Prevalence of Hepatic Fibrosis and Performance of Non-invasive Liver Fibrosis Scores in an Eastern Indian Diabetic Population with NAFLD
DOI:
https://doi.org/10.15605/jafes.040.02.16Keywords:
non-alcoholic fatty liver disease (NAFLD), vibration-controlled transient elastography (VCTE), fibrosis-4 index (FIB-4), NAFLD-fibrosis score (NFS), AST to platelet ratio index (APRI)Abstract
Objectives. Non-alcoholic fatty liver disease (NAFLD) is a major cause of chronic liver disease, especially in patients with type 2 diabetes mellitus (T2DM). Significant prevalence of liver fibrosis has been observed in Indian diabetic patients with fatty liver. Early detection of liver fibrosis in persons with diabetes prevents serious problems. This study compares noninvasive liver fibrosis scores and vibration-controlled transient elastography (VCTE) utilising FIBROSCAN™ to assess fibrosis prevalence in patients with T2DM and NAFLD.
Methodology. This cross-sectional, observational study enrolled 351 patients with T2DM and NAFLD from September to October 2023 from eight West Bengal diabetes facilities. Liver stiffness measurement (LSM) via VCTE was used to detect fibrosis. Non-invasive tests (NITs), including fibrosis-4 index (FIB-4), NAFLD fibrosis score (NFS), fibrotic NASH-index (FNI), and AST to platelet ratio index (APRI) were also calculated. To evaluate NIT diagnostic performance, AUROC curve calculations were used.
Results. Among patients with T2DM, 26.5% had fibrosis and 3.13% of individuals had advanced fibrosis (≥F3), whereas 11.97% had substantial fibrosis (≥F2). Fibrotic NASH-index could detect fibrosis best with area under the curve (AUROC) >0.70, whereas FIB-4 and NFS were better (AUROC >0.8) to identify advanced fibrosis, and APRI struggle to diagnose severe fibrosis.
Conclusion. In patients with T2DM with NAFLD, VCTE detects fibrosis. FNI is best tool for detection of fibrosis, whereas FNI and NFS are better for distinguishing advanced fibrosis in such patients. To increase fibrosis identification in this population, multiple diagnostic approaches are needed.
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References
1. Perumpail BJ, Khan MA, Yoo ER, Cholankeril G, Kim D, Ahmed A. Clinical epidemiology and disease burden of nonalcoholic fatty liver disease. World J Gastroenterol. 2017;23(47):8263–76. https://pubmed.ncbi.nlm.nih.gov/29307986 https://pmc.ncbi.nlm.nih.gov/articles/PMC5743497 https://doi.org/10.3748/wjg.v23.i47.8263 DOI: https://doi.org/10.3748/wjg.v23.i47.8263
2. Li J, Zou B, Yeo YH, et al. Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999-2019: A systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2019;4(5):389–98. https://pubmed.ncbi.nlm.nih.gov/30902670 https://doi.org/10.1016/S2468-1253(19)30039-1 DOI: https://doi.org/10.1016/S2468-1253(19)30039-1
3. Shalimar, Elhence A, Bansal B, et al. Prevalence of non-alcoholic fatty liver disease in India: A systematic review and meta-analysis. J Clin Exp Hepatol. 2022;12(3):818–29. https://pubmed.ncbi.nlm.nih.gov/35677499 https://pmc.ncbi.nlm.nih.gov/articles/PMC9168741 https://doi.org/10.1016/j.jceh.2021.11.010 DOI: https://doi.org/10.1016/j.jceh.2021.11.010
4. Shaji N, Singhai A, Sarawagi Rm Pakhare AP, Mishra VN, Joshi R. Assessment of liver fibrosis using non-invasive screening tools in individuals with diabetes mellitus and metabolic syndrome. Cureus. 2022;14(2):e22682. https://pubmed.ncbi.nlm.nih.gov/35386158 https://pmc.ncbi.nlm.nih.gov/articles/PMC8967074 https://doi.org/10.7759/cureus.22682 DOI: https://doi.org/10.7759/cureus.22682
