDCT scanner (Somatom Sensation 16, Siemens Medical Solutions). The method
of IV contrast injection and the scanning time were the same as those used for
preoperative CT of the donors. Bolus tracking was performed (CARE-Bolus,
Siemens). The scanning and reconstitution parameters were as follows: detector
configuration of 1.5 mm x 16 (unenhanced scan) or 0.75 mm x 16
(HAP and PVP scans), table feed of 24 mm (unenhanced scan) or 12 mm (HAP and
PVP scans) per gantry rotation, gantry rotation time of 0.6 second, 200
effective mAs, 120 kVp, and a slice thickness and interval of 5 mm (unenhanced
and PVP scans) or 3 mm (HAP scan).
CT scans were analyzed by a board-certified abdominal radiologist for the presence and distribution of hepatic attenuation differences in the anterior segment compared with the posterior segment of the modified right lobe graft. Opacification of the MHV tributaries and the interposition vein graft was also evaluated. On CT, hepatic venous congestion was diagnosed when the hepatic parenchyma of the typical anatomic distribution corresponding to the drainage areas of the MHV tributaries was seen as having persistent low attenuation on unenhanced, HAP, and PVP scans with no opacification of the MHV tributaries [18]. Each MHV tributary was subsequently categorized into either the hepatic venous congestion group or the non–hepatic venous congestion group according to the CT findings.
The clinical indication for hepatic venography was suspicion of hepatic outflow obstruction—that is, unexplained ascites, abnormal liver enzyme levels, or both after excluding problems of hepatic inflow (hepatic artery and portal vein) on an imaging study such as Doppler sonography or CT. The time interval between Doppler sonography and venography was from 0 to 7 days (mean ± SD, 2.6 ± 3.5 days). In all patients, the right internal jugular vein was punctured, and selective hepatic venograms of 24 MHV tributaries were obtained using a 5-French C3 catheter (Torcon NB Advantage Catheter, Cook). The pressure gradient between the MHV tributaries and the inferior vena cava across the interposition vein graft was obtained in selected cases when venograms showed stenosis at the anastomosis. On venography, obstruction of an MHV tributary was diagnosed when there was a thrombotic occlusion or severe narrowing at the anastomosis with a pressure gradient of 6 mm Hg or more [19–21].
Statistical Analyses
Using donors' preoperative CT scans and surgical records as a standard of
reference of the number and size of MHV tributaries, the sensitivity of
Doppler sonography for the detection of MHV tributaries in modified right lobe
grafts immediately after living donor liver transplantation was assessed. For
MHV tributaries found on Doppler sonography, the diagnostic values of this
examination for detecting hepatic venous congestion were assessed using
recipients' postoperative CT scans as a standard of reference in all patients,
and when venography was available, venographic information was also used as
the reference. Fisher's exact test was used to ascertain whether there were
differences between the hepatic venous congestion group and the
non–hepatic venous congestion group regarding the prevalence of the
following gray-scale and Doppler sonography findings: hyperechogenicity in
corresponding territories compared with the posterior segment of the modified
right lobe graft, reversed flow of MHV tributaries, and reversed flow of the
corresponding portal branch. Significance was indicated if a two-tailed
p value was less than 0.05. Statistical analyses were performed with
commercially available statistics software (SPSS version 12.0, SPSS) for
Windows (Microsoft).
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Of 129 large MHV tributaries found on Doppler sonography, 17 belonged to the hepatic venous congestion group and 112 to the non–hepatic venous congestion group. On Doppler sonography, diagnosis of hepatic venous congestion was made in 32 MHV tributaries based on the absence of Doppler-detectable blood flow in 24 (75%) or monophasic waveform in eight (25%). The sensitivity and specificity of Doppler sonography for hepatic venous congestion in the large MHV tributaries were 88% (15/17) and 85% (95/112), respectively.
For 24 large MHV tributaries in which venographic information was available, Doppler sonography produced a sensitivity, specificity, accuracy, positive predictive value, and negative predictive value of 100% (9/9), 93% (14/15), 96% (23/24), 90% (9/10), and 100% (14/14), respectively.
On gray-scale sonography, hepatic parenchymal echogenicity was homogeneously increased in 27 territories of MHV tributaries (17%). This finding was more commonly seen in the hepatic venous congestion group (65%, 20/31) than in the non–hepatic venous congestion group (6%, 7/124) (p < 0.01) (Figs. 2A, 2B, 2C, and 2D). On Doppler sonography, reversed flow was seen in five MHV tributaries and was seen only in the non–hepatic venous congestion group (Figs. 4A and 4B). On the contrary, hepatofugal flow of the corresponding portal branch was seen in five portal vein branches, all in the hepatic venous congestion group (Figs. 5A, 5B, and 5C).
