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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 32  |  Issue : 1  |  Page : 112-119

Computed tomography perfusion correlated with shear wave elastography in assessing the severity of chronic liver diseases


1 Department of Radiology, Faculty of Medicine, Menoufia University, Shebin El-Kom, Menoufia Governorate, Egypt
2 Department of Radiology, National Liver Institute, Menoufia University, Shebin El-Kom, Menoufia Governorate, Egypt

Date of Submission19-Mar-2018
Date of Acceptance06-May-2018
Date of Web Publication17-Apr-2019

Correspondence Address:
Bassuoni A. A. Bassuoni
Abo Hanefa Street, El-Shouhada 32717, Menoufia Governorate
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_129_18

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  Abstract 


Objective
The objective of this study was to assess the efficacy of computed tomography (CT) perfusion for quantitative measurement of hepatic perfusion as an useful tool in the evaluation of the severity of chronic liver diseases in correlation with shear wave elastography.
Background
CT perfusion is a noninvasive, safe technique for quantifying hepatic perfusion parameters, which is correlated significantly with the severity of chronic liver disease.
Patients and methods
This prospective study was carried out from October 2016 to December 2017, 80 patients with chronic liver disease and 20 patients without liver disease (control group) underwent CT perfusion and shear wave elastography (acoustic radiation force impulse imaging). Using the Child–Pugh classification for chronic liver disease patients, 35 patients were classified as Child A, 35 as Child B, and 10 as Child C. Total blood flow, total blood volume, hepatic perfusion index (HPI), mean transit time, and total liver perfusion for both liver lobes were measured for all patients.
Results
Total blood flow tended to decrease with the severity of chronic liver disease. HPI of the control group was significantly different from those of Child B and C, so HPI correlated significantly with the degree of fibrosis and linear relationship with acoustic radiation force impulse imaging results. However, there were changes in total blood volume and mean transit time between each groups, but not significant.
Conclusion
CT perfusion is a noninvasive technique for quantifying hepatic perfusion parameters and is useful tool for the evaluation of the severity of chronic liver diseases.

Keywords: elastography, hepatic perfusion index, liver cirrhosis, liver perfusion, mean transit time


How to cite this article:
El-Kholy MR, Mousa WA, Elsakhawy MM, Bassuoni BA. Computed tomography perfusion correlated with shear wave elastography in assessing the severity of chronic liver diseases. Menoufia Med J 2019;32:112-9

How to cite this URL:
El-Kholy MR, Mousa WA, Elsakhawy MM, Bassuoni BA. Computed tomography perfusion correlated with shear wave elastography in assessing the severity of chronic liver diseases. Menoufia Med J [serial online] 2019 [cited 2019 May 24];32:112-9. Available from: http://www.mmj.eg.net/text.asp?2019/32/1/112/256083




  Introduction Top


Liver fibrosis is a slowly progressing disease in which healthy liver tissue is replaced with scar tissue ended with liver cirrhosis, with a variety of causes, including viral, drug-induced, autoimmune, cholestatic, and metabolic diseases [1]. Fibrosis is an important cause of liver dysfunction and portal hypertension [2]. There is increasing evidence that, unlike cirrhosis, fibrosis is treatable and reversible in its early stages [3],[4]. Cirrhosis is the 12th leading cause of death by disease according to the National Institutes of Health. So knowledge of the stage of fibrosis is crucial for patient care because patients with mild disease should be monitored and those with advanced disease must be treated [5],[6].

The diagnosis of liver fibrosis is usually based on histological findings after liver biopsy. However, this procedure has inherent risks and it is prone to interobserver variability and sampling errors [7]. Therefore, there is obvious need for the development of noninvasive assessment of liver fibrosis, with possibility of whole liver examination, eliminating sampling errors, and reducing biopsy-related risk.

