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ORIGINAL ARTICLE
Year : 2020  |  Volume : 33  |  Issue : 1  |  Page : 309-314

Role of ultrasonography in assessment of postoperative vascular complications in recipients of living donor liver transplantation


1 Department of Radiology, Faculty of Medicine, Menoufyia University, Shebein Elkom, Menoufia, Egypt
2 Department of Radiology, National Liver Institute, Menoufyia University, Shebein Elkom, Menoufia, Egypt

Date of Submission12-Sep-2018
Date of Decision04-Nov-2018
Date of Acceptance10-Nov-2018
Date of Web Publication25-Mar-2020

Correspondence Address:
Dalia I Aggour
El-Bagour, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_276_18

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  Abstract 


Objective
The aim was to evaluate the role of color Doppler ultrasonography (CDUS) in the evaluation of vascular complications detected in recipients of living donor liver transplantation (LDLT).
Background
Post-transplant-related vascular complications remain threat to the recipients' survival. A higher risk for vascular complications was found in LDLT recipients because of complex vascular reconstruction and slender vessels. CDUS acted as a first-modality imaging technique to detect vascular complications in the early and late follow-up period.
Patients and methods
A total of 60 liver transplant recipients who underwent LDLT in National Liver Institute Menoufia University were included. The study was done over a period of 25 months from January 2016 to January 2018. These recipients underwent serial color Doppler sonographic evaluation of hepatic arteries, portal vein, and hepatic veins after surgery. Patients with abnormal sonographic finding underwent subsequent angiography.
Results
The study was done by gray-scale, CDUS and included 47 patients of 60 recipients who showed suspicious vascular complications as follows: 26, 13, and eight patients had suspected arterial, portal, and hepatic venous complications, respectively. All these patients underwent conventional angiography. The sensitivity and specificity of CDUS in the evaluation of arterial, portal, and hepatic venous complications were 95, 87.5, and 87%, respectively, and 86, 91, and 96%, respectively, and for the latest complications was 87 and 96%, respectively.
Conclusion
CDUS was the preferred postoperative screening method; it was an initial recipient workup for post-LDLT. Providing a perfect evaluation of hepatic vasculature and assessment of early and lately presented vascular complications.

Keywords: color Doppler ultrasound, conventional angiography, living related donor liver transplantation, postoperative, vascular complications


How to cite this article:
El Sayed EE, El Warraky MS, Aggour DI. Role of ultrasonography in assessment of postoperative vascular complications in recipients of living donor liver transplantation. Menoufia Med J 2020;33:309-14

How to cite this URL:
El Sayed EE, El Warraky MS, Aggour DI. Role of ultrasonography in assessment of postoperative vascular complications in recipients of living donor liver transplantation. Menoufia Med J [serial online] 2020 [cited 2020 Jun 3];33:309-14. Available from: http://www.mmj.eg.net/text.asp?2020/33/1/309/281291




  Introduction Top


Liver transplantation is an effective treatment for most end-stage liver diseases and acute liver failure. Innovative surgical techniques, including split liver transplantation and living-related donor liver transplantation (LDLT) have been developed owing to the worldwide shortage of cadaveric liver[1]. Post-transplant vascular complications remain a major threat to the recipients' survival. LDLT recipients had a higher risk than cadaveric liver transplantation recipients for postoperative vascular complications owing to their complex vascular reconstruction and slender vessels. Early diagnosis and treatment are critical for graft and recipient survival. As a non-radioactive, cost-effective and non-invasive modality with availability to be bedside, color Doppler ultrasonography (CDUS) serves as a first-line imaging technique to detect vascular complications in the early and long-term postoperative follow-up. Post-LDLT vascular complications mainly involved the hepatic artery, portal vein (PV), hepatic vein, and other outflow tracts[2]. Hepatic arterial complications included hepatic arterial stenosis (HAS), hepatic arterial thrombosis (HAT), and pseudoaneurysm formation. PV complications included portal vein thrombosis (PVT), stenosis, PV attenuation, PV stasis, and SMV and SV thrombosis. Hepatic venous complications included HV stenosis and HV thrombosis. The aim of this study was to evaluate the role of ultrasonography and CDUS in detection of these vascular complications in recipients of LDLT.


