Abstract
Background and aims
Non-invasive fibrosis assessment has been highly recommended in many liver diseases. However, comparative diagnostic accuracy of laboratory markers, ultrasound and magnetic resonance elastography (MRE) for fibrosis in autoimmune hepatitis (AIH) patients has not been established.
Methods
Medline, Embase and Cochrane Library were searched. Primary outcome was significant fibrosis (SF), advanced fibrosis (AF) and cirrhosis, defined as Metavir stage F ≥ 2, F ≥ 3 and F = 4 according to liver biopsy. Hierarchical summary receiver operating characteristic curve (ROC) model was used to evaluate diagnostic accuracy of non-invasive methods. Summary area under ROC (AUROC) and diagnostic odds ratio (DOR) with 95% confidence interval (CI) were calculated. The Grading of Recommendations Assessment, Development and Evaluation system was used to assess quality of evidence.
Results
Overall, 16 studies with 861 patients were included, comparing aspartate aminotransferase to platelet ratio index (APRI), fibrosis-4 index (FIB-4), aspartate aminotransferase/alanine aminotransferase ratio, transient elastography (TE), acoustic radiation force impulse, shear wave elastography and MRE versus liver biopsy. Among all non-invasive markers, TE had good performance for fibrosis staging. Summary AUROCs and DORs of TE were 0.90 (95% CI 0.87, 0.92) and 23.7, 0.91 (95% CI 0.89, 0.93) and 31.6, 0.89 (95% CI 0.86, 0.92) and 80.5 for staging SF, AF and cirrhosis, whereas APRI and FIB-4 showed poor performance for detecting AF (DOR, 4.6 and 4.7) and cirrhosis (DOR, 5.5 and 12.9).
Conclusions
TE performs well to stage liver fibrosis in patients with AIH, compared with other laboratory non-invasive indexes. Nevertheless, diagnostic accuracy of APRI and FIB-4 is poor.
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Abbreviations
- AIH:
-
Autoimmune hepatitis
- MRE:
-
Magnetic resonance elastography
- SF:
-
Significant fibrosis
- AF:
-
Advanced fibrosis
- ROC:
-
Receiver operating characteristic curve
- AUROC:
-
Summary area under ROC
- DOR:
-
Diagnostic odds ratio
- CI:
-
Confidence interval
- APRI:
-
Aspartate aminotransferase to platelet ratio index
- FIB-4:
-
Fibrosis-4 index
- AAR:
-
Aspartate aminotransferase/alanine aminotransferase ratio
- TE:
-
Transient elastography
- ARFI:
-
Acoustic radiation force impulse
- SWE:
-
Shear wave elastography
- HCC:
-
Hepatocellular carcinoma
- AASLD:
-
American Association for the Study of Liver Diseases
- EASL:
-
European Association for the Study of the Liver
- AST:
-
Aspartate aminotransferase
- ALT:
-
Alanine aminotransferase
- PC/SD:
-
Platelet count to spleen diameter
- NAFLD:
-
Non-alcoholic fatty liver disease
- PPV:
-
Positive predictive value
- NPV:
-
Negative predictive value
- QUADAS-2:
-
Quality Assessment of Diagnostic Accuracy Studies-2 scale
- GRADE:
-
The Grading of Recommendations Assessment Development and Evaluation
- LR+:
-
Positive likelihood ratio
- LR−:
-
Negative likelihood ratio
- ULN:
-
Upper limit normal
References
Michael PM, Ansgar WL, Diego V. Autoimmune hepatitis-update 2015. J Hepatol 2015;62:100–111
Wang Q, Yang F, Miao Q, et al. The clinical phenotypes of autoimmune hepatitis: a comprehensive review. J Autoimmun 2016;66:98–107
Czaja AJ, Carpenter HA. Progressive fibrosis during corticosteroid therapy of autoimmune hepatitis. Hepatology 2004;39:1631–1638
Montano-Loza AJ, Carpenter HA, Czaja AJ. Predictive factors for hepatocellular carcinoma in type 1 autoimmune hepatitis. Am J Gastroenterol 2008;103:1944–1951
Yeoman AD, Al-Chalabi T, Karani JB, et al. Evaluation of risk factors in the development of hepatocellular carcinoma in autoimmune hepatitis: implications for follow-up and screening. Hepatology 2008;48:863–870
Manns MP, Czaja AJ, Gorham JD, et al. Diagnosis and management of autoimmune hepatitis. Hepatology 2010;51:2193–2213
European Association for the Study of the Liver. EASL clinical practice guidelines: autoimmune hepatitis. J Hepatol 2015;63:971–1004
Rockey DC, Caldwell SH, Goodman ZD, et al. Liver biopsy. Hepatology 2009;49:1017–1044
Czaja AJ. Review article: the prevention and reversal of hepatic fibrosis in autoimmune hepatitis. Aliment Pharmacol Ther 2014;39:385–406
Wai CT, Greenson JK, Fontana RJ, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 2003;38:518–526
Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 2006;43:1317–1325
