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Exp Clin Endocrinol Diabetes 2022; 130(08): 532-538
DOI: 10.1055/a-1666-0431
Article

Shear Wave Elastography Reveals a High Prevalence of NAFLD-related Fibrosis even in Type 1 Diabetes

Gesine Meyer‡
1   Department of Internal Medicine, Goethe-University Hospital, Frankfurt, Germany
,
Nina Dauth‡
1   Department of Internal Medicine, Goethe-University Hospital, Frankfurt, Germany
,
Matthias Grimm
1   Department of Internal Medicine, Goethe-University Hospital, Frankfurt, Germany
,
Eva Herrmann
2   Institute of Biostatistics and Mathematic Modelling, Goethe-University, Frankfurt, Germany
,
Joerg Bojunga
1   Department of Internal Medicine, Goethe-University Hospital, Frankfurt, Germany
,
Mireen Friedrich-Rust
1   Department of Internal Medicine, Goethe-University Hospital, Frankfurt, Germany
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Abstract

Background The association between type 2 diabetes mellitus (T2DM) and advanced stages of non-alcoholic fatty liver disease is well known. Some studies indicate a relevant prevalence also in type 1 diabetes mellitus (T1DM), but so far there is only limited data.

Objective To determine the prevalence of non-alcoholic fatty liver disease (NAFLD)-related liver fibrosis in individuals with T1DM and compare to those with type 2 diabetes.

Methods Diabetic patients from a single diabetes care centre were screened for liver fibrosis by sonographic shear wave elastography (SWE). In addition, all patients received laboratory evaluation including non-alcoholic fatty liver fibrosis score and Fibrosis-4 Index.

Results Three hundred and forty patients were included in the study, of these, 310 received SWE. Overall 254 patients (93 with type 1 and 161 with type 2 diabetes) had reliable measurements and were included in the final analysis. In patients with type 1 diabetes, the prevalence of NAFLD-related liver fibrosis was 16–21%, depending on the method of detection. Significant liver fibrosis was observed in 30–46% of patients with type 2 diabetes.

Conclusions Our data revealed an unexpectedly high prevalence of NAFLD-related liver fibrosis in patients with type 1 diabetes. To our knowledge, this is one of the first studies using SWE to diagnose advanced NAFLD in type 1 diabetes in a non-preselected cohort. Considering the findings of our study, regular screening for hepatic complications must be recommended for all diabetic patients, even for those with type 1 diabetes.

Key words

Diabetes mellitus, type 1 - diabetes mellitus, type 2 - elasticity imaging techniques - non-alcoholic fatty liver disease