  Patients and Methods Top


This study was performed after written consent from patients and approval from ethical committee of the hospital of the National Liver Institute, Menoufia University. This study was done by Philips Affinity 70. Gray-scale and CDUS examinations were conducted on 60 recipients who underwent LDLT over a period of 25 months from January 2016 to January 2018, in whom clinical data, laboratory data, ultrasonographic data raised the suspicion of postoperative vascular complications. All patients underwent conventional angiography as confirmatory method for results obtained by CDUS. Postoperative vascular complications included the followings:

Review

Hepatic arterial complications

Hepatic arterial complications included HAS, HAT, and pseudoaneurysm formation. As the biliary tree received its blood supply from the hepatic arteries, so any hepatic arterial complication could cause biliary ischemia, leading to biliary strictures, necrosis, abscesses, and graft failure. Biliary strictures resulting from arterial complications were mostly nonanastomotic and involved the hilum, but could be multifocal and intrahepatic. Biliary changes owing to arterial complications took time to develop and were not evident on ultrasound in the early stages[3].

Hepatic artery thrombosis

HAT was the most severe hepatic artery complication, with an incidence of 4–12% in adult recipient and a fatality rate of 20–60%. Risk factors for early HAT (occurring within first few weeks after liver transplantation) included the following: (a) ABO blood type incompatibility, (b) increased cold ischemic time of the donor liver, (c) acute rejection, and (d) surgical factors such as hepatic artery spasm, compression by perianastomotic hematoma, intimal injury, artery distortion, artery anastomosis inversion, and small artery caliber. In contrast, late HAT (occurring >7 days after liver transplantation) was associated with chronic rejection and sepsis. Typical HAT was manifested as fever, severe hepatalgia, ascites, reduced bile flow, changed bile properties, sudden increase in serum transaminases, prolonged prothrombin time and sepsis, whereas the symptoms of late HAT are often atypical owing to the formation of collateral circulation. HAT could lead to biliary complications rapidly, graft necrosis, and even patient death[4]. It was of extreme importance for prompt diagnosis of HAT because early intervention (with thrombectomy, hepatic artery reconstruction, or both) may allow salvage of the graft. However, most patients ultimately require retransplantation. Even after retransplantation, the mortality rate is 27–30%. HAT-induced ischemia initially affects the bile ducts because bile ducts are supplied only by the hepatic artery, and the biliary epithelium is more sensitive to ischemic injury than hepatocytes. Biliary ischemia may lead to biliary necrosis, cast formation, abscesses, nonanastomotic bile leak, and bilomas. Conventional ultrasound plays an important role in the detection of bile duct complications as a first screening modality.

The Doppler ultrasound diagnostic criteria for HAT included the disappearance of arterial blood flow at the hilum hepatis and inside the liver on color Doppler imaging. When collateralization developed with HAT, a tardus-parvus spectrum (RI <0.5 and SAT >80 ms) of intrahepatic blood flow could be detected. The secondary changes mainly included hepatic infarction, biliary complications, and abscess[5].

Hepatic artery stenosis

Hepatic artery stenosis (HAS) is the most common vascular complication of liver transplantation after HAT, reported to occur in 5–11% of liver transplant recipients. HAS occurs within 3 months after transplantation, primarily at the anastomotic site. If left untreated, it could lead to HAT owing to slow flow or progress to cause hepatic ischemia, biliary stricture, sepsis, and graft loss.

