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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 8  |  Issue : 3  |  Page : 108-115

Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid-enhanced T1 mapping to evaluate liver damage caused by Clonorchis sinensis


Department of Radiology, Guangxi Medical University, Nanning, China

Date of Submission09-Mar-2021
Date of Acceptance04-Aug-2021
Date of Web Publication5-Apr-2022

Correspondence Address:
Prof. Jinyuan Liao
The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/RID.RID_26_21

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  Abstract 


OBJECTIVE: The objective of the study is to explore the feasibility of Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid (Gd-EOB-DTPA) T1 mapping for evaluating liver damage caused by Clonorchis sinensis infection in rabbit models.
MATERIALS AND METHODS: Forty-two rabbits were randomly divided into a control group (n = 10), mild infection group (n = 12), moderate infection group (n = 9), and severe infection group (n = 11). All rabbits underwent an magnetic resonance imaging scan and pathological examination to obtain the relaxation time before Gd-EOB-DTPA enhancement and the relaxation time after Gd-EOB-DTPA enhancement at intervals of 10, 15, 20, 25, 30, 35, and 40 min. The Ishak score was used to evaluate the inflammation and fibrosis of the liver.
RESULTS: The severity of C. sinensis infection was positively correlated with liver inflammation. The T1 relaxation time of liver increased with increasing inflammation. The highest correlation was recorded between inflammation and the T1 relaxation time at 30 min (P = 0.001). After enhancement, The T1 relaxation time has a significant difference between the severe infection group and control group and between the severe infection group and mild infection group. The area under the receiver operating characteristics curve showed that the T1 relaxation time was the most effective parameter for diagnosing the degree of inflammation at 30 min.
CONCLUSIONS: Gd-EOB-DTPA-enhanced T1 mapping can be used to evaluate the liver damage caused by C. sinensis infection.

Keywords: Clonorchis sinensis, gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid, imaging, liver damage, T1 mapping


How to cite this article:
Xiang Y, Li N, Zhou Z, Fang J, Liao J. Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid-enhanced T1 mapping to evaluate liver damage caused by Clonorchis sinensis. Radiol Infect Dis 2021;8:108-15

How to cite this URL:
Xiang Y, Li N, Zhou Z, Fang J, Liao J. Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid-enhanced T1 mapping to evaluate liver damage caused by Clonorchis sinensis. Radiol Infect Dis [serial online] 2021 [cited 2022 May 28];8:108-15. Available from: http://www.ridiseases.org/text.asp?2021/8/3/108/342632




  Introduction Top


Clonorchiasis is a disease caused by the Clonorchis sinensis parasite (Chinese or oriental liver fluke). C. sinensis is an important foodborne pathogen and a major cause of liver disease, especially in Asia. Specifically, its prevalence has been documented in South Korea, China, Japan, Taiwan, the Indo-China Peninsula and the far east of Russia,[2],[3],[4] where eating undercooked or raw fish is a cultural practice. After eating raw or undercooked freshwater fish containing metacercariae, excystation takes place in the duodenum with the emergence of a juvenile adult fluke. Within 4–7 h after ingestion of the intermediate host, the juvenile adult moves to the bile ducts through the ampulla of Vater, where it further develops into the C. sinensis.[1] Although it is mainly found in the biliary system of the liver, some studies have occasionally reported its presence in the pancreas. Thus, C. sinensis, and clonorchiasis, the disease caused by it, are an important public health problem.[5]

The pathogenic factors of C. sinensis include mechanical damage to the bile duct, inflammation, erosion of the epithelial lining of bile ducts, blockage of the ducts following thickening of scar tissue, secondary bacterial infection, excretory and secretory products (ESP), and metabolite secretion and excretion.[6],[7],[8] These factors are deleterious to the hepatobiliary duct. The pathological manifestations of the disease include edema and necrosis of hepatocytes, adenomatoid hyperplasia of bile duct epithelium, mucin secretion metaplasia, bile duct dilatation, dysplasia or canceration of bile duct cells, and inflammation and fibrosis around the bile duct.[6],[9] Clinically, although symptoms such as dull pain and indigestion in the liver area disappear after the treatment of C. sinensis, pathological changes such as intrahepatic bile duct dilatation, mucosal hyperplasia, and bile duct and surrounding fibrosis persist.[10] However, despite all these factors, the quantitative evaluation criteria for Clonorchiasis disease and related liver damage are still rather limited. Therefore, it is necessary to establish a noninvasive and effective method to evaluate biliary and liver damage in patients with clonorchiasis.

Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid (Gd-EOB-DTPA) is a liver-specific contrast agent that can be specifically absorbed by organic anion transporting polypeptides and an organic anion transport peptide on hepatocytes. Gd-EOB-DTPA has the potential to relatively reflect the metabolic function of hepatocytes,[11] and previous studies have shown that liver function can be evaluated with Gd-EOB-DTPA-enhanced magnetic resonance imaging (MRI).[12],[13],[14] The various serological methods for evaluating liver function can only evaluate the whole liver function; they cannot evaluate and predict the residual liver function on a local basis. In contrast, MRI can obtain anatomical information of the liver more intuitively and comprehensively than pathological and serological indexes. In this study, Gd-EOB-DTPA T1 mapping was used to evaluate liver injury in rabbits infected with C. sinensis, with the long-term intention of developing a quantitative evaluation method for determining clinical efficacy and prognosis.


  Materials and Methods Top


All the experimental animals were purchased from the Experimental Animal Center of Guangxi Medical University. All rabbits were raised in independently ventilated cages in a constant temperature and 12-h alternating light and darkroom. The animals were given a standard diet and water.

Extraction of Clonorchis sinensis eggs

Wild wheat ear fish (Pseudorasbora parva) infected with C. sinensis were caught in the waters of an epidemic area of Hengxian County, Guangxi. After the fish scales, bones, and internal organs were removed, the fish was stirred into minced meat. The minced fish meat was then put into a conical flask and artificial digestive juice was added. This juice was composed of 98.4% normal saline, 1% hydrochloric acid (HCL) (12 mol/L), and 0.6% pepsin (13,000, from pig stomach, Sangon Biotech, China). For every 10 ml of the digestive juice, 1 g of fish mince was used. The minced fish was fully mixed with artificial digestive juice and digested at 37°C for 12 h in a constant temperature oscillator. The digested mixture was then filtered out using a sieve and mixed with twice the volume of water in a cone measuring cup. After standing for 20 min, the liquid in the upper layer was discarded and the same amount of water was added to the contents. This was repeated several times, after which the liquid in the measuring cup was clarified. The bottom sediment was collected and the metacercariae of C. sinensis were picked out under a somatotype microscope. The collected pathogens were then concentrated, counted, and stored at 4°C to await the next processing stage.

Preparation of the rabbit model of liver trematode infection

Sixty rabbits were randomly divided into six groups. The rabbits in the five experimental groups were infected with 100, 200, 400, 600, or 800 metacercariae, depending on the specific group. The infection method was as follows. After the rabbits were anesthetized with pentobarbital sodium solution (20 mg/kg), a no. 8 rubber catheter was inserted into the stomach and the metacercaria were injected into the tube by an infusion device and washed through with normal saline. The control group was perfused with the same amount of normal saline.

Fecal egg examination

After 30 days of intragastric administration, the feces of the rabbits in the infected groups were collected. A 1-g sample of feces from each rabbit was obtained and put into a 20-ml centrifuge tube. The samples were then independently soaked in 5 ml of dilute HCL and softened for 10 min. Ether was then added to the sample and the contents were thoroughly shaken. After centrifuging for 3 min at 3000 G, 200 mL of sediment were dropped onto glass slides, covered with cover slips, and the eggs detected using a × 40 magnification microscope. Those rabbits in whose feces eggs were detected were considered to be successfully infected.

Magnetic resonance imaging examinations

After 90 days of intragastric administration, all rabbits were examined using MRI. After 12 h of fasting, the rabbits were injected with 30 mg sodium pentobarbital through the ear vein, which was washed through with 2 ml of normal saline. The rabbits were also injected with 1 ml heparin sodium (100 U/ml) contrast agent. In this experiment, all the MRI data were acquired using a Siemens Prisma 3.0-T MRI system with an 8-channel phased-array animal coil. After transverse and coronal haste T2-weighted imaging (T2WI) and transverse Blade T2WI were acquired to obtain general imaging features, the Gd-EOB-DTPA-enhanced transverse T1-weighted imaging vibe sequence was acquired to obtain T1-mapping images. The Gd-EOB-DTPA contrast medium (0.25 mol/L Bayer, Germany) was injected at a dose of 0.1 ml/kg within 3 s and washed with 2 ml of saline. After injection of the contrast medium, scanning was performed over 10–40 min with T1 mapping every 5 min. The MRI parameters used are shown in [Table 1].
Table 1: Magnetic resonance imaging pulse sequence and scanning parameters

