Case Control Study Open Access
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Cases. Jan 26, 2019; 7(2): 130-136
Published online Jan 26, 2019. doi: 10.12998/wjcc.v7.i2.130
Correlation analysis of collagen proportionate area in Budd-Chiari syndrome: A preliminary clinicopathological study
Fu-Liang He, Fu-Quan Liu, Department of Interventional Therapy, Beijing Shijitan Hospital, Capital Medical University, Beijing 100038, China
Chuan Li, Xing-Shun Qi, Liver Cirrhosis Study Group, Department of Gastroenterology, General Hospital of Shenyang Military Area, Shenyang 110016, Liaoning Province, China
Chuan Li, Section of Medical Services, General Hospital of Shenyang Military Area, Shenyang 110016, Liaoning Province, China
ORCID number: Fu-Liang He (0000-0003-1643-1465); Chuan Li (0000-0002-1130-9260); Fu-Quan Liu (0000-0001-7710-6135); Xing-Shun Qi (0000-0002-9448-6739).
Author contributions: He FL, Li C, and Liu FQ contributed equally as co-first authors; Liu FQ and Qi XS designed the study; He FL, Li C, and Qi XS wrote the manuscript.
Supported by the National Natural Science Foundation of China, No. 81500474; and Training Programme Foundation for Beijing Talents, No. 2016000021469G206.
Institutional review board statement: The study was approved by the ethics committee of Beijing Shijitan Hospital of the Capital Medical University.
Informed consent statement: All patients gave informed consent.
Conflict-of-interest statement: No conflict of interest.
STROBE statement: The STROBE checklist has been confirmed.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Xing-Shun Qi, MD, Vice-Chief Physician, Liver Cirrhosis Study Group, Department of Gastroenterology, General Hospital of Shenyang Military Area, No. 83 Wenhua Road, Shenyang 110016, Liaoning Province, China. xingshunqi@126.com
Telephone: +86-24-28897606 Fax: +86-24-28851113
Received: October 19, 2018
Peer-review started: October 19, 2018
First decision: November 15, 2018
Revised: December 1, 2018
Accepted: December 12, 2018
Article in press: December 12, 2018
Published online: January 26, 2019
Processing time: 100 Days and 4.8 Hours

Abstract
BACKGROUND

Collagen proportionate area (CPA) is an important index for assessing the severity of liver fibrosis. Budd-Chiari syndrome can frequently progress to liver fibrosis and cirrhosis. CPA might play an important role in the pathological progress of Budd-Chiari syndrome.

AIM

To explore the role of CPA in predicting the outcomes of patients with Budd-Chiari syndrome.

METHODS

Nine patients with Budd-Chiari syndrome undergoing transjugular intrahepatic portosystemic shunt (TIPS) were included. The median CPA level and correlation of CPA and prognosis of TIPS were determined.

RESULTS

Median CPA was 23.07% (range: 0%-40.20%). Pearson’s χ2 test demonstrated a significant correlation of CPA with history of gastrointestinal bleeding (Pearson’s coefficient: 0.832, P = 0.005), alanine aminotransferase (Pearson’s coefficient: -0.694, P = 0.038), and prothrombin time (Pearson’s coefficient: 0.68, P = 0.044). Although CPA was not significantly correlated with shunt dysfunction or hepatic encephalopathy after TIPS, the absolute CPA was relatively larger in patients who developed shunt dysfunction or hepatic encephalopathy after TIPS.

CONCLUSION

This preliminary clinicopathological study found a marginal effect of CPA on the outcomes of Budd-Chiari syndrome patients treated with TIPS.

Key Words: Budd-Chiari syndrome; Hepatic vein; Occlusion; Thrombosis; Fibrosis

Core tip: In the nine patients recruited for the study, we found a marginal effect of collagen proportionate area on the outcomes of Budd-Chiari syndrome patients treated with transjugular intrahepatic portosystemic shunt.



INTRODUCTION

Liver histology represents a clinically important tool for assessing the severity of liver fibrosis and the presence of liver cirrhosis in chronic liver diseases[1]. The conventional liver histological assessment systems, such as Knodell, Metavir, and Ishak scores, are semi-quantitative[2-4]. Recently, collagen proportionate area (CPA), a novel parameter that is fully quantitative for assessing the fibrotic area in liver tissues, has been developed and widely explored. CPA refers to the ratio of the area of collagen to the area of tissue. Early studies found that CPA was significantly correlated with Ishak stage, and that CPA, but not Ishak stage, was independently associated with hepatic venous pressure gradient[5]. Additionally, CPA can predict the risk of decompensation in liver transplant recipients with hepatitis C virus infection[6] and compensated cirrhotic patients with hepatitis C virus infection[7]. Evidence also suggests that CPA, rather than Laennec, Kumar, and Nagula semi-quantitative sub-classification parameters, septal thickness, and nodular size, predicts the risk of further decompensation in cirrhotic patients[8].