Xu Q, Sheng L, Bao H, et al. Evaluation of transient elastography in assessing liver fibrosis in patients with autoimmune hepatitis. J Gastroenterol Hepatol 2017;32(3):639–644
Guo L, Zheng L, Hu L, et al. Transient elastography (FibroScan) performs better than non-invasive markers in assessing liver fibrosis and cirrhosis in autoimmune hepatitis patients. Med Sci Monit 2017;23:5106–5112
Hartl J, Denzer U, Ehlken H, et al. Transient elastography in autoimmune hepatitis: timing determines the impact of inflammation and fibrosis. J Hepatol 2016;65(4):769–775
Sheptulina A, Shirokova E, Nekrasova T, et al. Platelet count to spleen diameter ratio non-invasively identifies severe fibrosis and cirrhosis in patients with autoimmune hepatitis. J Gastroenterol Hepatol 2016;31(12):1956–1962
Wang J, Malik N, Yin M, et al. Magnetic resonance elastography is accurate in detecting advanced fibrosis in autoimmune hepatitis. World J Gastroenterol 2017;23(5):859–868
Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011;155(8):529–536
Flahault A, Cadilhac M, Thomas G. Sample size calculation should be performed for design accuracy in diagnostic test studies. J Clin Epidemiol 2005;58(8):859–862
Kim JH, Kim MN, Han KH, et al. Clinical application of transient elastography in patients with chronic viral hepatitis receiving antiviral treatment. Liver Int 2015;35:1103–1115
Lee HW, Yoo EJ, Kim BK, et al. Prediction of development of liver-related events by transient elastography in hepatitis B patients with complete virological response on antiviral therapy. Am J Gastroenterol 2014;109:1241–1249
Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005;128:343–450
Loomba R, Wolfson T, Ang B, et al. Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 2014;60:1920–1928
Cui J, Heba E, Hernandez C, et al. Magnetic resonance elastography is superior to acoustic radiation force impulse for the diagnosis of fibrosis in patients with biopsy-proven nonalcoholic fatty liver disease: a prospective study. Hepatology 2016;63:453–461
Venkatesh SK, Wang G, Lim SG, et al. Magnetic resonance elastography for the detection and staging of liver fibrosis in chronic hepatitis B. Eur Radiol 2014;24:70–78
Huwart L, Sempoux C, Vicaut E, et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 2008;135:32–40
Xiao G, Yang J, Yan L. Comparison of diagnostic accuracy of aspartate aminotransferase to platelet ratio index and fibrosis-4 index for detecting liver fibrosis in adult patients with chronic hepatitis B virus infection: a systemic review and meta-analysis. Hepatology 2015;61:292–302
Xiao G, Zhu S, Xiao X, et al. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology 2017;66(5):1486–1501
de Oliveira AC, El-Bacha I, Vianna MV, et al. Utility and limitations of APRI and FIB4 to predict staging in a cohort of nonselected outpatients with hepatitis C. Ann Hepatol 2016;15:326–332
Acknowledgements
We are grateful to all cooperating organizations and their staff whose hard work made this study possible. ZRY is supported by the Cambridge Trust and the China Scholarship Council. Thanks to Prof. Jing Hua for supplying cut-off value, sensitivity and specificity of APRI and FIB-4 detecting advanced fibrosis.
Funding
This study is funded by Beijing Municipal Administration of Hospitals’ Youth Program (QML20170107) and Beijing Talents Fund (2016000021469G226). The sponsor had no role in study design, data collection, data analysis, data interpretation, or writing of the report.
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SSW and HY designed the study and drafted the manuscript. SSW, NZ, ZYH and JLZ extracted the data, SSW, ZRY, and SYZ evaluated the quality. SSW, ZRY, and SYZ assessed the quality of evidence by GRADE framework. SSW and ZRY analyzed the data. HY and JDJ interpreted the results, incorporated comments for the co-authors and finalized the manuscript. All authors approved the final version of the paper.
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Shanshan Wu, Zhirong Yang, Jialing Zhou, Na Zeng, Zhiying He, Siyan Zhan, Jidong Jia, and Hong You have no conflict of interests.
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Wu, S., Yang, Z., Zhou, J. et al. Systematic review: diagnostic accuracy of non-invasive tests for staging liver fibrosis in autoimmune hepatitis. Hepatol Int 13, 91–101 (2019). https://doi.org/10.1007/s12072-018-9907-5
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DOI: https://doi.org/10.1007/s12072-018-9907-5