5. Singhai A, Yadav V, Joshi R, Malik R, T SB, Kamle S. Prevalence, metabolic profile, and associated risk factors of non-alcoholic fatty liver disease in an adult population of India. Cureus. 2023;15(1):e33977. https://pubmed.ncbi.nlm.nih.gov/36820120 https://pmc.ncbi.nlm.nih.gov/articles/PMC9938792 https://doi.org/10.7759/cureus.33977 DOI: https://doi.org/10.7759/cureus.33977
6. Anton MC, Shanthi B, Sridevi C. Prevalence of non-alcoholic fatty liver disease in urban adult population in a tertiary care center, Chennai. Indian J Community Med. 2023;48(4):601–4. https://pubmed.ncbi.nlm.nih.gov/37662140 https://pmc.ncbi.nlm.nih.gov/articles/PMC10470578 https://doi.org/10.4103/ijcm.ijcm_437_22 DOI: https://doi.org/10.4103/ijcm.ijcm_437_22
7. Niriella MA, Ediriweera DS, Withanage MY, Darshika S, De Silva ST, Janaka de Silva H. Prevalence and associated factors for non-alcoholic fatty liver disease among adults in the South Asian Region: A meta-analysis. Lancet Reg Health Southeast Asia. 2023;15:100220. https://pubmed.ncbi.nlm.nih.gov/37614359 https://pmc.ncbi.nlm.nih.gov/articles/PMC10442973 https://doi.org/10.1016/j.lansea.2023.100220 DOI: https://doi.org/10.1016/j.lansea.2023.100220
8. Dharmalingam M, Yamasandhi P. Nonalcoholic fatty liver disease and type 2 diabetes mellitus. Indian J Endocrinol Metab. 2018;22(3):421-8. https://pubmed.ncbi.nlm.nih.gov/30090738 https://pmc.ncbi.nlm.nih.gov/articles/PMC6063173 https://doi.org/10.4103/ijem.IJEM_585_17 DOI: https://doi.org/10.4103/ijem.IJEM_585_17
9. Sinha A, Bankura B. Prevalence of nonalcoholic fatty liver disease in type 2 diabetes mellitus patients from the Eastern region of India. Diabet Epidemiol Manag. 2023;12:100161. https://doi.org/10.1016/j.deman.2023.100161 DOI: https://doi.org/10.1016/j.deman.2023.100161
10. Kalra S, Vithalani M, Gulati G, Kulkarni CM, Kadam Y, Pallivathukkal J, et al. Study of prevalence of nonalcoholic fatty liver disease (NAFLD) in type 2 diabetes patients in India (SPRINT). J Assoc Physicians India. 2013;61(7):448–53. https://pubmed.ncbi.nlm.nih.gov/24772746
11. Lomonaco R, Godinez Leiva E, Bril F, et al. Advanced liver fibrosis is common in patients with type 2 diabetes followed in the outpatient setting: The need for systematic screening. Diabetes Care. 2021;44(2):399–406. https://pubmed.ncbi.nlm.nih.gov/33355256 https://pmc.ncbi.nlm.nih.gov/articles/PMC7818321 https://doi.org/10.2337/dc20-1997 DOI: https://doi.org/10.2337/dc20-1997
12. Kawata N, Takahashi H, Iwane S, et al. FIB-4 index-based surveillance for advanced liver fibrosis in diabetes patients. Diabetol Int. 2021;12(1):118–25. https://pubmed.ncbi.nlm.nih.gov/33479587 https://pmc.ncbi.nlm.nih.gov/articles/PMC7790961 https://doi.org/10.1007/s13340-020-00453-7 DOI: https://doi.org/10.1007/s13340-020-00453-7
13. Younossi ZM, Golabi P, de Avila L, et al. The global epidemiology of NAFLD and NASH in patients with type 2 diabetes: A systematic review and meta-analysis. J Hepatol. 2019;71(4):793–801. https://pubmed.ncbi.nlm.nih.gov/31279902 https://doi.org/10.1016/j.jhep.2019.06.021 DOI: https://doi.org/10.1016/j.jhep.2019.06.021
14. Boeriu A, Dobru D, Fofiu C. Non-invasive diagnostic of NAFLD in type 2 diabetes mellitus and risk stratification: Strengths and limitations. Life (Basel). 2023;13(12):2262. https://pubmed.ncbi.nlm.nih.gov/38137863 https://pmc.ncbi.nlm.nih.gov/articles/PMC10744403 https://doi.org/10.3390/life13122262 DOI: https://doi.org/10.3390/life13122262
15. Sasso M, Beaugrand M, de Ledinghen V, et al. Controlled attenuation parameter (CAP): A novel VCTE™ guided ultrasonic attenuation measurement for the evaluation of hepatic steatosis: preliminary study and validation in a cohort of patients with chronic liver disease from various causes. Ultrasound Med BIol. 2010;36(11):1825-35. https://pubmed.ncbi.nlm.nih.gov/20870345 https://doi.org/10.1016/j.ultrasmedbio.2010.07.005 DOI: https://doi.org/10.1016/j.ultrasmedbio.2010.07.005
16. Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. 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):1486-501. https://pubmed.ncbi.nlm.nih.gov/28586172 https://doi.org/10.1002/hep.29302
17. Sporea I, Mare R, Popescu A, et al. Screening for liver fibrosis and steatosis in a large cohort of patients with type 2 diabetes using vibration controlled transient elastography and controlled attenuation parameter in a single-center real-life experience. J Clin Med. 2020;9(4):1032. https://pubmed.ncbi.nlm.nih.gov/32268517 https://pmc.ncbi.nlm.nih.gov/articles/PMC7230646 https://doi.org/10.3390/jcm9041032 DOI: https://doi.org/10.3390/jcm9041032
18. Lombardi R, Airaghi L, Targher G, Serviddio G, Maffi G, Mantovani A. Liver fibrosis by FibroScan(®) independently of established cardiovascular risk parameters associates with macrovascular and microvascular complications in patients with type 2 diabetes. Liver Int 2020;40:347–54. DOI: https://doi.org/10.1111/liv.14274
19. Eddowes PJ, Sasso M, Allison M, et al. Accuracy of FibroScan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156(6):1717–30. https://pubmed.ncbi.nlm.nih.gov/30689971 https://doi.org/10.1053/j.gastro.2019.01.042 DOI: https://doi.org/10.1053/j.gastro.2019.01.042
20. Ozercan AM, Ozkan H. Vibration-controlled transient elastography in NAFLD: Review study. Euroasian J Hepatogastroenterol. 2022;12(Suppl 1):S41–5. https://pubmed.ncbi.nlm.nih.gov/36466098 https://pmc.ncbi.nlm.nih.gov/articles/PMC9681576 https://doi.org/10.5005/jp-journals-10018-1365 DOI: https://doi.org/10.5005/jp-journals-10018-1365
21. Cassinotto C, Boursier J, de Lédinghen V, et al. Liver stiffness in nonalcoholic fatty liver disease: A comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy. Hepatology. 2016;63(6):1817-27. https://pubmed.ncbi.nlm.nih.gov/26659452 https://doi.org/10.1002/hep.28394 DOI: https://doi.org/10.1002/hep.28394
22. Alqahtani SA, Golabi P, Paik JM, et al. Performance of noninvasive liver fibrosis tests in morbidly obese patients with nonalcoholic fatty liver disease. Obes Surg. 2021;31(5):2002–10. https://pubmed.ncbi.nlm.nih.gov/33616848 https://pmc.ncbi.nlm.nih.gov/articles/PMC8041679 https://doi.org/10.1007/s11695-020-04996-1 DOI: https://doi.org/10.1007/s11695-020-04996-1
23. Tavaglione F, Jamialahmadi O, De Vincentis A, et al. Development and validation of a score for fibrotic nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol. 2023;21(6):1523-32.e1. https://pubmed.ncbi.nlm.nih.gov/35421583 https://doi.org/10.1016/j.cgh.2022.03.044 DOI: https://doi.org/10.1016/j.cgh.2022.03.044
24. Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology. 2019;156(5):1264-81.e4. https://pubmed.ncbi.nlm.nih.gov/30660725 https://pmc.ncbi.nlm.nih.gov/articles/PMC7505052 https://doi.org/10.1053/j.gastro.2018.12.036 DOI: https://doi.org/10.1053/j.gastro.2018.12.036
25. Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. 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):1486–501. https://pubmed.ncbi.nlm.nih.gov/28586172 https://doi.org/10.1002/hep.29302 DOI: https://doi.org/10.1002/hep.29302
26. Yoneda M, Yoneda M, Mawatari H, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis. 2008;40(5):371–8. https://pubmed.ncbi.nlm.nih.gov/18083083 https://doi.org/10.1016/j.dld.2007.10.019 DOI: https://doi.org/10.1016/j.dld.2007.10.019
27. Lucidarme D, Foucher J, Le Bail B, et al. Factors of accuracy of transient elastography (fibroscan) for the diagnosis of liver fibrosis in chronic hepatitis C. Hepatology. 2009;49(4):1083–9. https://pubmed.ncbi.nlm.nih.gov/19140221 https://doi.org/10.1002/hep.22748 DOI: https://doi.org/10.1002/hep.22748
28. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: A nonparametric approach. Biometrics. 1988;44(3):837–45. https://pubmed.ncbi.nlm.nih.gov/3203132 DOI: https://doi.org/10.2307/2531595
29. Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology. 1982;143(1):29–36. https://pubmed.ncbi.nlm.nih.gov/7063747 https://doi.org/10.1148/radiology.143.1.7063747 DOI: https://doi.org/10.1148/radiology.143.1.7063747
30. Jaeschke R, Guyatt G, Sackett DL. Users’ guides to the medical literature. III. How to use an article about a diagnostic test. A. Are the results of the study valid? Evidence-Based Medicine Working Group. JAMA. 1994;271(5):389–91. https://pubmed.ncbi.nlm.nih.gov/8283589 https://doi.org/10.1001/jama.271.5.389 DOI: https://doi.org/10.1001/jama.1994.03510290071040
31. Prasad M, Gupta S, Kashyap N, Kapil U. Diagnostic performance of non-invasive liver fibrosis risk scores in biopsy-proven non-alcoholic fatty liver disease patients in India. Indian J Gastroenterol. 2023;42(2):192-8.https://pubmed.ncbi.nlm.nih.gov/37191918 https://doi.org/10.1007/s12664-022-01335-3 DOI: https://doi.org/10.1007/s12664-022-01335-3
32. Gastaldelli A, Cusi K. From NASH to diabetes and from diabetes to NASH: Mechanisms and treatment options. JHEP Rep. 2019;1(4):312–28. https://pubmed.ncbi.nlm.nih.gov/32039382 https://pmc.ncbi.nlm.nih.gov/articles/PMC7001557 https://doi.org/10.1016/j.jhepr.2019.07.002 DOI: https://doi.org/10.1016/j.jhepr.2019.07.002
33. Hossain N, Afendy A, Stepanova M, Nader F, Srishord M, Rafiq N, et al. independent predictors of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2009;7(11):1224–9, 1229.e1-2. https://pubmed.ncbi.nlm.nih.gov/19559819 https://doi.org/10.1016/j.cgh.2009.06.007 DOI: https://doi.org/10.1016/j.cgh.2009.06.007
34. Liao Y, Liu L, Yang J, et al. Analysis of clinical features and identification of risk factors in patients with non-alcoholic fatty liver disease based on FibroTouch. Sci Rep. 2023;13(1):14812. https://pubmed.ncbi.nlm.nih.gov/37684380 https://pmc.ncbi.nlm.nih.gov/articles/PMC10491815 https://doi.org/10.1038/s41598-023-41596-2 DOI: https://doi.org/10.1038/s41598-023-41596-2
35. Schuppan D, Surabattula R, Wang XY. Determinants of fibrosis progression and regression in NASH. J Hepatol. 2018;68(2):238–50. https://pubmed.ncbi.nlm.nih.gov/29154966 https://doi.org/10.1016/j.jhep.2017.11.012 DOI: https://doi.org/10.1016/j.jhep.2017.11.012
36. Hashemi SA, Alavian S-M, Gholami-Fesharaki M. Assessment of transient elastography (FibroScan) for diagnosis of fibrosis in non-alcoholic fatty liver disease: A systematic review and meta-analysis. Caspian J Intern Med. 2016;7(4):242–52. https://pubmed.ncbi.nlm.nih.gov/27999641 https://pmc.ncbi.nlm.nih.gov/articles/PMC5153515
37. Salehi H, Salehi AM, Ghamarchehreh ME, Khanlarzadeh E, Sohrabi MR. Diagnostic accuracy of vibration controlled transient elastography as non-invasive assessment of liver fibrosis in patients with non-alcoholic fatty liver disease. Middle East J Dig Dis. 2023;15(1):26–31. https://pubmed.ncbi.nlm.nih.gov/37547160 https://pmc.ncbi.nlm.nih.gov/articles/PMC10404076 https://doi.org/10.34172/mejdd.2023.316 DOI: https://doi.org/10.34172/mejdd.2023.316
38. Tapper EB, Challies T, Nasser I, Afdhal NH, Lai M. The performance of vibration controlled transient elastography in a US cohort of patients with nonalcoholic fatty liver disease. Am J Gastroenterol. 2016;111(5):677–84. https://pubmed.ncbi.nlm.nih.gov/26977758 https://pmc.ncbi.nlm.nih.gov/articles/PMC4860094 https://doi.org/10.1038/ajg.2016.49 DOI: https://doi.org/10.1038/ajg.2016.49