Currently, several methods are available for assessing hepatic fibrosis and progression of fibrogenesis including scintigraphy, magnetic resonance diffusion-weighted imaging, and magnetic resonance spectroscopy could differentiate between cirrhosis or severe fibrosis and normal liver. However, an accurate staging of fibrosis or diagnosis of mild fibrosis was often not achievable [8]. These techniques have not been accepted as the standard methods because of low spatial resolution or poor reproducibility.

Perfusion imaging in liver fibrosis is based on the occurrence of substantial microcirculatory changes in this disease. It has been previously shown that perfusion changes occur early during fibrosis in chronic hepatitis C virus (HCV) infection and perfusion computed tomography (CT) can compare the changes in perfusion parameters measured with CT perfusion in patients with and without chronic liver disease [9].

The aim of this study was to assess the ability of CT perfusion in the diagnosis of liver fibrosis, liver cirrhosis with evaluate severity of chronic liver disease with shear wave elastogrpahy results correlation.


  Patients and Methods Top


This prospective study was carried out on 100 patients who underwent CT perfusion examination during the period from October 2016 to December 2017 the in National Liver Institute, Menoufia University. Of these, 20 patients were without liver disease (group I, seven women, 13 men, age range: 32–63 years, mean ± SD: 44.5 ± 9.9 years); 80 patients were with chronic liver diseases (29 women, 51 men, age range: 30–70 years, mean: 51 ± 9.8 years). According to the Child–Pugh classification, 35 patients were classified as Child A (group II), 35 as Child B (group III), and 10 as Child C (group IV). The study protocol was approved by the Medical Ethics Committee of Faculty of Medicine, Menoufia University. After an informed consent taken from each patient included in the study, all the patients underwent CT perfusion and shear wave elastography on the same day.

Inclusion criteria

Both sexes are included: patients who were diagnosed to had chronic liver diseases without present hepatic focal lesions.

Exclusion criteria

  1. Lactating and pregnant women: Patients known to had high serum creatinine
  2. Patient preparation: All the patients included were subjected to take a detailed medical history, general examination, laboratory investigations were done such as complete blood count and liver biochemical tests and informed instruction on breath-holding during the procedure
  3. Equipment and drugs used: multislice wide-bore gantry SOMATOM Definition Flash CT Scanners 128 slices (Siemens Healthineers Global, Erlangen, Germany), workstation (Syngo via Client; Seimens Healthcare Medical Systems) with CT perfusion software (Syngo. CT body perfusion), for shear wave elastograhy use Philips iU22 ultrasound machine with its C5–C1 curvilinear transducer (Philips Ultrasound, Bothell, Washington, USA), intravenous cannula (18–20 G), 60 ml of non-ionic-iodinated contrast medium: iopromide (Ultravist 300 mg of iodine/ml; Bayer Healthcare).


Procedure

All the patients included in this study were fasting for 8 h before the procedure. Acoustic radiation force impulse imaging (ARFI) was done, an intravenous cannula of size 18 G was inserted, every patient was positioned supine on the CT table in the 'head first' position with his arm resting comfortably above the head. Patients were taught how to hold breath during examination when requested, to ensure their cooperation. Abdominal scout was acquired in the anteroposterior view. Precontrast axial cuts were taken during a breath-hold at the end of inspiration. The coverage area starts from the level of the top of the right diaphragmatic copula (Hepatic Dome) till 20 cm caudally (end of iliac crest). After interested liver parenchymal cuts localization, a 3 cm region was selected based on the precontrast series for the dynamic study. A dynamic study of the selected area was performed in a single breath-hold at the end of inspiration at a static table position, the total amount of contrast medium was injected at a rate of 5 ml/s. Scanning was initiated after a 4 s delay from the start of injection, and images were acquired for a total duration of 40 s. Data analysis was processed at a workstation, functional data were calculated by the following steps: Displaying images at an appropriate window, such as soft tissue for the abdomen (width = 400 HU, level = 40 HU), obtaining a reference arterial input curve by placing a region of interest (ROI) in the aorta manually ensuring that the ROI did not include any mural calcification. Obtaining a reference venous input curve by placing an ROI in the main portal vein or portal vein branch and spleen manually, ROI was drawn in, liver parenchymal perfusion values were calculated averaging the functional parameters across all four sections and displayed as: tables of blood flow (BF), blood volume (BV), mean transit time (MTT), and hepatic perfusion index (HPI) value functional maps of BF and HPI. These functional maps were displayed in colors ranging from blue to red, blue being the lower range of display for BF and HPI and red being the upper range of display.