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Image processing

The image data were transferred to a Prisma work station for postprocessing. The T1 mapping pseudocolor image was generated by calculating T1 vibe images with multiple inversion angles. The measurement method was as follows. First, the region of interest (ROI) position was determined on T2WI, with a low position less-influenced by respiratory movement being selected, to avoid interfering with the bile duct and blood vessels in the middle level of the right posterior lobe. Three ROIs of 0.1 cm2 were selected around the bile duct and were thereafter copied to the T1 mapping images at each time point to ensure that the position of the ROIs was the same. The average of the three ROIs was regarded as the T1 relaxation time of the hepatic lobe.

Pathological evaluation

After scanning, all the rabbits were killed and their livers were removed immediately. Liver tissue samples measuring about 2 cm × 1 cm × 2 mm were cut off the middle of the hepatic lobe perpendicular to the direction of the bile duct. The cut tissues were then soaked in formalin tissue-fixation solution for more than 24 h and embedded in paraffin wax. The paraffin wax blocks were sliced and stained with hematoxylin–eosin and Massonand nh slice. The samples were imaged and saved using an Olympus Intelligent pathological Microscopy system (BX53 + DP80). The inflammatory activity of the liver was then scored according to the Ishak scoring system[15] by pathologists with a working experience of 15 years. According to the methods of Jing et al.,[16] tissue inflammation was divided into no hepatitis activity (score of 1–4), mild hepatitis (score of 5–8), moderate hepatitis (score of 9–12), and severe hepatitis (score of 13–18).

Statistical analysis

Data are expressed as mean ± standard deviation. Single factor analysis of variance was used to analyze differences in T1 relaxation time of rabbit liver according to different degrees of infection. Levene's test was used to test the homogeneity of variance. When the variance was uneven, Welch's test was used, and the least-significant difference method was used for paired comparisons after the event. Spearman rank correlation was used to analyze the correlation between Ishak score and the number of infected metacercariae, as well as the correlation between T1 relaxation time and the degree of infection. The area under the receiver operating characteristics (ROC) curve was used to compare the diagnostic efficiency of T1 mapping in different stages. P < 0.05 was taken to indicate a statistically significant difference.


  Results Top


Modeling

Of the 60 rabbits, 9 died of anesthetic accident, 9 died of malnutrition, diarrhea, and pulmonary infection, and the remaining 42 rabbits completed the experiment, including 10 rabbits in the control group. Of the 32 remaining experimental rabbits, 6 belonged to the 100 cysticercosis group, 6 belonged to the 200 group, 9 belonged to the 400 group, 6 belonged to the 600 group, and 5 belonged to the 800 group. On the 30th day, fecal examination confirmed that all the rabbits in the experimental groups were successfully infected with C. sinensis. We combined the 100 and 200 metacercaria groups into a mild infection group, considered the 400 metacercaria group as the moderate infection group, and the 600 and 800 metacercaria groups combined into a severe infection group. Finally, all animals were divided into four groups: the control group (n = 10), mild infection group (n = 12), moderate infection group (n = 9), and severe infection group (n = 11).

Pathological results

The livers of the control group were ruddy and bright red with a soft texture. With an increase in the degree of liver injury in the experimental groups, the liver was reddish brown, the texture was hard, and granular nodular changes were observed on the surface of part of the liver [Figure 1]. Microscopic observation showed that the pathological manifestations of the experimental groups were in accordance with the Ishak liver inflammatory activity score standard [Figure 2]. The Ishak score results and liver inflammation classification in each group are reported in [Table 2]. The severity of hepatitis in each group increased along with increasing severity of infection. The Spearman correlation coefficient between the hepatitis score and infection severity was 0.372, P = 0.030, and the correlation coefficient between hepatitis severity and infection severity was 0.389, P = 0.014.
Figure 1: General observation of the liver. (a) Control group liver, smooth and soft; (b) Granular nodular changes can be seen on the surface of infected liver; (c) Cross-section of the hepatic lobe from an infected animal showing bile duct thickening and dilatation

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Figure 2: Microscopic pathological findings in the experimental group: (a) inflammatory cell infiltration (×100, HE-stained) (b) inflammatory cell infiltration, hepatocyte necrosis (×200, HE-stained) (c) Normal hepatocyte (×200, HE-stained) (d) C. sinensis (×100, HE-stained) (e) peri-biliary collagen deposition (×100, HE-stained) (f) pseudolobular formation (×100, Masson's trichrome)