39. De A, Keisham A, Mishra S, et al. FibroScan-AST (FAST) score for nonalcoholic steatohepatitis - validation in an Indian cohort. J Clin Exp Hepatol. 2022;12(2):440–7. https://pubmed.ncbi.nlm.nih.gov/35535068 https://pmc.ncbi.nlm.nih.gov/articles/PMC9077185 https://doi.org/10.1016/j.jceh.2021.06.008 DOI: https://doi.org/10.1016/j.jceh.2021.06.008
40. Arab JP, Barrera F, Arrese M. The evolving role of liver biopsy in non-alcoholic fatty liver disease. Ann Hepatol. 2018;17(6):899–902. https://doi.org/10.5604/01.3001.0012.7188. DOI: https://doi.org/10.5604/01.3001.0012.7188
41. Mózes FE, Lee JA, Vali Y, Alzoubi O, Staufer K, Trauner M, et al. Performance of non-invasive tests and histology for the prediction of clinical outcomes in patients with non-alcoholic fatty liver disease: An individual participant data meta-analysis. Lancet Gastroenterol Hepatol 2023;8(8):704–13. https://pubmed.ncbi.nlm.nih.gov/37290471 https://doi.org/10.1016/S2468-1253(23)00141-3 DOI: https://doi.org/10.1016/S2468-1253(23)00141-3
42. Ciardullo S, Carbone M, Invernizzi P, Perseghin G. Noninvasive identification of probable fibrotic nonalcoholic steatohepatitis across the spectrum of glucose tolerance in the United States. Diabetes Res Clin Pract. 2023;199:110679. https://pubmed.ncbi.nlm.nih.gov/37094749 https://doi.org/10.1016/j.diabres.2023.110679 DOI: https://doi.org/10.1016/j.diabres.2023.110679
43. Graupera I, Thiele M, Serra-Burriel M, Caballeria L, et al. Low accuracy of FIB-4 and NAFLD fibrosis scores for screening for liver fibrosis in the population. Clin Gastroenterol Hepatol. 2022;20(11):2567-76.e6. https://pubmed.ncbi.nlm.nih.gov/34971806 https://doi.org/10.1016/j.cgh.2021.12.034 DOI: https://doi.org/10.1016/j.cgh.2021.12.034
44. Cox B, Trasolini R, Galts C, Yoshida EM, Marquez V. Comparing the performance of fibrosis-4 and non-alcoholic fatty liver disease fibrosis score with transient elastography scores of people with non-alcoholic fatty liver disease. Can Liver J. 2021;4(3):275–82. https://pubmed.ncbi.nlm.nih.gov/35992256 https://pmc.ncbi.nlm.nih.gov/articles/PMC9202768 https://doi.org/10.3138/canlivj-2021-0004 DOI: https://doi.org/10.3138/canlivj-2021-0004
45. European Association for the Study of the Liver. EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis – 2021 update. J Hepatol. 2021;75(3):659–89. https://pubmed.ncbi.nlm.nih.gov/34166721 https://doi.org/10.1016/j.jhep.2021.05.025 DOI: https://doi.org/10.1016/j.jhep.2021.05.025
46. Duseja A, Singh SP, De A, Madan K, Rao PN, Shukla A, et al. Indian National Association for Study of the liver (INASL) guidance paper on nomenclature, diagnosis and treatment of nonalcoholic fatty liver disease (NAFLD). J Clin Exp Hepatol. 2023;13(2):273–302. https://pubmed.ncbi.nlm.nih.gov/36950481 https://pmc.ncbi.nlm.nih.gov/articles/PMC10025685 https://doi.org/10.1016/j.jceh.2022.11.014 DOI: https://doi.org/10.1016/j.jceh.2022.11.014
47. Rinella ME, Neuschwander-Tetri BA, Siddiqui MS, et al. AASLD Practice Guidance on the clinical assessment and management of nonalcoholic fatty liver disease. Hepatology. 2023;77(5):1797–835. https://pubmed.ncbi.nlm.nih.gov/36727674 Phttps://pmc.ncbi.nlm.nih.gov/articles/PMC10735173 https://doi.org/10.1097/HEP.0000000000000323 DOI: https://doi.org/10.1097/HEP.0000000000000323
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Copyright (c) 2025 Debmalya Sanyal, Dr. Subhankar Chowdhury, Dr. Soumik Goswami, Dr. Arundhati Dasgupta, Dr. Amarta Shankar Chowdhury, Dr. Sunetra Mondal, Dr. Supratik Bhattacharyya, Dr. Soumyabrata Roy Chowdhury, Dr. Mahuya Sikdar
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