The causes are diverse and mainly include the following: (a) surgical factors, (b) clamp injury, (c) intimal trauma caused by perfusion catheters, and (d) vasa vasorum disruption leading to ischemia of the arterial ends and rejection. Early detection of HAS is very important to allow treatment (surgical reconstruction or balloon angioplasty) and avoid the necessity of retransplantation. According to the diameter-narrowing rates, HAS can be classified as mild stenosis (narrowing rate <50%), moderate stenosis (narrowing rate 50–75%), and severe stenosis (narrowing rate >75%). Mild stenosis not inducing hemodynamic disorders of the hepatic artery or graft ischemia presents no significant Doppler abnormalities. In contrast, moderate and severe stenosis, resulting in graft complications such as biliary ischemia, hepatic dysfunction, or even hepatic failure might have abnormal artery blood flow on Doppler imaging. HAS could be diagnosed by Doppler ultrasound by the presence of focal increased blood flow velocity greater than 200 cm/s at the extrahepatic artery or the tardus-parvus waveform at the intrahepatic arteries. Tardus-parvus waveform is considered an effective diagnostic parameter for HAS, but not a specific finding, which could be also found in the following: (a) long-term HAT accompanied with collateral vessel formation, (b) PVT, and (c) atherosclerotic disease, resulting in a false-positive diagnosis[6].

Hepatic artery pseudoaneurysm

Hepatic artery pseudoaneurysm (HAP) is not a common complication and has an incidence of 0.3–1%. Extrahepatic pseudoaneurysms mostly develop at the site of anastomosis or as a complication of angioplasty. It can rupture intraperitoneally and lead to hemorrhage manifested by acute shock, and this is the most severe and life-threatening presentation. Extrahepatic pseudoaneurysms could be treated by surgical resection, embolization, or exclusion with stent placement. Intrahepatic pseudoaneurysms, which could occur after percutaneous liver biopsy or focal parenchymal infection, are often detected incidentally. Rupture of intrahepatic pseudoaneurysm could result in portal or biliary fistulas, in the latter case manifesting as upper gastrointestinal bleeding or hemobilia. Intrahepatic pseudoaneurysm is treated with endovascular coil embolization. Early diagnosis and treatments are essential for graft salvage. Gray-scale ultrasound and Doppler ultrasound are considered the primary imaging techniques for diagnosis and follow-up of HAP. The diagnosis of HAP is suspected when a focal cystic lesion of the hepatic artery is detected with pulsatile wave pattern on Doppler ultrasound.

Arterial steal syndrome

After liver transplantation, a shift of blood flow from hepatic artery into the splenic artery (lienalis steal syndrome) or gastroduodenal artery (gastroduodenal steal syndrome) had been observed. In arterial steal syndrome, liver ischemia is related to a reduced perfusion of HA rather to an obstruction. Celiac angiography is the 'gold standard' for splenic artery steal syndrome (SASS) diagnosis. When a high-resistance waveform (RI >0.8) with low diastolic flow of the intrahepatic or extrahepatic arteries was detected on Doppler ultrasound, with dilated splenic arterial and splenomegaly, SASS should be highly suspected[6].

Portal vein complications

Portal vein thrombosis

PVT most commonly results from technical problems (vessel misalignment, differences in the caliber of the anastomosed vessels, kink of the PV, or stretching of the PV at the anastomotic site), previous PV surgery or previous thrombosis, decreased portal inflow, increased downstream resistance owing to a suprahepatic stricture of the hepatic veins, and hypercoagulable states. Diagnosis of PVT is not difficult using gray-scale and Doppler ultrasound including absence or filling defect of blood flow. Conventional ultrasound provided an ideal specificity ranging from 95 to 100% in diagnosing PVT; however, it is difficult to identify the duration and range of thrombosis[7].

Portal vein stenosis

Portal vein stenosis (PVS) is found mainly at the anastomosis site. During LDLT, vessel caliber mismatch is often found between the donor and recipient PV. So, mild anastomotic stenosis is common but not affecting hemodynamics and liver function. Stenosis greater than 50% was considered hemodynamically significant and clinically presented with symptoms of portal hypertension, liver failure, massive ascites, or edema. The criteria for PVS include the following: regional stenosis with a diameter less than 2.5 mm, blood flow aliasing and acceleration at the stenotic site, blood flow velocity ratio greater than or equal to 3:1 between stenotic and prestenotic flow, and signs of portal hypertension, such as splenomegaly, ascites or collateral circulation formation. Treatment includes percutaneous transluminal angioplasty with or without stent placement, surgical thrombectomy, placement of venous jump graft, creation of a Porto systemic shunt, or even retransplantation[7].