Budd-Chiari syndrome refers to the obstruction of hepatic venous outflow from hepatic veins to supra-hepatic inferior vena cava[9-11] and is classified as acute, subacute, and chronic according to the rapidity and extension of occlusion and clinical presentations[12]. Patients with acute and subacute forms of Budd-Chiari syndrome can present with acute hepatic failure due to extensive necrosis of hepatic tissues[10,11]. Most patients with the chronic form of Budd-Chiari syndrome progress to liver fibrosis and cirrhosis because of long-term hepatic congestion, and they often present with portal hypertension-related gastrointestinal hemorrhage as well as leg ulcers and abdominal varices[13].

Severity of liver fibrosis and cirrhosis may reflect the disease status of Budd-Chiari syndrome. Until now, the role of CPA has not been analyzed in patients with Budd-Chiari syndrome. We conducted a preliminary clinicopathological study to analyze the correlation between CPA and clinical and laboratory variables and clinical outcomes in such patients.

MATERIALS AND METHODS

We retrospectively reviewed patients with Budd-Chiari syndrome who were admitted to the Beijing Shijitan Hospital of the Capital Medical University who underwent transjugular intrahepatic portosystemic shunt (TIPS) between August 2016 and July 2017. Budd-Chiari syndrome was diagnosed according to the current consensus and practice guideline[10,11]. All eligible patients underwent contrast-enhanced computed tomography (CT) before TIPS and had liver biopsy specimens collected during TIPS procedures. Computer-assisted digital image analyses of picroSirius red stained liver histological sections were performed to calculate the CPA.

We collected data regarding demographic profile, history of other liver diseases, location of the obstruction, clinical presentations and signs, CT findings, and major laboratory test results. We recorded shunt dysfunction, hepatic encephalopathy and death events, time of shunt dysfunction and hepatic encephalopathy development, and time of death during follow-up. The patients were followed until February 2018, the last visit, or death.

Continuous data are presented as means with standard deviation and median with range. The categorical data are presented as frequency with percentage. Pearson’s χ2 test was performed to explore the correlation of CPA with other variables. Pearson’s coefficient with P value was calculated. A two-side P value of < 0.05 was considered statistically significant. All statistical analyses were performed using SPSS Statistics version 19.0.0 software (Armonk, NY, United States).

RESULTS

Nine patients (four males and five females) with Budd-Chiari syndrome were included. Median age was 29 years (range: 12-60 years). Patient characteristics are shown in Table 1. Among them, six patients had obstruction of all major hepatic veins, two patients had obstruction of inferior vena cava, three patients had a history of gastrointestinal bleeding, and seven patients had hepatic patchy enhancement on CT. Median CPA was 23.07% (range: 0%-40.20%). Two patients developed shunt dysfunction after TIPS and had a CPA of 32.5% and 23.07%, respectively. One patient developed hepatic encephalopathy after TIPS and had the largest CPA (40.2%). No patient died during follow-up.

