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Hepatic Vein Stenosis after Living Donor Liver Transplantation: Evaluation with Doppler US¹

¹ From the Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine, 388–1 Poongnap-dong, Seoul 138–736, Korea. Received June 10, 2002; revision requested August 20; final revision received May 5, 2003; accepted May 6. Address correspondence to T.K.K. (e-mail: tkkim@amc.seoul.kr).

	ABSTRACT

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PURPOSE: To determine the spectral Doppler ultrasonographic (US) findings that would indicate hepatic vein stenosis after living donor liver transplantation (LDLT).

MATERIALS AND METHODS: The authors retrospectively reviewed postoperative Doppler US images of the hepatic veins in 113 consecutive patients who underwent LDLT. Doppler US was performed 1–25 times (mean, 5.2 times) during 1–433 days after LDLT. Nineteen patients who were inadequate for analysis were excluded; thus, 94 patients (72 male patients and 22 female patients; mean age, 40 years) were included in the study. Patients with more than 10 mm Hg of pressure gradient between the hepatic vein and the inferior vena cava were considered to have substantial hepatic vein stenosis (stenosis group). Those without substantial stenosis (control group) included patients with no clinical or radiologic evidence of hepatic vein stenosis for at least 3 months after LDLT. The wave pattern and peak flow velocity of the hepatic veins were compared between the groups.

RESULTS: Five patients (5%) had substantial hepatic vein stenosis: three had persistent monophasic wave patterns at all US examinations, and two had monophasic wave patterns at most US examinations and biphasic or triphasic wave patterns at 6- and 9-day follow-up examinations. In the control group, 52 (58%) of 89 patients had a persistent triphasic or biphasic wave pattern and 37 (42%) had a monophasic wave pattern at one or more US examinations; this included two patients with persistent monophasic wave patterns. A monophasic wave pattern was more frequent in the stenosis group than in the control group (P = .015). There was no significant difference between the velocities of the hepatic veins in the stenosis group (22.3 cm/sec ± 9.6 [SD]) and those in the control group (37.5 cm/sec ± 20.3) (P = .14).

CONCLUSION: A persistent monophasic wave pattern on Doppler US images of the hepatic veins is suggestive of, but not specific for, substantial hepatic vein stenosis after LDLT. A persistent triphasic wave pattern on Doppler US images can exclude the possibility of substantial stenosis.

© RSNA, 2003

Index terms: Hepatic veins, stenosis or obstruction, 959.7173 • Hepatic veins, US, 959.12984 • Liver, transplantation, 761.45 • Ultrasound (US), Doppler studies, 761.12984

	INTRODUCTION

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Hepatic vein stenosis has emerged as one of the important vascular complications of living donor liver transplantation (LDLT). In a case of orthotopic liver transplantation from a cadaveric donor, the anastomosis is performed between the venae cavae without touching the hepatic veins. In LDLT, however, each hepatic vein of the transplanted liver is connected directly to the recipient’s inferior vena cava (IVC) after total hepatectomy has been performed (1). This surgical technique can induce mechanical or functional stenosis of the hepatic veins, which can cause venous outflow obstruction and even graft loss of the transplanted liver.

Ultrasonography (US) is a very useful imaging modality in the early postoperative period after liver transplantation, and it is sometimes the only available modality. Spectral and color Doppler US can provide useful information for monitoring vascular complications. The use of Doppler US in evaluating vascular compromise, particularly of the hepatic artery and portal vein, has been well established, as it offers diagnostic criteria on Doppler spectral examinations (2–7). However, to our knowledge, there have been no study results that provide diagnostic criteria for using Doppler US in the evaluation of hepatic vein stenosis.

The purpose of this study was to determine the spectral Doppler US findings that would indicate hepatic vein stenosis after LDLT.

	MATERIALS AND METHODS

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Patients
During a 14-month period, 113 consecutive patients underwent LDLT at our hospital. Nineteen of these patients were excluded from the study because of early postoperative death (n = 8), hepatic venous stent placement before Doppler US examination (n = 5), or an insufficient (<3 months) postoperative follow-up period (n = 6); therefore, 94 patients were included in this study. There were 72 male patients and 22 female patients, with a mean age of 40 years (range, 1/2–60 years). Sixty-nine patients received a right lobe graft, 20 patients received a left lobe graft, and five patients received bilobe grafts (two left lobe grafts from two living donors). Two patients underwent repeat (secondary) liver transplantation because of rejection of a previous graft from a cadaveric donor or a graft failure resulting from severe portal vein stenosis. Hepatic veins from a total of 99 grafts in 94 patients (including the five patients with bilobe grafts) were evaluated.