Statistical analysis

Statistical analysis was done by an IBM personal computer (SPSS Inc., Chicago, Illinois, USA) software package, version 20.0. Two types of statistics were done: descriptive statistics: for example, percentage (%), mean, SD, and range. Analytic statistics: for example, P value of less than 0.001 was considered statistically significant.


  Results Top


CT perfusion was carried out for 100 adult patients. The technique was successfully performed in 100 (95%) patients, with 5% failure rate due to marked obesity and rapid respiratory movement, of whom 64 (67%) were men and 36 (33%) were women with a mean age of 51 ± 9.8 years. Eight (8%) patients had negative HCV and 92 (92%) had positive HCV.

According to the laboratory investigation, patients were classified according to Child classification as follows: 20 patients without liver diseases (control group: 20%) [Figure 1], 35 (35%) patients with Child A classification, 35 (35%) patients with Child B classification, and 10 (10%) patients with Child C classification [Figure 2] and [Table 1].
Figure 1: A male patient of 43 years with normal liver profile, normal ultrasound for liver parenchyma. Used as control at the study. Acoustic radiation force impulse imaging study of about 4.6 kPa, denoting F0 and no fibrosis. Homogeneous liver parenchyma, smooth outline surface at the triphasic computed tomographic (CT) study (a and b), (c) selection of regions of interest (ROIs), (d) dynamic curve of each ROI, (e) functional map of blood flow (BF) (red = high BF, blue = low BF), (f) functional map of hepatic perfusion index (HPI) (red = high HPI, blue = low HPI), (g) table of CT perfusion parameters of ROIs. CT perfusion parameters: BF = 105.13 ml/min/100 g, blood volume = 14.63 ml/100 g, mean transit time = 10.26 s, and HPI = 13.89%. There was a high blood flow with low hepatic perfusion index; these are the natural changes that occur within normal liver parenchyma.

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Figure 2: A male patient of 64 years with abdominal enlargement and hepatitis C virus-positive, low serum albumin (2.1 g/dl), and elevated serum total bilirubin (3.5 mg/dl), Child C 11 according to Child–Pugh classification. Acoustic radiation force impulse imaging study of about 25.5 kPa, denoting F4 and advanced fibrosis and cirrhosis. Coarse liver parenchyma, irregular outline surface, moderate splenomegaly, and mild ascites at triphasic computed tomographic (CT) study (a and b), (c) selection of regions of interest (ROIs), (d) dynamic curve of each ROI, (e) functional map of blood flow (BF) (red = high BF, blue = low BF), (f) functional map of hepatic perfusion index (HPI) (red = high HPI, blue = low HPI), (g) table of CT perfusion parameters of ROIs. CT perfusion parameters: BF = 77.09 ml/min/100 g, blood volume = 11.53 ml/100 g, mean transit time = 13.04 s, and HPI = 43.12%. There was high HPI with lower BF; these mean that the patient had significant liver cirrhosis.