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In our series, MHV tributary territories frequently (17%) appeared hyperechoic compared with normal parenchyma on gray-scale sonography, and this finding was more commonly seen in the hepatic venous con gestion group (65%) than in the non–hepatic venous congestion group (6%) (p < 0.01). This finding was inconsistent with those of a pre vious report indicating that acute hepatic vein occlusion may cause subsequent hemor rhagic infarction that appeared as a hypo echoic area [22]. In our study, the cause of hyper echogenicity in the congested area was not clearly understood, and therefore further study is warranted to correlate this finding with pathologic changes.
Reversed flow of MHV tributaries was invariably seen in the non–hepatic venous congestion group. This result implies that although the reversal of hepatic venous flow direction represents outflow obstruction, it also indicates the development of intrahepatic collateral venous drainage, usually into the RHV. Indeed, the authors of previous studies have reported that 20–24% of the cases had venous anastomoses between MHV tributaries and the RHV immediately after MHV ligation on intraoperative Doppler sonography [11, 12]; it also has been proposed that MHV reconstruction not be mandatory if there is such a finding [11].
Hepatofugal flow of the corresponding portal branch was rarely, but exclusively, seen in the hepatic venous congestion group. This finding indicates that the portal vein may act as a draining vein in acute hepatic outflow obstruction and is consistent with previous studies using helical CT and intraoperative Doppler sonography that showed that hepatic venous blood could be regurgitated to the portal vein through the sinusoid when the hepatic vein was obstructed [13, 23].
Our study has several limitations. First, pathologic examination or venography was not performed in most of the patients. However, it is ethically impossible to perform biopsy or venography on all patients, especially when there is no evidence of severe congestion on noninvasive studies. Therefore, we made the reference diagnoses with helical CT findings on the basis of a previous study [18]. In that study, severe hepatic venous congestion was indicated when the hepatic parenchyma of typical anatomic distribution that corresponded to the drainage areas of MHV tributaries showed persistent low attenuation on unenhanced, HAP, and PVP scans with no opacification of the MHV tributaries [18]. Because we included the cases of severe hepatic venous congestion based on CT scans, the accuracy of Doppler sonography could have been affected. However, regarding the 24 large MHV tributaries for which venographic information was available, the diagnostic values of Doppler sonography for hepatic venous congestion were not reduced but, rather, were enhanced.
Second, because we did not correlate the Doppler sonography findings to the clinical findings, the clinical impact of this study is difficult to determine, and further study to correlate the Doppler sonography findings to the clinical findings will be required. However, the findings of this study show that Doppler sonography on postoperative day 1 is fairly accurate for assessing the patency of individual MHV tributaries. Therefore, the prompt diagnosis of hepatic venous congestion in a large MHV tributary using Doppler sonography as a screening technique may lead to a timely intervention such as percutaneous stent placement. In general, clinical consequences of and decision to perform an interventional treatment are influenced not only by the severity of hepatic venous congestion but also by liver volume, excluding the territory of hepatic venous congestion. Similar to the indication of MHV reconstruction, we propose that intervention is recommended when Doppler sonography shows no flow in a large MHV tributary and if liver volume, excluding the territory of hepatic venous congestion, is estimated to be insufficient for the postoperative metabolic demands of the recipient.
Third, all Doppler sonography examinations were performed by one radiologist using a Sequoia 512 scanner exclusively. Therefore, our study is limited in terms of interobserver variation according to the sono grapher's experience and the differences among the sonography scanners. Fourth, data clustering was inevitable in this study because every donor had multiple MHV tributaries. Fifth, CT scans were analyzed by only one reviewer and interobserver variability could be present in the analysis of the CT scans. However, the interpretation of the CT scans was relatively simple because we compared the attenuation of the corresponding segment of MHV tributaries and the rest of the liver and determined whether MHV tributaries were opacified or not.
In conclusion, Doppler sonography provides a reliable, noninvasive surveillance method for detecting hepatic venous con gestion in the paramedian sector of the modified right lobe graft during the early postoperative period after living donor liver transplantation. This examination is both highly sensitive and highly specific for that purpose when there is no Doppler-detectable blood flow in the MHV tributaries.
Acknowledgments
We thank Bonnie Hami for her editorial assistance in preparing the
manuscript.
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