EARLY PERIOD AFTER CADAVERIC
ORTHOTOPIC LIVER
TRANSPLANTATION: THE ROLE
OF IMAGING
Tesi Scuola Specializzazione
Radiodiagnostica
Pisa
Candidato: Relatore:
Lorenzo Cini Prof. Carlo Bartolozzi
Abstract
Purpose
To evaluate the role of imaging - Doppler Ultrasound (US) and/or multidetector row computed tomography (MDCT) - performed within 30 days after orthotopic liver
transplantation (OLT) in a prospective cohort of patients. Current imaging schedule was validated and patient-and procedure-related factors that could prompt a different
management investigated.
Material and Methods
Patients submitted to OLT at the Pisa University Hospital in the period between 1 January 2014 and 25 March 2015 were prospectively enrolled. US and Doppler US were routinely scheduled one month after surgery and earlier Doppler US or MDCT performed in case of clinical or laboratory abnormalities. Analysis of clinical, operative, procedural, and
radiologic findings was performed to determine the incidence of vascular complications, biliary complications, large hematomas/fluid collections, extra-hepatic complications.
Logistic regression analysis was used to analyze which factors among age, sex, donor age (>65 years and > 80 years), cause of liver disease (HCV-, HBV-,alcool-related cirrhosis) and presence of hepatocellular carcinoma were predictive of an earlier (within 30 days) positive imaging.
Results
One-hundred and twentyfive subjects were enrolled. Fifty patients out of 125 (40%) received early imaging for clinical or laboratory abnormalities; 31/125 patients (25%) had postoperative complications depicted by imaging. Seventyfive out of 125 patients (60%) underwent Doppler US about 30 days after OLT; in 64/125 (51,2%) Doppler US did not
show any abnormal findings, 11/125 (8,8%) had positive Doppler US at 30 days
examination in the absence of clinical or laboratory signs and 4/125 (3,2%) underwent interventional radiology procedures or ERCP. At logistic regression analysis no variable was determined as significant in predicting a positive earlier imaging, apart from a slight significance of female sex. In particular donor age, higher than 65 years and 80 years, was not demonstrated to be a significant variable in predicting the need of an earlier imaging.
Conclusions
Planning a first Doppler US at 30 days after OLT, reserving earlier imaging by Doppler US and MDCT in the case of clinical or laboratory abnormalities, allow to correctly diagnose and treat complications after OLT.
Introduction
Orthotopic liver transplantation (OLT) has become the major treatment for end-stage chronic liver disease and for severe acute liver failure. Currently, 1-year, 3-year, and 5-year patient survival rates are 88%, 80 % and 74 %, respectively. The improvement in survival can be attributed to better patient selection and preparation, advances in organ preservation, improved immunosuppressive therapy agents, and refinement of surgical techniques. However, despite great technological and immunological advances in the field of liver transplantation, there are still significant complications that can lead to increased morbidity, graft loss and death. It is known that these complications might occur early (<3 months) or late (>3 months) after transplantation and can result from imperfect surgical techniques or due to protracted ischemic or immunogenic injury. [1] [2] [3]
OLT requires donor-to recipient surgical anastomosis of the hepatic artery, portal vein, inferior vena cava, and bile duct (Fig.1). Dysfunction at these anastomotic sites often results in transplant dysfunction. Therefore complications of liver transplantation are usually divided into three categories: vascular (stenosis and thrombosis of the hepatic artery, portal vein, and inferior vena cava), biliary (strictures, bile leak, obstruction and infection, stone formation), and graft (acute rejection, ischemia, infarction, abscess, hematoma) abnormalities ( Fig.2). [4]
Diagnosis of acute rejection, one of the most serious complications after liver transplantation, is established with graft biopsy and histologic study .The role of imaging methods consists of excluding the other complications, which can have clinical signs and symptoms similar to acute rejection. Doppler ultrasonography (US) is routinely performed in OLT for assessment of the hepatic parenchyma, biliary tree, and vasculature. US is sensitive but not specific in the evaluation of peritransplant fluid collections. Bile, lymph, blood and pus can all present on imaging as a simple fluid collection. Multidetector row CT (MDCT) scanner is accepted as a practical noninvasive diagnostic method in various complications after OLT. MDCT imaging is usually performed for the evaluation of postoperative collections, vascular complications, or if the ultrasound examination is technically unsatisfactory. Magnetic resonance imaging (MRI) is not routinely performed
Fig.1. Liver transplantation anatomy. Drawing illustrates an orthotopic liver transplant, with
the surgical anastomotic sites in the portal vein (1), bile duct (2), inferior vena cava (3), and hepatic artery (4). From Singh A K et al. Radiographics 2010;30:339-351
Fig.2. Chart illustrates the classification of post-surgical complications of OLT.
and is genereally reserved to study of late-onset complication, in particular biliary complications, for its capacity of intra and extrahepatic biliary tree depiction. [5] [6]
The aim of this study was to evaluate the role of imaging - Doppler US and/or MDCT - performed within 30 days in a prospective cohort of patients submitted to OLT. Current imaging schedule was validated and patient- and procedure-related factors that could prompt a different management investigated.