Publication History

Received: 22 July 2021
Received: 14 September 2021

Accepted: 06 October 2021

Article published online:
16 November 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Szczepaniak LS, Nurenberg P, Leonard D. et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: Prevalence of hepatic steatosis in the general population. Am J Physiol - Endocrinol Metab 2005; 288: E462-E468
    CrossrefPubMedSearch in Google Scholar
  • 2 Williams CD, Stengel J, Asike MI. et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: A prospective study. Gastroenterology 2011; 140: 124-131
    CrossrefPubMedSearch in Google Scholar
  • 3 Lee JY, Kim KM, Lee SG. et al. Prevalence and risk factors of non-alcoholic fatty liver disease in potential living liver donors in Korea: A review of 589 consecutive liver biopsies in a single center. J Hepatol 2007; 47: 239-244
    CrossrefPubMedSearch in Google Scholar
  • 4 Ekstedt M, Nasr P, Kechagias S. Natural history of NAFLD/NASH. Curr Hepatol Reports 2017; 16: 391-397
    CrossrefPubMedSearch in Google Scholar
  • 5 Rinella ME. Nonalcoholic fatty liver disease A systematic review. JAMA 2015; 313: 2263-2273
    CrossrefPubMedSearch in Google Scholar
  • 6 Meex RCR, Watt MJ. Hepatokines: Linking nonalcoholic fatty liver disease and insulin resistance. Nature Rev Endocrinol 2017; 13: 509-520
    CrossrefPubMedSearch in Google Scholar
  • 7 Lonardo A, Lugari S, Ballestri S. etal. A round trip from nonalcoholic fatty liver disease to diabetes: molecular targets to the rescue?. Acta Diabetol 2019; 56: 385-396
    CrossrefPubMedSearch in Google Scholar
  • 8 Stefan N, Häring HUH, Cusi K. Non-alcoholic fatty liver disease: Causes, diagnosis, cardiometabolic consequences, and treatment strategies. Lancet Diabetes Endocrinol 2019; 7: 313-324
    CrossrefPubMedSearch in Google Scholar
  • 9 Lonardo A, Nascimbeni F, Mantovani A. et al. Hypertension, diabetes, atherosclerosis and NASH: Cause or consequence?. J Hepatol 2018; 335-352
    CrossrefPubMedSearch in Google Scholar
  • 10 Adams LA, Lymp JF, Sauver J. et al. The natural history of nonalcoholic fatty liver disease: A population-based cohort study. Gastroenterology 2005; 129: 113-121
    CrossrefPubMedSearch in Google Scholar
  • 11 Porepa L, Ray JG, Sanchez-Romeu P. et al. Newly diagnosed diabetes mellitus as a risk factor for serious liver disease. CMAJ 2010; 182: E526-E531
    CrossrefPubMedSearch in Google Scholar
  • 12 Tada T, Toyoda H, Sone Y. et al. Type 2 diabetes mellitus: A risk factor for progression of liver fibrosis in middle-aged patients with non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2019; 34: 2011-2018
    CrossrefPubMedSearch in Google Scholar
  • 13 Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156: 1264-1281
    CrossrefPubMedSearch in Google Scholar
  • 14 Baršić N, Lerotić I, Smirčić-Duvnjak L. et al. Overview and developments in noninvasive diagnosis of nonalcoholic fatty liver disease. World J Gastroenterol 2012; 18: 3945-3954
    CrossrefPubMedSearch in Google Scholar
  • 15 Pandyarajan V, Gish RG, Alkhouri N. et al. Screening for nonalcoholic fatty liver disease in the primary care clinic. Gastroenterol Hepatol 2019; 15: 357-365
    PubMedSearch in Google Scholar
  • 16 Angulo P, Hui JM, Marchesini G. et al. The NAFLD fibrosis score: A noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology 2007; 45: 846-854
    CrossrefPubMedSearch in Google Scholar
  • 17 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: 1817-1827
    CrossrefPubMedSearch in Google Scholar
  • 18 Liu H, Fu J, Hong R. et al. Acoustic radiation force impulse elastography for the non-invasive evaluation of hepatic fibrosis in non-alcoholic fatty liver disease patients: A systematic review & meta-analysis. PLoS One 2015; 10: e0127782
    CrossrefPubMedSearch in Google Scholar
  • 19 Casey SP, Kemp WW, Mclean CA. et al. A prospective evaluation of the role of transient elastography for the detection of hepatic fibrosis in type 2 diabetes without overt liver disease. Scand J Gastroenterol 2012; 47: 836-841
    CrossrefPubMedSearch in Google Scholar
  • 20 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: 793-801
    CrossrefPubMedSearch in Google Scholar
  • 21 Lombardi R, Airaghi L, Targher G. et al. 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: 347-354
    CrossrefPubMedSearch in Google Scholar
  • 22 Mantovani A, Turino T, Lando MG. et al. Screening for non-alcoholic fatty liver disease using liver stiffness measurement and its association with chronic kidney disease and cardiovascular complications in patients with type 2 diabetes. Diabetes Metab 2020; 46: 296-303
    CrossrefPubMedSearch in Google Scholar
  • 23 Mansour A, Mohajeri-Tehrani MR, Samadi M. et al. Risk factors for non-alcoholic fatty liver disease-associated hepatic fibrosis in type 2 diabetes patients. Acta Diabetol 2019; 56: 1199-1207
    CrossrefPubMedSearch in Google Scholar
  • 24 Cusi K, Sanyal AJ, Zhang S. et al. Non-alcoholic fatty liver disease (NAFLD) prevalence and its metabolic associations in patients with type 1 diabetes and type 2 diabetes. Diabetes, Obes Metab 2017; 19: 1630-1634
    CrossrefPubMedSearch in Google Scholar
  • 25 Serra-Planas E, Aguilera E, Castro L. et al. Low prevalence of non-alcoholic fatty liver disease in patients with type 1 diabetes is associated with decreased subclinical cardiovascular disease. J Diabetes 2017; 9: 1065-1072
    CrossrefPubMedSearch in Google Scholar
  • 26 Singh A, Le P, Lopez R. et al. The utility of noninvasive scores in assessing the prevalence of nonalcoholic fatty liver disease and advanced fibrosis in type 1 diabetic patients. Hepatol Int 2018; 12: 37-43
    CrossrefPubMedSearch in Google Scholar
  • 27 Sviklāne L, Olmane E, Dzērve Z. et al. Fatty liver index and hepatic steatosis index for prediction of non-alcoholic fatty liver disease in type 1 diabetes. J Gastroenterol Hepatol 2018; 33: 270-276
    CrossrefPubMedSearch in Google Scholar
  • 28 Marjot T, Sbardella E, Moolla A. et al. Prevalence and severity of non-alcoholic fatty liver disease are underestimated in clinical practice: impact of a dedicated screening approach at a large university teaching hospital. Diabet Med 2018; 35: 89-98
    CrossrefPubMedSearch in Google Scholar
  • 29 de Lédinghen V, Vergniol J, Gonzalez C. et al. Screening for liver fibrosis by using FibroScan® and FibroTest in patients with diabetes. Dig Liver Dis 2012; 44: 413-418
    CrossrefPubMedSearch in Google Scholar
  • 30 Elkabbany ZA, Elbarbary NS, Ismail EA. et al. Transient elastography as a noninvasive assessment tool for hepatopathies of different etiology in pediatric type 1 diabetes mellitus. J Diabetes Complications 2017; 31: 186-194
    CrossrefPubMedSearch in Google Scholar
  • 31 Williamson RM, Price JF, Glancy S. et al. Prevalence of and risk factors for hepatic steatosis and nonalcoholic fatty liver disease in people with type 2 diabetes: The Edinburgh type 2 diabetes study. Diabetes Care 2011; 34: 1139-1344
    CrossrefPubMedSearch in Google Scholar
  • 32 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
    CrossrefPubMedSearch in Google Scholar
  • 33 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: 1486-1501
    CrossrefPubMedSearch in Google Scholar
  • 34 Sun W, Cui H, Li N. et al. Comparison of FIB-4 index, NAFLD fibrosis score and BARD score for prediction of advanced fibrosis in adult patients with non-alcoholic fatty liver disease: A meta-analysis study. Hepatol Res 2016; 46: 862-870
    CrossrefPubMedSearch in Google Scholar
  • 35 Sarvazyan AP, Rudenko OV, Swanson SD. et al. Shear wave elasticity imaging: A new ultrasonic technology of medical diagnostics. Ultrasound Med Biol 1998; 24: 1419-1435
    CrossrefPubMedSearch in Google Scholar
  • 36 Friedrich-Rust M, Nierhoff J, Lupsor M. et al. Performance of Acoustic Radiation Force Impulse imaging for the staging of liver fibrosis: A pooled meta-analysis. J Viral Hepat 2012; 19: 212-219
    CrossrefPubMedSearch in Google Scholar