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Table 1: Different types of groups, number of patients, and mean age of each group at our study

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ARFI mean values of the control group was 4.6 ± 0.65 kPa. The ARFI mean values of patients with Child A, B, and C were 8.278 ± 1.15, 14.84 ± 6.7, and 27.54 ± 3 kPa, respectively [Table 2].
Table 2 Mean values of shear wave elastography grading: acoustic radiation force impulse imaging, total blood flow, total blood volume, total liver perfusion, mean transit time, and hepatic perfusion index parameters of four groups and relation in between four groups

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The mean values of total blood flow (TBF), total blood volume (TBV), MTT, total liver perfusion (TLP), and HPI of the control group were 106 ± 2.7 ml/min/100 g, 13.78 ± 1.7 ml/100 g, 11.88 ± 2.2 s, 102.45 ± 1.6 ml/min/100 ml, and 19.78 ± 2.4%, respectively. The mean values of TBF, TBV, MTT, TLP, and HPI of patients with Child A were 99.74 ± 4.4 ml/min/100 g, 13.12 ± 1.6 ml/100 g, 12.55 ± 1.4 s, 75.5 ± 1.7 ml/min/100 ml, and 19.49 ± 2.9%, respectively. The mean values of TBF, TBV, MTT, TLP, and HPI of patients with Child B were 90.73 ± 4.8 ml/min/100 g, 13.12 ± 1.6 ml/100 g, 12.55 ± 1.4 s, 74.8 ± 1.9 ml/min/100 ml, and 30.24 ± 1.9%, respectively. The mean values of TBF, TBV, MTT, TLP, and HPI of patients with Child C were 79.43 ± 3.1 ml/min/100 g, 12.9 ± 2.2 ml/100 g, 12.89 ± 1.7 s, 56.8 ± 1.2 ml/min/100 ml, and 40.93 ± 3.1%, respectively [Table 2].

There were significant differences at TBF and TLP in between the control group in comparison with Child A, B, and C groups; Child A and B groups with Child C group (P < 0.001, each), but no significant difference was found between Child A and B groups. So TBF and TLP tended to decrease with the severity of chronic liver disease [Figure 3].
Figure 3: Perfusion parameters according to the severity of chronic liver disease. Top left: hepatic tissue blood flow (TBF, ml/min/100 g). Top right: hepatic blood flow (TBV, ml/min); middle left: mean transit time (MTT, s); middle right: hepatic perfusion index (HPI, %); bottom left: total liver perfusion (TLP, ml/min/100 ml); bottom right: fibrosis rate by acoustic radiation force impulse imaging (kPa). TBF of the liver parenchyma of patients with Child C was significantly lower than that without liver disease (P < 0.001). HPI of the liver parenchyma increased significantly with the severity of chronic liver disease. A significant difference in the HPI of the liver parenchyma was seen between patients without liver disease and Child A and those with Child B and C (P < 0.001), and between patients without liver disease and those with Child B and C (P < 0.001).

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HPI of the control group was significantly different from those of Child B and C and Child A with B and C (P < 0.001, each), but no significant difference between the control group and the Child A group [Figure 3].

However, there were changes in TBV and MTT between each groups, but no significant differences [Figure 3].

HPI was the best single factor used in the evaluation of severity of liver diseases. HPI correlated significantly with the degree of fibrosis (P < 0.001). In comparison with shear wave results, HPI correlated significantly with the proportions of shear wave grading of fibrosis [Figure 4].
Figure 4: Illustrative curve demonstrating the relationship between hepatic perfusion index (HPI) and the fibrosis rate measured by acoustic radiation force impulse imaging. Note that there was significant linear relationship between HPI and rate of fibrosis (P < 0.001).

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  Discussion Top


Liver fibrosis is a progressive condition that if diagnosed early and staged accurately allows early clinical intervention that may arrest or slow down progression to end-stage decompensated cirrhosis. The spectrum of chronic liver disease and fibrosis that leads to end-stage decompensated cirrhosis is an important cause of morbidity and mortality in the world [10]. Early diagnosis and staging of liver fibrosis is aimed at avoiding the progression from normal to minimal to significant fibrosis and timely management of patients with advanced disease.

The current gold standard in the diagnosis and staging of liver fibrosis is liver biopsy. But it is invasive, has a complication rate, and is subject to intraobserver and interobserver variability [11]. Because of the imperfect nature of liver biopsies, over the last several years there has been a growing trend to validate noninvasive tools to diagnose and stage liver fibrosis.