Material and methods
PatientsWe prospectively included all patients who underwent OLT at Pisa University Hospital in the period between 1 January 2014 and 25 March 2015. In our transplantation center, Doppler US and MDCT are not routinely performed in the early period (within 30 days) in a regular post-transplantation course. Anticipated imaging studies are required in the presence of clinical (fever, abdominal pain, loss of consciousness, nausea and vomiting), or laboratory (leukocytosis, anemia, hyperbilirubinemia) abnormalities. MDCT is performed in case of positive findings at Doppler US, following a normal Doppler US in the presence of high clinical suspicion of abdominal complications and as a first imaging modality when a extra-abdominal complication is suspected (respiratory failure, central nervous system symptoms).
Doppler US is usually scheduled 30 days after OLT by an experienced radiologist in order to evaluate liver parenchyma, hepatic artery and portal anastomoses, intrahepatic arterial doppler signal, systemic veins, biliary tree and contingent fluid collections. MRI is reserved for further evaluation of biliary abnormalities seen with US and CT and is not generally performed in the early period post-transplantation (Fig.3).
Imaging techniques
Doppler US examinations were performed by using latest generation ultrasound systems (Philips iU 22 equipped with C5-1 curved array transducer or Siemens Acuson s2000 equipped with 6C2 transducer). MDCT examinations were performed by using a 64 or 128 slices MDCT scanner (Somatom\5 Syngo CT 2009\E, Siemens or GE LightSpeed 7.0 CT Scanner System, GE Medical Systems). Our imaging protocol included abdomen
examination performed before and after the intravenous injection of non-ionic contrast material (90 -120 ml, 320 to 400 mg of iodine per milliliter) via a power injector (injection flow-rate, 3 to 5 mL\sec). Early arterial phase of upper abdomen was acquired with bolus trigger technique, positioning of the respective region of interest in the abdominal aorta, with a threshold of 100 HU. Following scanning included late arterial phase (35-40 sec), portal-venous phase with a delay of 70-80 sec and delayed phase at 180 sec after the start of the injection. Chest was evaluated, when clinically recommended, before and after intravenous injection of contrast material in arterial and venous phase. Tube voltages were 100 or 120 KVp and automatic adjustment for mAs was used. Examination parameters for Somatom/5 Syngo CT (Siemens) were: collimation 64.0x2.0x0.6mm for early arterial and portal venous phases, and 24.0x3.0x1.0mm for late arterial and delayed phases.; rotation time 0.5 sec; pitch 1.2. Examination parameters for GE Lightspeed 7.0 CT scanner system (GE) were: collimation 64.0x2.5x1.0 mm for early arterial, late arterial, portal venous and delayed phases.; rotation time 0.5 sec; pitch 1.2.
Images were reconstructed with a 1 mm thickness and were evaluated using a picture archiving and communication system (Esaote-Fuji); post-processing with multiplanar reconstructions and three-dimensional reformatting techniques such as maximum intensity projection (MIP) and volume rendering (VR) was performed on a dedicated workstation (Advantage Workstation 4.4, GE Medical System)
Imaging findings
Doppler US examination included a real-time morphologic evaluation of liver parenchyma and color mapping of hepatic artery, portal vein, hepatic veins and inferior vena cava. Spectral analyses of the right and left hepatic arteries were performed to measure peak systolic and diastolic velocities. Spectral analyses for the hepatic vein, portal vein and inferior vena cava were also obtained. The right and left hepatic artery resistive index (RI) was calculated according to the formula:
resistive index (RI) = peak systolic velocity - end-diastolic velocity peak systolic velocity
The normal hepatic artery Doppler waveform shows a rapid systolic upstroke with continuous diastolic flow. The acceleration time, which represents the time from end-diastole to the first systolic peak,should be less than 0.08 sec, and the RI should be > 0,5.