Venography of the hepatic veins was performed in 10 patients who were suspected of having hepatic vein stenosis on the basis of clinical and radiologic findings. The clinical findings that prompted hepatic venography included abnormal laboratory values, hepatomegaly, ascites, and pleural effusions. The pressure gradient between the IVC and the hepatic vein was measured in these patients. A metallic stent was inserted into the hepatic vein in patients who had a pressure gradient greater than 10 mm Hg.

Each patient was assigned to either the stenosis group or the control group on the basis of the presence of hepatic vein stenosis in the transplanted liver. The stenosis group included patients with clinical findings suggestive of hepatic vein stenosis (eg, hepatomegaly, increased ascites, or abnormal liver function according to laboratory tests) and patients who showed a greater than 10 mm Hg pressure gradient between the hepatic vein and the IVC during the insertion of the stent. The control group included patients with no clinical or radiologic evidence of hepatic vein stenosis for least 3 months after LDLT (mean, 9.6 months; range, 3–15 months).

Our institutional review board did not require its approval or patient informed consent for this retrospective study.

US Examination
Doppler US was routinely performed on the 1st, 2nd, and 3rd days, and at 1 week following the LDLT surgery. Additional examinations were performed when a vascular complication was suspected on the basis of clinical findings. All patients underwent Doppler US examinations 1–25 times (mean, 5.2 times) during the 1–433 days after LDLT. All US examinations were performed by one of the eight board-certified abdominal radiologists in our department. They each had 5–20 years of experience in performing US. US examinations were performed by using a HDI 3000 scanner (ATL, Bothell, Wash) with a 2–4-MHz convex probe, a Sequoia 512 scanner (Acuson, Mountain View, Calif) with a 3–4-MHz convex probe, or a LOGIQ 700 scanner (GE Medical Systems, Milwaukee, Wis) with a 2–4-MHz convex probe. Color and spectral Doppler US examinations were performed in the hepatic artery, portal vein, and hepatic vein of the transplanted liver. A spectral Doppler wave of the hepatic vein was obtained within 3 cm of the IVC. In the early postoperative state, most Doppler US examinations were performed without patient breath hold because these patients were not able to hold their breath. The spectral Doppler wave of the hepatic vein was obtained several times, and the peak flow velocity of the hepatic vein was measured in each hepatic vein.

US Evaluation and Analysis
Two radiologists (E.Y.K. and T.K.K.) retrospectively reviewed the spectral Doppler US findings of the hepatic vein on static images by consensus. One reviewer had 10 years of experience in the field of radiology, and the other reviewer had 5 years of experience. They classified the hepatic venous wave patterns into three groups: triphasic, biphasic, and monophasic (8). The triphasic wave pattern consisted of two antegrade peaks with a short period of reversed flow at the end of the second antegrade wave (Fig 1). The monophasic wave pattern was defined as the loss of normal hepatic vein periodicity and a continuous flat wave (Fig 2). The biphasic wave pattern was defined as the loss of reversed flow but preservation of hepatic vein periodicity (Fig 3). The peak flow velocity of the hepatic vein was also assessed.

View larger version (93K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Transverse oblique duplex Doppler US image shows triphasic wave pattern of the hepatic vein in a 61-year-old man without hepatic vein stenosis after LDLT. Two antegrade peaks are separated by a short phase of retrograde flow (v), and a period of reversed flow (a) follows at the of the second antegrade flow.

View larger version (164K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Sagittal oblique duplex Doppler US image shows monophasic wave pattern of the hepatic vein in a 49-year-old man with hepatic vein stenosis after LDLT.

View larger version (114K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Transverse oblique duplex Doppler US image shows biphasic wave pattern of the hepatic vein in a 40-year-old woman without hepatic vein stenosis after LDLT.