Table 1 Patient characteristics.
VariablenFrequency [n (%), or mean ± SD]Median (range)
Age930.00 ± 15.7529.00 (12.00-60.00)
Gender (male/female)94 (44.4)/5 (55.6)
Hepatitis B virus90 (0)
Hepatitis C virus90 (0)
Alcohol abuse90 (0)
Vascular obstruction
IVC obstruction92 (22.2)
RHV obstruction98 (88.9)
MHV obstruction97 (77.8)
LHV obstruction99 (100.0)
All HVs obstruction96 (66.7)
Portal vein thrombosis90 (0)
Clinical presentations and signs
Hepatic encephalopathy before TIPS90 (0)
Gastrointestinal bleeding93 (33.3)
Abdominal pain92 (22.2)
Abdominal distension97 (77.8)
Abdominal varices91 (11.1)
Limb swelling91 (11.1)
Pigmentation91 (11.1)
Limb ulcer91 (11.1)
CT signs
Hydrothorax on CT93 (33.3)
Ascites on CT94 (44.4)
Splenomegaly on CT98 (88.9)
Hepatic patchy enhancement on CT97 (77.8)
Gastroesophageal varices on CT97 (77.8)
Paraesophageal varices on CT91 (11.1)
Laboratory tests
Hemoglobin (g/L)9122.67 ± 34.81127.00 (82.00-171.00)
White blood cell (109/L)96.86 ± 2.856.67 (2.99-12.48)
Platelet count (109/L)9122.22 ± 69.32109.00 (42.00-270.00)
Alanine aminotransferase (U/L)929.22 ± 17.5623.00 (13.00-71.00)
Aspartate aminotransferase (U/L)947.22 ± 20.9739.00 (18.00-71.00)
Alkaline phosphatase (U/L)9178.33 ± 69.20148.00 (96.00-288.00)
Gamma glutamyl transferase (U/L)993.44 ± 42.2184.00 (19.00-161.00)
Total bilirubin (mmol/L)986.98 ± 91.8142.80 (18.90-262.40)
Direct bilirubin (mmol/L)957.71 ± 68.4217.30 (6.20-180.00)
Albumin (g/L)936.19 ± 7.0839.60 (22.20-44.10)
Prothrombin time (s)955.67 ± 15.3356.00 (25.00-78.00)
International normalized ratio91.48 ± 0.431.37 (1.12-2.55)
Serum creatinine (mmol/L)951.00 ± 14.6550.00 (29.00-76.00)
Blood urea nitrogen (mmol/L)95.06 ± 1.515.15 (2.94-8.27)
Sodium (mmol/L)9134.78 ± 8.56138.00 (120.00-143.00)
Potassium (mmol/L)94.33 ± 0.644.17 (3.77-5.77)
Collagen proportionate area923.44 ± 13.8823.07 (0-40.20)
Shunt dysfunction after TIPS92 (22.2)
Hepatic encephalopathy after TIPS91 (11.1)

CPA was significantly correlated with prior history of gastrointestinal bleeding (Pearson’s coefficient: 0.832, P = 0.005), alanine aminotransferase (Pearson’s coefficient: -0.694, P = 0.038), and prothrombin time (Pearson’s coefficient: 0.68, P = 0.044) (Table 2). There was, however, no significant correlation between CPA and shunt dysfunction (Pearson’s coefficient: -0.168, P = 0.665) and hepatic encephalopathy (Pearson’s coefficient: -0.453, P = 0.221) after TIPS.

Table 2 Correlation analysis of collagen proportionate area.
VariablenPearson coefficientP value
Age90.3600.342
Gender (male/female)90.0380.922
Hepatitis B virus9NANA
Hepatitis C virus9NANA
Alcohol abuse9NANA
Vascular obstruction
IVC obstruction9-0.3900.300
RHV obstruction9-0.5020.168
MHV obstruction9-0.1360.726
LHV obstruction9NANA
All HVs obstruction9-0.4550.218
Portal vein thrombosis9NANA
Clinical presentations and signs
Hepatic encephalopathy before TIPS9NANA
Gastrointestinal bleeding90.8320.005
Abdominal pain9-0.2570.504
Abdominal distension9-0.0930.813
Abdominal varices9-0.3420.367
Limb swelling9-0.2330.547
Pigmentation9-0.3420.367
Limb ulcer9NANA
CT signs
Hydrothorax on CT90.1420.716
Ascites on CT9-0.0120.975
Splenomegaly on CT9-0.5020.168
Hepatic patchy enhancement on CT9-0.0370.924
Gastroesophageal varices on CT90.2190.572
Paraesophageal varices on CT90.6330.067
Laboratory tests
Hemoglobin (g/L)90.1570.687
White blood cell (109/L)9-.0250.949
Platelet count (109/L)90.2420.530
Alanine aminotransferase (U/L)9-0.6940.038
Aspartate aminotransferase (U/L)9-0.6420.062
Alkaline phosphatase (U/L)9-0.3580.344
Gamma glutamyl transferase (U/L)90.0800.837
Total bilirubin (μmol/L)9-0.3380.373
Direct bilirubin (μmol/L)9-0.4150.267
Albumin (g/L)90.3480.358
Prothrombin time (seconds)90.680.044
International normalized ratio9-0.6380.065
Serum creatinine (μmol/L)90.0190.962
Blood urea nitrogen (mmol/L)9-0.4110.272
Sodium (mmol/L)90.2720.478
Potassium (mmol/L)9-0.3760.319
Shunt dysfunction after TIPS9-0.1680.665
Hepatic encephalopathy after TIPS9-0.4530.221
DISCUSSION