PISA POST-OLT IMAGING PROTOCOL
The shape of the waveform was evaluated for evidence of the “tardus parvus” pattern. Hepatic artery complications - including thrombosis and stenosis - were suspected in the presence of one or more of the following Doppler criteria: RI <0.5, acceleration time >0.08 sec, no flow in the main hepatic artery, or a peak hepatic artery velocity > 2 m/sec. The normal portal vein Doppler waveform is a continuous flow pattern toward liver with mild velocity variations induced by respiration. The normal Doppler appearance of the hepatic veins hepatic veins and inferior vena cava shows a phasic flow pattern, reflecting the physiologic changes in the blood flow during the cardiac cycle [7] [8] [9]. Caliber of intrahepatic biliary tree, correct positioning of the T-tube and the presence of fluid collections, ascites, pleural fluid were evaluated.
Abdominal MDCT images are evaluated for the assessment of liver parenchyma and vasculature. The presence of enlarged abdominal lymphnodes, fluid collections, ascites are also evaluated. In the case of chest CT pulmonary parenchyma and vessels are assessed for the presence of pulmonary embolism, pneumonia, pneumothorax and severe pleural effusion.
Right-sided mild pleural effusion, minimal ascites, perihepatic hematoma, and periportal edema are recognized as normal post-transplantation imaging findings.
Data acquisition and analysis
Analysis of clinical, operative, procedural, and radiologic findings was performed to determine the incidence of vascular complications, biliary complications, large hematomas/ fluid collections, extra-hepatic complications. Logistic regression analysis was used to analyze which factor among age, sex, donor age (>65 years and > 80 years), cause of liver disease (HCV-, HBV-,alcool-related cirrhosis) and presence of hepatocellular carcinoma were predictive of an earlier (within 30 days) positive imaging.
Logistic regression was perfomed by using an online calculator (http://statpages.org/ logistic.html) for one exposure variable and summary data. Regression coefficient, Standard Errors, Odds Ratios, p value and 95% Confidence Limits were calculated for each variable. P value less than 0.05 was considered statistically significant.
Results
Between 1 January 2014 and 25 March 2015 127 subjects (96 M, and 31 F; age range 24– 68 years, mean 56 years, median 54.5 years) were submitted to OLT at our Center. Two of them died respectively during surgery and in the first perioperative period without undergoing any abdominal radiological examination; final patient populations included 125 subjects (96 M, and 29 F; age range, 24– 68 years, mean 55 years, median 54,4 years).
Fifty patients ( 40%) received early imaging ( 32 Doppler US, 49 MDCT, 1 MRI) for clinical or laboratory abnormalities. Thirty one patients ( 25%) had postoperative complications depicted by imaging. Among 29 patients who underwent both Doppler US and CT we found 2 hepatic artery thrombosis, 6 hepatic artery stenosis, 2 partial portal vein thrombosis, 1 portal vein stenosis, 1 inferior vena cava partial thrombosis, 1 subcapsular hepatic hematoma, 1 hepatic abscess, 4 large abdominal collections, 1 pancreatitis, 7 pulmonary consolidation, 1 pulmonary edema. In 1 patient head CT demonstrated intracranial hemorrhage and in 1 patient an abdominal corpuscolate fluid collection - not revealed by US - was depicted by MDCT. In 1 case biliary leakage suspect at US was confimed by MRI colangiography. One patient had biliary anastomotic leak 21 days after OLT and subsequently developed a right hepatic artery pseudoaneurysm. In 19 ( 15%) patients imaging did not depict significative findings; 2 of them underwent ultrasound guided liver biopsy for persistent laboratory abnormalities.
Patients with vascular arterial complications at early imaging were treated with re-OLT (1), angioplasty (2), angioplasty and stenting (4); biliary complications were treated with percutaneous biliary drainage (1), ERCP and biliar endoprosthesis insertion (1), a fluid collection was treated with ultrasound guided percutaneous drainage (1).
Portal and IVC complications, hepatic abscess, abdominal collections, pancreatitis, all the thoracic findings and the hemorrhagic stroke where treated with medical therapies and underwent radiological follow-up.
Seventyfive (60%) patients underwent routine Doppler US 30 days after OLT; in 64 no abnormal finding was demonstrated, however 9 out of them underwent US guided liver biopsy for persistent abnormal laboratory findings. Eleven patients (8,8%) had postoperative complications depicted by imaging.; we found 2 intrahepatic biliary sludge (CT not performed), 1 intrahepatic sludge and mild biliary anastomotic stenosis, 2 hepatic artery stenosis, 1 hepatic artery kinking, 1 sovrahepatic vein partial thrombosis, 1
pancreatitis with gastroduodenal artery pseudoaneurysm, 1 large organized collection in the hepatorenal recess, 1 pneumonia (chest CT after US demonstration of bilateral abundant pleural effusion), 1 anasarca and pulmonary consolidation probably in correlation with CMV infections. All patients underwent second level imaging and radiological follow-up when necessary.