	RESULTS

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On the basis of venographic and follow-up results, five (5%) of 94 patients were included in the stenosis group, and 89 patients (95%) were included in the control group. Three (60%) of the five patients in the stenosis group showed a persistent monophasic wave pattern during all Doppler US examinations. In the remaining two patients (40%), a monophasic wave pattern was obtained during three of four US examinations in one patient and during five of six US examinations in the other; however, there was a biphasic or triphasic wave pattern during the remaining US examinations (6 days and 9 days after LDLT, respectively). In three patients, the persistent monophasic waves changed to triphasic or biphasic waves after insertion of the metallic stent in the hepatic vein (Fig 4). In the control group, 52 patients (58%) had a persistent triphasic or biphasic wave pattern at all US examinations, and 37 patients (42%) had a monophasic wave pattern at one or more US examinations (Table). Among these 37 patients, a persistent monophasic wave pattern was found in two patients. A persistent triphasic or biphasic wave pattern was found only in the control group, and a persistent monophasic wave pattern was found mostly in the stenosis group (60% in the stenosis group vs 2% in the control group). Monophasic wave pattern was found more frequently in the stenosis group than in the control group (P = .015), and a persistent monophasic wave pattern was also found more frequently in the stenosis group than in the control group (P = .001). However, visualization of the monophasic wave pattern during a single Doppler US examination did not necessarily mean that there was hepatic vein stenosis, because this finding was also found in 37 patients (42%) in the control group.

View larger version (137K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Monophasic wave pattern in a 42-year-old man with hepatic vein stenosis after LDLT. (a) Sagittal oblique duplex Doppler US image shows monophasic wave pattern of the hepatic vein. (b, c) Images obtained at hepatic venography. (b) Luminal narrowing (arrow) is seen at the anastomotic site of the hepatic veins. The pressure gradient between the hepatic vein and IVC is 12 mm Hg. (c) After stent insertion (arrowheads), the narrowed segment of the hepatic vein has disappeared, and the pressure gradient is 1 mm Hg. (d) Sagittal oblique duplex Doppler US image obtained after stent placement into the hepatic vein shows a triphasic wave pattern.

View larger version (110K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Monophasic wave pattern in a 42-year-old man with hepatic vein stenosis after LDLT. (a) Sagittal oblique duplex Doppler US image shows monophasic wave pattern of the hepatic vein. (b, c) Images obtained at hepatic venography. (b) Luminal narrowing (arrow) is seen at the anastomotic site of the hepatic veins. The pressure gradient between the hepatic vein and IVC is 12 mm Hg. (c) After stent insertion (arrowheads), the narrowed segment of the hepatic vein has disappeared, and the pressure gradient is 1 mm Hg. (d) Sagittal oblique duplex Doppler US image obtained after stent placement into the hepatic vein shows a triphasic wave pattern.

View larger version (92K): [in this window] [in a new window] [Download PPT slide]   Figure 4c. Monophasic wave pattern in a 42-year-old man with hepatic vein stenosis after LDLT. (a) Sagittal oblique duplex Doppler US image shows monophasic wave pattern of the hepatic vein. (b, c) Images obtained at hepatic venography. (b) Luminal narrowing (arrow) is seen at the anastomotic site of the hepatic veins. The pressure gradient between the hepatic vein and IVC is 12 mm Hg. (c) After stent insertion (arrowheads), the narrowed segment of the hepatic vein has disappeared, and the pressure gradient is 1 mm Hg. (d) Sagittal oblique duplex Doppler US image obtained after stent placement into the hepatic vein shows a triphasic wave pattern.

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 4d. Monophasic wave pattern in a 42-year-old man with hepatic vein stenosis after LDLT. (a) Sagittal oblique duplex Doppler US image shows monophasic wave pattern of the hepatic vein. (b, c) Images obtained at hepatic venography. (b) Luminal narrowing (arrow) is seen at the anastomotic site of the hepatic veins. The pressure gradient between the hepatic vein and IVC is 12 mm Hg. (c) After stent insertion (arrowheads), the narrowed segment of the hepatic vein has disappeared, and the pressure gradient is 1 mm Hg. (d) Sagittal oblique duplex Doppler US image obtained after stent placement into the hepatic vein shows a triphasic wave pattern.