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Table 2: Ishak score for hepatitis and hepatitis severity grouping in each infection group

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Magnetic resonance imaging scan results

T2WI showed that the bile ducts of the experimental group animals were significantly more dilated than those of the control group. The Gd-EOB-DTPA enhanced the hepatobiliary phase, with contrast medium retention being observed in the dilated bile duct [Figure 3].
Figure 3: Magnetic resonance imaging scan results. (a) Experimental group T2-weighted imaging showing bile duct dilatation; (b) Experimental group T1-weighted imaging plain scan; (c) Experimental group hepatobiliary phase T1-weighted imaging at 30 min delay showing contrast medium retention; (d-f) control group liver

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The T1 mapping results showed that the T1 relaxation time of the liver decreased significantly after enhancement, then gradually increased with the prolongation of scanning delay time [Figure 4]. The T1 relaxation time of liver was positively correlated with the degree of infection at each time point [Table 3]. The T1 relaxation time of liver was prolonged in relation to the extent of aggravation of the infection. The highest correlation (r = 0.555) was recorded at 30 min, followed by 20 min (r = 0.525). The correlation coefficients at 15 and 25 min were 0.491 and 0.498, respectively. There was a significant difference in the T1 relaxation time of liver between the severe infection group and control group (P < 0.05). The results of the postenhancement scanning revealed a significant difference between the severe infection group and mild infection group (P < 0.05). Similarly, there was a significant difference in the T1 relaxation time of the liver between the severe infection group and mild infection group (P < 0.05). There were also significant differences between the severe infection group and mild infection group for each phase of the postenhancement scanning (P < 0.05). The results showed the T1 relaxation time has significant difference between moderate and severe infection groups in 10 and 25 min postenhancement. To the contrary, there was no significant difference between the control and the mild infection groups, between the control and the moderate infection groups, or between the mild infection and moderate infection groups [Table 4].
Figure 4: T1 mapping results. (a) The mean and standard deviation of the T1 relaxation times in each phase scan. There is a positive correlation between T1 relaxation time and the degree of infection. (b) The average change in T1 relaxation time in each group. 0 min represents preenhancement

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Table 3: Correlation between T1 relaxation time and infection degree at different time points

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Table 4: Statistical analysis of liver T1 relaxation time at different time points in each group

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The 15-30-min scan phase with high correlation between T1 relaxation time and infection degree was analyzed using ROC curves. The diagnostic ability of T1 mapping for determining infection degree was calculated, and the area under the curve (AUC) was used to express the ability to distinguish each infection degree [Figure 5]. The sum of the AUC was largest at 30 min, at which time the AUC of the control group versus mildly infected group–severely infected group was 0.70, with a cut-off value of 383.6. The AUC for the control group–mildly infected group vs. moderately infected group was 0.83, with a cutoff value of 392.1. The AUC for the control group–moderately infected group versus the severely infected group was 0.90, with a cutoff value of 423.9.
Figure 5: ROC analysis of the diagnostic ability of T1 mapping in assessment of liver damage. Three ROC curves are displayed for each period to indicate the ability of the T1 mapping scheme to distinguish each fibrous stage. The sums of the areas under the three curves were 2.35 at 15 min, 2.40 at 20 min, 2.35 at 25 min, and 2.43 at 30 min

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  Discussion Top


Liver injury caused by C. sinensis is a complex pathological process that includes not only mechanical blockage but also a series of biochemical and immune injuries. Liver fluke parasites in the bile duct first damage the bile duct epithelium, then damage the hepatocytes around the bile duct, causing hepatocyte necrosis, inflammation, and collagen deposition, resulting in the decline of liver function. In our study, we used the degree of liver inflammation and fibrosis to represent the severity of liver damage. Our results showed that the liver Ishak score was positively correlated with the extent of clonorchiasis infection. Gd-EOB-DTPA is a gadolinium-based contrast medium transported by functional hepatocytes through an active transport system involving factors such as organic anion transport peptides. Intracellular uptake of Gd-EOB-DTPA may be reduced because of impaired liver function.[17] Quantitative evaluation of liver function using Gd-EOB-DTPA-enhanced MRI has become a hot topic in recent years. There are two ways to evaluate liver function based on signal intensity and T1 relaxation time. Haimerl et al.[18] found that the signal intensity and relative increase of the 20-min signal were significantly correlated with liver function. Nakagawa et al.[19] showed that the T1 relaxation time of the hepatobiliary phase was highly correlated with indocyanine green clearance. Haimerl et al.,[20] through the indocyanine green test, considered that the index measured with T1 relaxation was better than that based on signal intensity.