In this latter group of patients vascular arterial complications where treated with angioplasty and stenting (2), one biliary complications was treated with ERCP (1), the large collection in the hepatorenal space was treated with ultrasound guided percutaneous drainage (1), the hepatic artery kinking underwent just diagnostic angiography because of a too high risk to benefit ratio, all the other complications required medical therapies only; one patient of this group underwent US guided liver biopsy .
At logistic regression analysis the only variable that significantly correlated with the outcome of an earlier (within 30 days ) positive imaging was female sex (p=0.03, OR 2.97, 95%CI 1.09-8.05). Results are reported in detail in table 1.
Variable Regression Coefficient
SD Odds ratio 95%CI P value Male sex -1,0886 0,5093 0,3367 0,1241 - 0,9137 0,0326
Female sex 1,0886 0,5093 2,97 1,0945 - 8,0595 0,0326
Donor age >65ys 0,3624 0,4609 1,4368 0,5823 - 3,5457 0,4316
Donor age >80ys -0,2472 0,4752 0,7810 0,3077 - 1,9822 0,6029
HCV+ cirrhosis -0,1374 0,4966 0,9978 0,3644 - 2,0736 0,7561 HBV+ cirrhosis -0,2189 0,2233 1,0732 0,3795 - 2,1145 0,9978 A l c o o l r e l a t e d cirrhosis 0,0377 0,5975 1,0385 0,3220 - 3,3494 0,9496 Presence of HCC -0,2828 0,4527 0,7537 0,3103 - 1,8305 0,5323 Table.1. Results of logistic regression analysis to examine early (within 30 days) positive
Fig.3c. Hepatic Artery thrombosis, VR MDCT image
Fig.4b. Hepatic Artery Stenosis, US Doppler
Fig.4d. Hepatic Artery Stenosis, 3D VR MDCT image
Fig.5a. Biliary leakage, US image
Discussion
Patients who are candidates for liver transplantation are those with acute liver failure (fulminant hepatic failure) or chronic liver disease for which conventional treatment is unavailable or has ceased to be effective. Fulminant hepatic failure, a disorder that ordinarily affects young people, causes a large portion of liver tissue to be destroyed in a short time, leading to failure of liver function, changes in mental status (hepatic encephalopathy), infections, and kidney failure. Chronic liver diseases that may be treated by transplantation include chronic hepatitis B and C, autoimmune chronic hepatitis, primary biliary cirrhosis, primary sclerosing cholangitis, alcoholic liver disease, and drug induced liver injury. Hereditary disorders of metal metabolism including hemochromatosis and Wilson disease (involving disordered iron and copper metabolism) also may require transplantation. Liver transplantation has long been accepted as a very good, and arguably the best treatment for early HCC because while radically removing the cancer it treats the two main limitations imposed by the cirrhotic liver on liver resection, namely the diminished hepatic reserve and the recurrence of de novo tumors in the residual liver; so early stages of primary liver cancer are now accepted as a leading indication to LT , while o t h e r m a l i g n a n c i e s s u c h a s c h o l a n g i o c a r c i n o m a s , h e p a t o b l a s t o m a s , hemangioendotheliomas, and liver metastases from neuroendocrine tumors are still proposed for transplant in individual cases, while permanently lacking reproducible selection criteria based on scientific evidence. [10] [11] [12]
After surgery, the patient ordinarily spends 1 to 3 days in the intensive care unit and then moves to the ward. The average hospital time after the procedure is about 10 days to 2 weeks.
