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Prediction for steatosis in type-2 diabetes: clinico-biological markers versus 1H-MR spectroscopy

  • Hepatobiliary-Pancreas
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Abstract

Objectives

The SteatoTest, fatty liver index (FLI) and hepatic steatosis index (HSI) are clinico-biological scores of steatosis validated in general or selected populations. Serum adiponectin (s-adiponectin) and retinol binding protein 4 (s-RBP4) are adipokines that could predict liver steatosis. We investigated whether the Steatotest, FLI, HSI, s-adiponectin and s-RBP4 could be valid predictors of liver steatosis in type-2 diabetic (T2D) patients.

Methods

We enrolled 220 consecutive T2D patients. Reference standard was 3.0 T 1H-MR spectroscopy (corrected for T1 and T2 decays). Intraclass correlation coefficients (ICCs), Kappa statistic measures of agreement, receiver operating characteristic (ROC) curves were assessed.

Results

Median liver fat content was 91 mg triglyceride/g liver tissue (range: 0–392). ICCs among the Steatotest, FLI, HSI, s-adiponectin, s-RBP4 and spectroscopy were low: 0.384, 0.281, 0.087, −0.297 and 0.048. Agreement between scores and spectroscopy was poor (Kappa range: 0.042–0.281). The areas under the ROC curves were low: 0.674, 0.647, 0.637, 0.616 and 0.540. S-adiponectin and s-RBP4 levels were strongly related to the presence of diabetic nephropathy (P = 0.0037 and P = 0.004; Mann–Whitney).

Conclusion

The SteatoTest, FLI, HSI, s-adiponectin, s-RBP4 are not valid predictors of steatosis in T2D patients. Clino-biological markers cannot replace 1H-MR spectroscopy for the assessment of liver fat in this population.

Key Points

1 H-MR spectrosopy can reliably estimate the weight fraction of liver steatosis

Type-2 diabetes provides an interesting model for assessing liver steatosis

Clinico-biological markers seem to be invalid predictors for steatosis in type-2 diabetes

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References

  1. Browning JD, Szczepaniak LS, Dobbins R et al (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40:1387–1395

    Article  PubMed  Google Scholar 

  2. Wieckowska A, McCullough AJ, Feldstein AE (2007) Noninvasive diagnosis and monitoring of nonalcoholic steatohepatitis: present and future. Hepatology 46:582–589

    Article  PubMed  CAS  Google Scholar 

  3. Johnson NA, Walton DW, Sachinwalla T et al (2008) Noninvasive assessment of hepatic lipid composition: Advancing understanding and management of fatty liver disorders. Hepatology 47:1513–1523

    Article  PubMed  CAS  Google Scholar 

  4. de Moura AA, Cotrim HP, Barbosa DB et al (2008) Fatty liver disease in severe obese patients: diagnostic value of abdominal ultrasound. World J Gastroenterol 14:1415–1418

    Article  Google Scholar 

  5. Saadeh S, Younossi ZM, Remer EM et al (2002) The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 123:745–750

    Article  PubMed  Google Scholar 

  6. Kotronen A, Peltonen M, Hakkarainen A et al (2009) Prediction of non-alcoholic fatty liver disease and liver fat using metabolic and genetic factors. Gastroenterology 137:865–872

    Article  PubMed  CAS  Google Scholar 

  7. Longo R, Pollesello P, Ricci C et al (1995) Proton MR spectroscopy in quantitative in vivo determination of fat content in human liver steatosis. J Magn Reson Imaging 5:281–285

    Article  PubMed  CAS  Google Scholar 

  8. Szczepaniak LS, Babcock EE, Schick F et al (1999) Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am J Physiol 276:E977–E989

    PubMed  CAS  Google Scholar 

  9. van Werven JR, Marsman HA, Nederveen AJ et al (2010) Assessment of hepatic steatosis in patients undergoing liver resection: comparison of US, CT, T1-weighted dual-echo MR imaging, and point-resolved 1H MR spectroscopy. Radiology 256:159–168

    Article  PubMed  Google Scholar 

  10. Chalasani N (2009) Nonalcoholic fatty liver disease liver fat score and fat equation to predict and quantitate hepatic steatosis: promising but not prime time! Gastroenterology 137:772–775

    Article  PubMed  CAS  Google Scholar 

  11. Poynard T, Ratziu V, Naveau S et al (2005) The diagnostic value of biomarkers (SteatoTest) for the prediction of liver steatosis. Comp Hepatol 4:10

    Article  PubMed  Google Scholar 

  12. Bedogni G, Bellentani S, Miglioli L et al (2006) The Fatty Liver Index: a simple and accurate predictor of hepatic steatosis in the general population. BMC Gastroenterol 6:33

    Article  PubMed  Google Scholar 

  13. Lee JH, Kim D, Kim HJ et al (2010) Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis 42:503–508

    Article  PubMed  CAS  Google Scholar 

  14. Kantartzis K, Rittig K, Balletshofer B et al (2006) The relationships of plasma adiponectin with a favorable lipid profile, decreased inflammation, and less ectopic fat accumulation depend on adiposity. Clin Chem 52:1934–1942

    Article  PubMed  CAS  Google Scholar 

  15. Stefan N, Hennige AM, Staiger H et al (2007) High circulating retinol-binding protein 4 is associated with elevated liver fat but not with total, subcutaneous, visceral, or intramyocellular fat in humans. Diabetes Care 30:1173–1178