Noninvasive measurement perfusion of parenchymal organs has long been a domain of scintigraphy [12]. However, the major drawback of scintigraphic methods is their limited spatial resolution, also it is difficult to separate overlapping components of arterial and portal venous inflow of radiotracer represented in time–activity curves, though the liver receives a dual blood supply from the hepatic artery and the portal vein, thus resulting in a biphasic inflow of any radiotracer or contrast media [13].

Although diffusion-weighted MRI enabled to differentiate accurately mild (F1) and moderate fibrosis (F2) from advanced fibrosis stages (F3–F4), larger studies are needed to evaluate the influence of both diffusion and perfusion on apparent diffusion coefficient values in cirrhosis [14]. It was not possible to accurately discriminate normal, mild, and moderate fibrosis due to significant overlap of the corresponding apparent diffusion coefficient values [15]. MRI is associated with difficulties in the quantification of TBF, because signal enhancement of vessels and tissue by nonspecific MR contrast medium, such as gadolinium complex, does not show a linear correlation to the concentration of the contrast medium [16].

Sande et al. [17] reported that shear wave elastography is a noninvasive imaging tool in the diagnosis of liver fibrosis that has a sensitivity and specificity that almost parallels histological diagnosis from a liver biopsy and the staging of liver fibrosis at diagnosis uses a METAVIR scoring system that has been adapted by elastography. So we depend on shear wave elastography in the staging of liver fibrosis and cirrhosis instead of liver biopsy. Automatic median value generated by the ultrasound software was used to establish the elastography grade as follows: less than 4.6 = F0, 4.6–5.6 = F1, 5.7–7.0 = F2, 7.1–12 = F3, and more than 12 = F4 [18].

One advantage of the CT technique is the ability to assess perfusion at the capillary level, which is more directly related to the metabolic requirements of the tissue than BF in the supplying vessel. Quantification of hepatic perfusion on dynamic CT, introduced by Miles et al. [19], allowed separate evaluations of arterial and portal perfusion of the liver. To date, different methodologies, such as the maximum slope method and the dual-input one-compartmental model have been described [20].

In our study, we used the deconvolution method. We hypothesize that the different previous study parameters may have a certain discrepancy due to the difference in the selection of patients, etiopathogenesis, stage of liver disease, and its severity and sex distribution among the cirrhotic patients in previous studies with our study.

Our CT perfusion parameter of patients without liver disease was concordant with the normal values published in previous studies. Also perfusion parameters had changes in between groups of chronic liver disease is compared with patients without liver disease. We find that no significant changes at HPI, MTT, and TBV between normal group (F0–F1) and group II with minimal fibrosis (F1–F2). But there was a significant difference at TBV in between all groups, with patients without liver disease having a significantly higher difference than that of those with Child B and C liver diseases. The HPI of patients without liver disease (control group and Child A) was significantly lower than that of those with Child B and C liver disease. TLP significantly reduced with increased severity of liver diseases. However, the TBV and MTT showed a difference in between all groups, but not significant.

These results in agreement with Hashimoto et al. [21] reported that TBF tended to decrease with increased severity of chronic liver disease, but there was no significant difference in TBV and MTT between the groups. Hepatic arterial fraction of the liver parenchyma significantly increased with increased severity of chronic liver disease.

Also, Wang et al. [22] noted HPI, arterial liver perfusion, and TBF increased with the progression of liver fibrosis. BV had no marked change and portal venous perfusion decreased with the progression of liver fibrosis.

These changes at perfusion parameters due to the pathogenesis of liver fibrosis, which is activated by myofibroblasts derived from perisinusoidal hepatic stellate cells and portal or central vein fibroblasts proliferate and produce excess extracellular matrix, which leads to fibrous portal tract expansion, central vein fibrosis and capillarization of the sinusoids, and congestion of the space of Disse. Finally blood is shunted directly from the terminal portal veins and arteries into the central veins, with consequent portal hypertension [21]. So congestion at the space of Disse leading to a decreased flow rate of blood within the vascular space in the liver parenchyma, leading to decreased TBF. The increased vascular resistance in the cirrhotic liver reduces portal perfusion. The reduction of portal perfusion is buffered by liver arterialization, increasing the arterial fraction of liver perfusion, However, the increased arterial perfusion is often not sufficient to maintain TLP in cirrhosis because of the high extrahepatic portosystemic shunting, which explains the increased HPI and the reduction of TLP [23].