Hepatic vein complications

Reconstruction of the outflow tract during LDLT is complex. In an adult right lobe LDLT, the right hepatic veins are preserved in the right lobes of the graft liver. As for preservation of the middle hepatic vein and reconstruction of the other blood vessels, decisions should be made in accordance with the specific individual condition. Currently, in consideration of the safety of the donor, the middle hepatic vein is often preserved in the donor. Therefore, to ensure adequate drainage, reconstruction of the inferior right hepatic vein and thick tributaries of the middle hepatic vein V5 and/or V8 is usually required. Therefore, for an adult right lobe LDLT without the middle hepatic vein, the right hepatic vein, inferior right hepatic vein, tributaries of the middle hepatic vein, and bridging veins may serve as outflow tracts of the liver. Outflow tract obstruction leads to congestions in the drained area. Mild congestion may manifest no significant clinical symptoms, whereas severe congestion can result in effective liver volume reduction, which may also cause small-for-size syndrome and liver failure. Therefore, postoperative monitoring of the outflow tracts is extremely important. Ultrasound is a commonly used method for outflow tract monitoring. Gray-scale ultrasound can reveal the inferior vena cava, hepatic vein, inferior right hepatic vein, and some thick bridging veins, and sometimes congestion may be revealed preliminarily by sonographic changes in the liver parenchyma. Doppler ultrasound can reveal the blood flow of hepatic veins and bridging veins[8]. Hepatic veins complications included thrombosis and stenosis, usually at the anastomotic site. Technical factors, such as size discrepancy between recipient and donor vessels or suprahepatic caval kinking owing to organ rotation, may cause acute hepatic vein stenosis. Delayed hepatic vein stenosis, may be due to fibrosis, neointimal hyperplasia, or a chronic thrombus. Chronic venous stenosis is more common after retransplantation and in children. Clinical presentation included hepatomegaly, ascites, and pleural effusions[9]. Hepatic vein thrombosis is a rare complication but not difficult to be diagnosed by conventional ultrasound. In HVS, a significant stenosis is revealed by the gray-scale ultrasound, and a high-speed blood flow appears at the stenosis on Doppler spectral imaging. The ratio of stenotic to prestenotic blood flow velocity should be greater than 3–4: 1, with a flat monophasic hepatic venous wave form [Figure 1]. A venous outflow obstruction may be treated with placement of a balloon-expandable stent or thrombectomy [Figure 2] and [Figure 3].
Figure 1: Postoperative hepatic vein stenosis detected by gray.scale and color Doppler ultrasound.

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Figure 2: Postoperative hepatic artery thrombosis with graft abscess.

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Figure 3: Postoperative partial portal vein thrombosis with stenosis of the remaining patent part.

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Arterioportal fistula

Intrahepatic arterioportal fistula is not an uncommon complication of liver transplantation following liver biopsy, whether surgical or percutaneous, which was performed to rule out graft rejection. The prevalence of arterioportal fistula owing to liver biopsy is as high as 50% in the first week but decreased to 10% after this time, as these shunts tend to close spontaneously.

Statistical analysis

Data were fed to the computer using IBM (SPSS Inc., Chicago, Illinois, USA).

Software package, version 20.0. The results were expressed by applying sensitivity and specificity tests.