Budd-Chiari syndrome is a rare vascular liver disease, which can progress into liver cirrhosis. Currently, TIPS is the mainstay treatment option for Budd-Chiari syndrome[14]. Despite favorable survival of patients with Budd-Chiari syndrome[15], a majority of patients treated with TIPS will experience adverse events, such as shunt dysfunction and/or hepatic encephalopathy. Common risk factors for the development of shunt dysfunction include type of stent and inferior vena cava obstruction. Risk factors for the development of hepatic encephalopathy include age, prior hepatic encephalopathy, and type of stent[1]. The present study for the first time explored whether CPA can predict the outcomes of Budd-Chiari syndrome patients after TIPS. However, we did not find any significant association of CPA with shunt dysfunction or hepatic encephalopathy. This unexpected phenomenon might be mainly attributed to the fact that this disease is so rare, and only nine patients were included. Additional explanation for this phenomenon could be the small proportion of patients who developed shunt dysfunction (n = 2/9) and hepatic encephalopathy (n = 1/9) in the present study. Indeed, it should be noted that only one patient developed hepatic encephalopathy, and this patient had the largest CPA (40.2%) among the included patients. Two patients developed shunt dysfunction and had a CPA equal to or beyond the median value (32.5% and 23.07%). This preliminary result encourages us to enlarge the sample size and confirm the predictive role of CPA.

Our study also found that CPA was positively associated with prior history of gastrointestinal bleeding and prothrombin time at baseline but negatively associated with alanine aminotransferase. These findings can be explained by the following fact. First, in patients with Budd Chiari syndrome, gastrointestinal bleeding is mainly attributed to the development of portal hypertension and secondary variceal bleeding, which is closely associated with progression of liver fibrosis. Second, prothrombin time is an important component of Child-Pugh and model for end-stage liver disease (commonly known as MELD) scores for assessing the outcomes of liver cirrhosis[16,17]. Third, a higher level of alanine aminotransferase reflects less frequent liver fibrosis but more frequent liver cell necrosis in patients with Budd Chiari syndrome[18].

In conclusion, this preliminary clinicopathological study found a marginal effect of CPA on the outcomes of Budd-Chiari syndrome patients treated with TIPS. Further study with a larger sample size should be carried out to confirm the present findings.

ARTICLE HIGHLIGHTS
Research background

Collagen proportionate area (CPA) is an important index for assessing the severity of liver fibrosis. Budd-Chiari syndrome can frequently progress to liver fibrosis and cirrhosis.

Research motivation

Clinically, we found that CPA might play an important role in the pathological progress of Budd-Chiari syndrome. We designed the study to investigate this hypothesis.

Research objectives

We conducted a preliminary clinicopathological study to explore the role of CPA in predicting the outcomes of patients with Budd-Chiari syndrome.

Research methods

Nine patients with Budd-Chiari syndrome undergoing transjugular intrahepatic portosystemic shunt (TIPS) were included. The median CPA level, correlation of CPA and patients’ history, and correlation of CPA and prognosis of TIPS were conducted.

Research results

The median CPA was 23.07% (range: 0%-40.20%). Pearson’s χ2 test demonstrated a significant correlation of CPA with a history of gastrointestinal bleeding (Pearson’s coefficient: 0.832, P = 0.005), alanine aminotransferase (Pearson’s coefficient: -0.694, P = 0.038), and prothrombin time (Pearson’s coefficient: 0.68, P = 0.044). Although CPA was not significantly correlated with shunt dysfunction or hepatic encephalopathy after TIPS, the absolute CPA was relatively larger in patients who developed shunt dysfunction or hepatic encephalopathy after TIPS.

Research conclusions

This preliminary clinicopathological study found a marginal effect of CPA on the outcomes of Budd-Chiari syndrome patients treated with TIPS. This study provides a new perspective for predicting the outcome of Budd-Chiari syndrome. In the future, more patients could be recruited in the study.

Research perspectives

In the future studies of Budd-Chiari syndrome and portal hypertension, emphasis should be placed on the correlation of pathological changes and outcomes of TIPS.

Footnotes

Manuscript source: Unsolicited manuscript

Specialty type: Medicine, research and experimental

Country of origin: China

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P- Reviewer: Goldaracena N, Park J S- Editor: Wang JL L- Editor: Filipodia E- Editor: Wu YXJ

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