	DISCUSSION

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Liver transplantation has become the treatment of choice for end-stage liver disease. Liver cirrhosis and hepatocellular carcinoma are the major health problems, and liver transplantation is increasingly required; this is especially true in eastern countries, where the incidence of type B and type C viral hepatitis is high. The persistent shortage of cadaveric liver for transplantation has caused LDLT to emerge as a strong alternative.

In contrast to orthotopic liver transplantation, LDLT surgical procedures include anastomosis between the hepatic vein of the graft and the IVC of the recipient. In orthotopic liver transplantation, the position of the graft liver is relatively fixed, and the anastomoses between the two venae cavae are stable. In LDLT, however, the graft hepatic vein is either anastomosed in an end-to-end fashion to the stump of the hepatic vein in the recipient, or it is anastomosed in an end-to-side fashion directly to the IVC after total hepatectomy in the recipient. The relative position of the hepatic veins is fixed so that even a slight movement of the graft results in buckling of the vessels and poor flow in the hepatic veins (1). The clinical signs of hepatic vein stenosis are usually nonspecific and include congestion of the liver parenchyma with abnormal laboratory values, hepatomegaly, ascites, and pleural effusions. Biopsy results indicate hepatocellular necrosis and stasis, and without proper management, there can even be graft loss or the need for retransplantation (1,9,10).

In our study, the incidence of hepatic vein stenosis after LDLT was 5%. Early detection of hepatic vein stenosis is important because it can lead to timely intervention, such as hepatic vein stent placement, and thereby improve the patient’s chance for a successful outcome (10,11). Normal hepatic veins usually show a triphasic waveform reflecting the cardiac cycle. Hosoki et al (12) reported that blood flow patterns altered from phasic to absent, reversed, turbulent, or continuous—with or without directional changes—are characteristic of hepatic outflow obstruction; this includes conditions such as Budd-Chiari syndrome. Rossi et al (9) reported that a flat hepatic venous wave on Doppler US images is a very sensitive, but not specific, indicator of upper IVC obstruction after orthotopic liver transplantation. However, to our knowledge, no prior study results have provided the reliable diagnostic criteria for using Doppler US examinations in the evaluation of hepatic vein stenosis after LDLT.

In our study, all patients with substantial hepatic vein stenosis after LDLT showed monophasic waves at Doppler US. However, monophasic waves were also found in many patients (42%) in the control group. In most of the control group patients, a monophasic waveform was a transient finding that was seen during only one or two US examinations, whereas three of five patients in the stenosis group showed a persistent monophasic waveform during all US examinations. Therefore, a monophasic waveform is considered a sensitive but not specific finding of hepatic vein stenosis after LDLT. We think it unreasonable to make the diagnosis of hepatic vein stenosis with a monophasic wave pattern from a single Doppler US examination. Correlation with clinical findings and/or follow-up study is warranted before an invasive procedure such as venography or an interventional procedure is considered. However, the possibility of hepatic vein stenosis can be ruled out when persistent triphasic or biphasic waves are seen during US examinations.

The cause of monophasic wave patterns in the control group is still not clear. It may be due to transient outflow disturbance caused by graft movement, parenchymal changes associated with other LDLT-related complications, postoperative edema, influence of the patient’s respiration, or changes in abdominal pressure. Among the 37 patients without hepatic vein stenosis who showed a monophasic wave pattern, nine had other complications, which included portal vein obstruction, hepatic arterial stenosis or aneurysm, and acute rejection.

The peak flow velocity of the hepatic vein is very much influenced by respiration, as well as by intraabdominal and intrathoracic pressure. The difference in flow velocity between the stenosis group and the control group is thought to be the result of the differences in flow wave patterns in both groups (ie, a more frequent triphasic wave pattern in the control group than in the stenosis group). The fact that there was no significant difference in the flow velocity of hepatic veins with monophasic wave pattern between the two groups indicates that the flow velocity itself is not an important parameter in the diagnosis of hepatic vein stenosis.