Despite great technological and immunological advances in the field of liver transplantation, there are still significant complications that can lead to increased morbidity, graft loss and even death. Complications of liver transplantation are usually divided into three categories: vascular, biliary and others. [13]
Diagnosis of acute rejection, one of the most serious complications after liver transplantation, is established with graft biopsy and histologic study. The role of imaging methods consists of excluding the other complications, which could have clinical signs and symptoms similar to acute rejection. [14] [15]
In our study we evaluated all patients who underwent OLT in our transplantation center between 1 January 2014 and 25 March 2015, in order to assess their clinical and
radiological history with a particular focus on the early period (30 days). During the early period, the most frequent events are vascular complications, such as hepatic artery stenosis and thrombosis or portal vein thrombosis, so that a close monitoring of the anastomotic vessels, the tissue perfusion and the microcirculation is necessary. Clinical presentations of vascular complications vary from mild elevation of hepatic function tests to hepatic failure. Because the clinical presentation is so varied, their early detection and adequate management are important elements for ensuring graft and patient survival after OLT. For this reason, imaging studies can be particularly helpful in finding or eliminating vascular complications from the differential diagnosis. [16] [17] [18]
Doppler US is the primary modality used to search possible perihepatic fluid collections and to evaluate the hepatic vasculature in the post-transplantation period. [19] [20] [21]
According to some authors the reported sensitivities of Doppler US for the detection of hepatic artery stenosis and thrombosis are, respectively, 80–85% and 60–80%. Some authors reports an accuracy of Doppler US for the diagnosis of hepatic artery thrombosis of 92%. Doppler US can show false positive finding of hepatic artery thrombosis, probably from hepatic edema, systemic hypotension or arterial spasm. False-negative results may be due to the development of subacute extensive arterial collaterals that produce an arterial signal on the Doppler sonogram, leading to the diagnosis of a suffering artery.
In cases where Doppler US results are inconclusive or clinical suspicion of a complication persists despite normal sonographic findings, CT should be performed.
Unlike US, CT is not as dependent on the operator’s skill performing the study or on the patient’s body habitus. In particular, MDCT offers excellent spatial and temporal resolution, that combined with post-processing of the imaging data using a variety of three-dimensional reformatting techniques such as maximum intensity projection (MIP) and volume rendering (VR) allows to depict hepatic vasculature anatomy efficiently and accurately. Moreover, MDCT has several advantages over other imaging modalities. Compared with catheter angiography, MDCT angiography is non-invasive and cost effective. [22] [23] Digital subtraction angiography (DSA) allows a concomitant angioplasty-stenting procedure under some circumstances; however, it is not an ideal screening test because of the associated high cost and invasive nature of the procedure with the associated risks and potential complications.
In addition, despite the enormous improvement in post-OLT survival over the years, biliary tract complications lead to a risk of significant morbidity and mortality (2–7%).
Complications such as leaks, obstructions, strictures, and stones have been observed in 9% to 35% of large clinical series of liver transplant recipients. In our hospital, in the first period after OLT MR study is not routinely used, considering that biliary complications usually occur later in the post-operative course after surgery. After T-tube removal (after three months), MR studies allow complete visualization of the extra-hepatic bile ducts and biliary anastomosis (choledocho-choledocho-stomy) in nearly all the investigated subjects. [2]
Advanced donor age is a composite surrogate of poor liver graft quality. Different deceased donor scoring systems have been reported in the international literature with the aim of gauging the impact of donor age on the outcome of LT.However, during the last decade some investigators have illustrated excellent early- and middle-term results with donors >70 or >80 years, especially when optimal donor managementand recipient selection strategies are used, and in the absence of additional risk factors for graft loss. The demographic characteristics of the Tuscany population, the epidemiology of brain death and the deceased donor organizational model in place in our region all account for the large proportion of very old (≥80 years) donors reported annually. The demographic characteristics of the Tuscany population, the epidemiology of brain death and the deceased donor organizational model in place in our region all account for the large proportion of very old (≥80 years) donors reported annually. Liver pool might be safely expanded by using marginal and extemely marginal liver grafts from decease donors. [24] [25]
According to our center imaging protocol for patient submitted to OLT a anticipated imaging (within 30 days) is required in the presence of clinical or laboratory abnormalities. Doppler US is usually performed first and CT is used as a confirmatory imaging modality or after inconclusive US. Fifty patients(40%) received early imaging ( 32 Doppler US, 49 MDCT, 1 MRI) for clinical or laboratory abnormalities. Thirty one patients (25%) had postoperative complications depicted by imaging. In 19 (15%) patients imaging did not depict significative findings; 2 of them underwent ultrasound guided liver biopsy for persistent laboratory abnormalities. Eleven out of 125 patients (8,8%) had positive Doppler US at 30 days examination in the absence of clinical or laboratory signs and 4 patients ( 3,2%) underwent interventional radiology procedures or ERCP. At logistic regression no variable was determined as significant in predicting a positive earlier imaging, apart from a slight significance of female sex. In particular donor age, higher than 65years and 80 years, was not demonstrated to be a significant variable in predicting the need of an earlier
imaging. It can be therefore concluded that planning a first Doppler US at 30 days after OLT, reserving earlier imaging by Doppler US and MDCT in the case of clinical or laboratory abnormalities, allow to correctly diagnose and treat complications after OLT.
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