In contrast with our results, van Beer et al. [20] noticed a significant increased MTT in between cirrhotic patients and noncirrhotic patients. This difference due to difference in the type of method in analysis of liver perfusion and the different etiology of liver diseases, we used the deconvolutional mode in CT perfusion and patients with chronic hepatitis post-HCV infection. In contrast, they used a dual-input single-compartment model that was used at CT perfusion analysis and with different etiologies of liver diseases.

Also, Guan et al. [24] were the first to focus on the use of CT perfusional changes in the early stage of fibrosis in an animal model. They demonstrated that the differences in hepatic arterial fraction and MTT at different stages of the test group were significant, and the differences in BV and BF between hepatitis and hepatic cirrhosis, hepatic fibrosis, and early stage of hepatic cirrhosis were significant; there was no significant difference in BV and BF between hepatitis and hepatic fibrosis.

Chen et al. [25] showed the MTT to be higher in patients with decompensated liver cirrhosis than those with compensated liver cirrhosis in patients with different types of etiology of liver cirrhosis.

Ronot et al. [9] noticed that the MTT to be significantly higher in patients with intermediate fibrosis in comparison to patients with minimal fibrosis and there was a large amount of overlap in the parameters in the different patient groups, and neither portal venous nor TLP were found to be independent; also they did not found changes in other perfusion parameters that have previously been described in liver cirrhosis, such as an increase in arterial perfusion. They published work focusing on human patients who had early stages of the disease which is asymptomatic. In contrast, we focused on the advanced fibrotic stages, at which the clinical manifestations start to appear and compared the perfusional changes between normal patients with different stages of Child–Pugh classification patients.

Li et al. [26] noted that the perfusion parameters hepatic blood flow and hepatic arterial perfusion were increased in cirrhotic liver parenchyma without hepatocellular carcinoma compared with the controls; however, the differences were not significant. Also HBV were lower in cirrhotic liver without hepatocellular carcinoma compared with the control group.

Moreover, Ma et al. [27] noted significantly decreased MTT in the liver cirrhosis group than the control group. They used male Wistar rats with chemical induction of liver cirrhosis with intraperitoneal injection of diethyl nitrosamine, but we used human patients with chronic hepatitis C with different stages of liver fibrosis up to cirrhosis.

Fortunately our study let us found that TBF, HPI, and TLP have changes in between groups which was significantly altered in accordance with the degree of cirrhosis, but best single factor was HPI used to evaluate the severity of liver diseases. In comparison with shear wave results we found that HPI correlated significantly with the shear wave grading of fibrosis. Liver biopsy suffered from lack of exact matching between the ROIs analyzed at CT perfusion, we overcame this problem using shear wave elastography, which covers a large area of liver tissue more than biopsy. We could hypothesize that changes in perfusion parameters in patients over time could help with patient monitoring and avoidance of repeated biopsies. These results suggest that the value of CT perfusion can be useful for long-term follow-up of patients with chronic liver disease.

Limitations

First, the aorta and portal vein should always be included in the scan section for the calculation process. Second, a maximum of 30 mm width could be scanned on cine-mode, thus limiting the study to cover only the portahepatis area.

During our experiment, the procedure showed a failure rate of about 5. Overall, 3% resulting from excessive respiratory movement and 2% resulting from marked obesity resulting in low signal/noise ratio.


  Conclusion Top


CT perfusion is a noninvasive, safe technique for quantifying hepatic perfusion parameters and is a useful tool for the evaluation of the severity of chronic liver diseases.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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