There were several limitations to our study. The first is that conventional venography was performed only in the patients suspected of having hepatic vein stenosis and not in all of our study patients. However, we assume that a patient’s well-being for more than 3 months may be accepted as a criterion for not having significant hepatic vein stenosis. Second, the results from Doppler US examinations may have influence on the decision to perform hepatic venography. However, hepatic venography was performed mainly on the basis of clinical findings (eg, persistent abnormal liver function, ascites, hepatomegaly) rather than on Doppler US examination results, because the Doppler US criteria for hepatic vein stenosis had not been established during the study period. Third, the threshold of 10 mm Hg is an arbitrary criterion without any confirmed diagnostic criteria of substantial hepatic vein stenosis. Further studies, including a larger series with a longer follow-up period, will be necessary to determine accurate criteria of hepatic vein stenosis and to confirm our results.

In conclusion, a persistent monophasic wave pattern on Doppler US images is a sensitive finding, but not a specific finding, of hepatic vein stenosis after LDLT. A monophasic waveform during a single Doppler US examination is not diagnostic of substantial hepatic vein stenosis, and it is necessary to document this waveform during several US examinations. Persistent triphasic or biphasic waves at Doppler US can exclude the possibility of substantial hepatic vein stenosis.

	FOOTNOTES

 
² Current address: Department of Radiology, Hallym University Sacred Heart Hospital, Anyang, Kyunggi-do, Korea.

Abbreviations: IVC = inferior vena cava, LDLT = living donor liver transplantation

Author contributions: Guarantor of integrity of entire study, T.K.K.; study concepts, H.K.H.; study design, T.K.K.; literature research, P.N.K.; clinical studies, E.Y.K.; data acquisition, A.Y.K.; data analysis/interpretation, E.Y.K.; statistical analysis, A.Y.K.; manuscript preparation, definition of intellectual content, and editing, E.Y.K.; manuscript revision/review, T.K.K.; manuscript final version approval, M.G.L.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Inomata Y, Uemoto S, Asonuma K, et al. Right lobe graft in living donor liver transplantation. Transplantation 2000; 69:258-264.[CrossRef][Medline]
2. Lee J, Ben-Ami T, Yousefzadeh D, et al. Extrahepatic portal vein stenosis in recipients of living-donor allografts: Doppler sonography. AJR Am J Roentgenol 1996; 167:85-90.[Abstract/Free Full Text]
3. Platt JF, Yutzy GG, Bude RO, Ellis JH, Rubin JM. Use of Doppler sonography for revealing hepatic artery stenosis in liver transplant recipients. AJR Am J Roentgenol 1997; 168:473-476.[Abstract/Free Full Text]
4. Dodd GD, III, Memel DS, Zajko AB, Baron RL, Santaguida LA. Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 1994; 192:657-661.[Abstract/Free Full Text]
5. Norten A, Sproat IA. Hepatic artery thrombosis after liver transplantation: temporal accuracy of diagnosis with duplex US and the syndrome of impending thrombosis. Radiology 1996; 198:553- 559.[Abstract/Free Full Text]
6. Langnas AN, Marujo W, Stratta RJ, Wood RP, Shaw BW, Jr. Vascular complications after orthotopic liver transplantation. Am J Surg 1991; 161:76-83.[CrossRef][Medline]
7. Lomas DJ, Britton PD, Farman P, et al. Duplex Doppler ultrasound for the detection of vascular occlusion following liver transplantation in children. Clin Radiol 1992; 46:38-42.[CrossRef][Medline]
8. Herbay AV, Frieling T, Haussinger D. Association between duplex Doppler sonographic flow pattern in right hepatic vein and various liver disease. J Clin Ultrasound 2001; 29:25-30.[CrossRef][Medline]
9. Rossi AR, Pozniak MA, Zarvan NP. Upper inferior vena caval anastomotic stenosis in liver transplant recipients: Doppler US diagnosis. Radiology 1993; 187:387-389.[Abstract/Free Full Text]
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11. Pfammatter T, Williams DM, Lane KL, Campbell DA, Jr, Cho KJ. Suprahepatic caval anastomotic stenosis complicating orthotopic liver transplantation: treatment with percutaneous transluminal angioplasty, Wallstent placement, or both. AJR Am J Roentgenol 1997; 168:477-480.[Abstract/Free Full Text]
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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2293020700v1 229/3/806    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Ko, E. Y. Articles by Lee, M.-G. Search for Related Content PubMed PubMed Citation Articles by Ko, E. Y. Articles by Lee, M.-G.