  Results Top


By CDUS, 47 of 60 patients had vascular complications, 26 patients had arterial complications, 13 patients had portal complications, and eight patients had venous complications. Patients with suspected arterial complications underwent conventional angiography, and the results were as follows: 11 patients had HAS, six patients had HAT, two patients had SASS, and two patients had gastroduodenal artery steal. So sensitivity and specificity of CDUS in detection of arterial complications is 95 and 86%, respectively. Patients with suspected portal complications detected by CDUS, underwent conventional angiography, and the results were as follows: two patients had PVT; two patients had PV attenuation [decreased diameter of intrahepatic portion of PV (of the donated graft) in relation to the extrahepatic portion of the PV of the recipient, which is dilated owing to portal hypertension]; two patients had SMV thrombosis; one patient had PVS; and one patient had splenic vein thrombosis. Sensitivity and specificity of CDUS in detection of portal complications is 87.5 and 91%, respectively. Patients with suspected hepatic venous osteal stenosis and hepatic vein thrombosis underwent hepatic venography, and the results were as follows: two (3.3%) patients had HV stenosis and five (8.3%) patients had HV thrombosis, so sensitivity and specificity of ultrasound in the detection of venous complications is 87 and 96%, respectively. The sensitivity and specificity of CDUS in the detection of vascular complications is shown in [Table 1].
Table 1: Sensitivity and specificity of color Doppler ultrasonography in detection of vascular complications

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  Discussion Top


CDUS is a portable, non-invasive tool that provides comprehensive, rapid, and accurate evaluation of the entire hepatic vasculature. CDUS sensitivity and specificity in arterial complications detection was 95 and 87%, respectively. Tamselet al.[10] mentioned that the sensitivity of Doppler ultrasound in HAS had been reported to be between 75 and 100% and also mentioned HAT can be detected even before the clinical symptoms appear. Hom et al.[5] reported that false positive rate may even reach as high as 75%, and false-negative results arise mainly from collateral circulation with reported false-negative rate of 7–29%. Sanyalet al.[11] mentioned that diagnosis of HAS by CDUS is based on focal increased velocity of blood flow greater than 200 cm/s at the extrahepatic artery or the tardus parvus wave form at the intrahepatic arteries with a sensitivity of 72–97% and a specificity of 64–99%. In this study, we had 13 patients who had portal complications, representing 21.6% of the total patients. Perkins[12] reported that incidence PV complications was 9%. Yerdelet al.[13] noted an extremely high incidence of PV complications at 12.5% in patients with a history of severe portal hypertension or thrombosis at the time of LDLT. Sanvalet al.[14] mentioned that PV complications following LT are relatively uncommon, occurring in 1–3% in most reports (with an incidence reaching 13%). Akun et al.[15] and Hwanget al.[8]reported that HVS is a relatively uncommon complication after LDLT, with incidence rate of 0. 5–3.2%. Darcy[16]mentioned that diagnostic criteria for HVS using Doppler ultrasound remain controversial. HV stenosis was either significant or insignificant stenosis according the degree of diameter reduction of the hepatic veins and the accompanied newly developed ascites. Our findings are similar to what were mentioned by Drudiet al.[17].


  Conclusion Top


Conventional gray-scale and Doppler ultrasound played important roles in vascular monitoring after LDLT, providing effective method for the detection and evaluation of post-LDLT vascular complications.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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8.
Hwang HJ, Kim KW, Jeong WK, Song GW, Ko GY, Sung KB, et al. Right hepatic vein stenosis at anastomosis in patients after living donor liver transplantation: optimal Doppler US venous pulsatility index and CT criteria-receiver operating characteristic analysis. Radiology 2009; 253:543–551.  Back to cited text no. 8
    
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Yerdel MA, Gunson B, Mirza D, Karayalçin K, Olliff S, Buckels J, et al. Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome. Transplantation 2000; 69:1873–1881.  Back to cited text no. 13
    
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Sanval R, Lall CG, Lamba R, Brody MB, Rodgers SK, Horrow MM. Orthotopic liver transplantation: reversible Doppler US findings in the immediate postoperative period. Radiographics 2012; 32:199–211.  Back to cited text no. 14
    
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Akun E, Yaprak O, Killi R, Balci NC, Tokat Y, Yuzer Y. Vascular complications in hepatic transplantation: single-center experience in 14 years. Transplant Proc 2012; 44:1368–1372.  Back to cited text no. 15
    
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