The Gd-EOB-DTPA-enhanced MRI evaluated in our study is based on conventional clinical imaging schemes, which can not only accurately diagnose focal liver lesions but also provide additional information. Based on this advantage, T1 mapping in the hepatobiliary phase can be used to quantitatively evaluate liver function by measuring T1 relaxation time. To evaluate liver function, scoring systems such as the Child-Pugh score and model for end-stage liver diseases are used in the clinical environment. Pan et al.[21] found that the T1 relaxation time of normal subjects was significantly different from that of patients with liver cirrhosis at 20 min after injection of Gd-EOB-DTPA. Furthermore, the authors reported that in patients with liver cirrhosis, T1 relaxation time increased significantly with Child–Pugh rating. Other studies have shown that the value of T1 relaxation time in the evaluation of liver function is similar to that of the Child–Pugh system.[22] The common imaging findings of C. sinensis include intrahepatic bile duct dilatation, bile duct wall thickening, filling defect, and biliary stricture.[23] In our study, the anatomical MRI scans of rabbits infected with clonorchiasis showed an increase in intrahepatic bile duct and dilatation of bile duct, which are consistent with previous descriptions.[24],[25] In the hepatobiliary phase of the enhanced scan, contrast media retention appeared in the dilated bile duct, which has not been found in previous studies as far as we know. The possible explanation for these results is that the bile duct could be blocked by C. sinensis, which makes it difficult for Gd-EOB-DTPA to be excreted smoothly from the bile duct. The enhancements of bile duct wall and lumen filling defect, as reported by Jeong et al.,[23] were not observed in this experiment, which may be due to a lack of scanning resolution and the interference caused by animal breathing movement.

In our study, all animals were divided into different infection groups based on the number of metacercariae administered. The T1 relaxation time of liver was measured before enhancement and over 10–30 min after enhancement. There was always a positive correlation between T1 relaxation time and the severity of infection. For all rabbits with severe infection, the T1 relaxation times before and after enhancement were significantly higher than those in the control group and also significantly higher than those in the mild infection group. These results may be related to lower uptake of Gd-EOB-DTPA because of liver damage and the disturbance to excretion caused by bile duct injury. Some studies have shown that with the aggravation of liver fibrosis, the expression of organic anion transport peptides and multidrug resistance-related proteins decreases.[26] Organic anion transport peptides and multidrug resistance-related proteins mediate the molecular structure of hepatocyte uptake and excretion of Gd-EOB-DTPA. Therefore, a decrease in them may lead to a decrease in contrast agent uptake and excretion, which may explain the molecular protein mechanism found in this study.

The T1 relaxation times were no significant difference between the control group and mild infection group, the control group and moderate infection group, and the mild infection group and moderate infection group. This suggests that the T1 relaxation time method may be sensitive only to severe liver damage. Our analysis of the AUC of the ROC curve of T1 relaxation time in the detection of the degree of infection showed that diagnostic efficacy was strongest at 30 min, which may be caused by the postponement of the hepatobiliary phase because of the disturbed Gd-EOB-DTPA uptake and excretion caused by liver damage.

The current research has some limitations. First, there were not enough rabbits to complete all the experiments. Thus, the number of samples was limited and might have negatively influenced the even distribution of severity of hepatitis in the experimental groups. Further experiments are needed to increase the sample size. Second, because there is no accurate standard for the pathological evaluation of liver inflammation caused by C. sinensis, the Ishak scoring system for viral hepatitis was used in this experiment. Therefore, there may be some errors in the pathological evaluation of liver inflammation in this experiment. Nonetheless, this study suggests that Gd-EOB-DTPA-enhanced T1 mapping has value for evaluating liver damage caused by C. sinensis infection and provides a quantitative imaging method for clinical evaluation of C. sinensis infection.


  Conclusion Top


In summary, Clonorchiasis Characteristic findings of MRI are the intrahepatic bile ducts dilation diffusely, and on the Gd-EOB-DTPA enhanced hepatobiliary phase, the contrast medium retention in the dilated bile duct can be observed. T1 mapping is a useful tool for quantitative evaluating the liver damage caused by C. sinensis infection.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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