    Article  PubMed  CAS  Google Scholar 

  16. Targher G, Bertolini L, Rodella S et al (2007) Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 30:2119–2121

    Article  PubMed  CAS  Google Scholar 

  17. Guiu B, Petit JM, Loffroy R et al (2009) Quantification of liver fat content: comparison of triple-echo chemical shift gradient-echo imaging and in vivo proton MR spectroscopy. Radiology 250:95–102

    Article  PubMed  Google Scholar 

  18. Guiu B, Loffroy R, Petit JM et al (2009) Mapping of liver fat with triple-echo gradient echo imaging: validation against 3.0-T proton MR spectroscopy. Eur Radiol 19:1786–1793

    Article  PubMed  Google Scholar 

  19. Jansen JF, Backes WH, Nicolay K, Kooi ME (2006) 1H MR spectroscopy of the brain: absolute quantification of metabolites. Radiology 240:318–332

    Article  PubMed  Google Scholar 

  20. Naressi A, Couturier C, Devos JM et al (2001) Java-based graphical user interface for the MRUI quantitation package. MAGMA 12:141–152

    Article  PubMed  CAS  Google Scholar 

  21. Szczepaniak LS, Nurenberg P, Leonard D et al (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288:E462–E468

    Article  PubMed  CAS  Google Scholar 

  22. Stevens LA, Coresh J, Greene T, Levey AS (2006) Assessing kidney function–measured and estimated glomerular filtration rate. N Engl J Med 354:2473–2483

    Article  PubMed  CAS  Google Scholar 

  23. Weiner E, Stewart B (1984) Assessing individuals. Oxford University Press, Oxford

    Google Scholar 

  24. Fujita H, Morii T, Koshimura J et al (2006) Possible relationship between adiponectin and renal tubular injury in diabetic nephropathy. Endocrine J 53:745–752

    Article  CAS  Google Scholar 

  25. Koshimura J, Fujita H, Narita T et al (2004) Urinary adiponectin excretion is increased in patients with overt diabetic nephropathy. Biochem Biophys Res Commun 316:165–169

    Article  PubMed  CAS  Google Scholar 

  26. Henze A, Frey SK, Raila J et al (2008) Evidence that kidney function but not type 2 diabetes determines retinol-binding protein 4 serum levels. Diabetes 57:3323–3326

    Article  PubMed  CAS  Google Scholar 

  27. Murata M, Saito T, Otani T et al (2009) An increase in serum retinol-binding protein 4 in the type 2 diabetic subjects with nephropathy. Endocrine J 56:287–294

    Article  CAS  Google Scholar 

  28. Perseghin G, Lattuada G, De Cobelli F et al (2008) Increased mediastinal fat and impaired left ventricular energy metabolism in young men with newly found fatty liver. Hepatology 47:51–58

    Article  PubMed  CAS  Google Scholar 

  29. Ollerton RL, Playle R, Ahmed K, Dunstan FD, Luzio SD, Owens DR (1999) Day-to-day variability of fasting plasma glucose in newly diagnosed type 2 diabetic subjects. Diabetes Care 22:394–398

    Article  PubMed  CAS  Google Scholar 

  30. Widjaja A, Morris RJ, Levy JC, Frayn KN, Manley SE, Turner RC (1999) Within- and between-subject variation in commonly measured anthropometric and biochemical variables. Clin Chem 45:561–566

    PubMed  CAS  Google Scholar 

  31. Bookstein L, Gidding SS, Donovan M, Smith FA (1990) Day-to-day variability of serum cholesterol, triglyceride, and high-density lipoprotein cholesterol levels. Impact on the assessment of risk according to the National Cholesterol Education Program guidelines. Arch Intern Med 150:1653–1657

    Article  PubMed  CAS  Google Scholar 

  32. Westerbacka J, Corner A, Tiikkainen M et al (2004) Women and men have similar amounts of liver and intra-abdominal fat, despite more subcutaneous fat in women: implications for sex differences in markers of cardiovascular risk. Diabetologia 47:1360–1369

    Article  PubMed  CAS  Google Scholar 

  33. Kotronen A, Juurinen L, Hakkarainen A et al (2008) Liver fat is increased in type 2 diabetic patients and underestimated by serum alanine aminotransferase compared with equally obese nondiabetic subjects. Diabetes Care 31:165–169

    Article  PubMed  CAS  Google Scholar 

  34. Ratziu V, Imbert-Bismut F, Messous D, Poynard T (2004) The elusiveness of “normal” ALT in fatty liver. Hepatology 39:1172, author reply 1173

    Article  PubMed  Google Scholar 

  35. Ritchie RF, Palomaki GE, Neveux LM, Navolotskaia O, Ledue TB, Craig WY (2004) Reference distributions for alpha2-macroglobulin: a practical, simple and clinically relevant approach in a large cohort. J Clin Lab Anal 18:139–147

    Article  PubMed  CAS  Google Scholar 

  36. Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F (2009) Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 51:433–445

    Article  PubMed  Google Scholar 

  37. Bugianesi E, Pagotto U, Manini R et al (2005) Plasma adiponectin in nonalcoholic fatty liver is related to hepatic insulin resistance and hepatic fat content, not to liver disease severity. J Clin Endocrinol Metab 90:3498–3504

    Article  PubMed  CAS  Google Scholar 

  38. Matikainen N, Manttari S, Westerbacka J et al (2007) Postprandial lipemia associates with liver fat content. J Clin Endocrinol Metab 92:3052–3059

    Article  PubMed  CAS  Google Scholar 

  39. Bajaj M, Suraamornkul S, Piper P et al (2004) Decreased plasma adiponectin concentrations are closely related to hepatic fat content and hepatic insulin resistance in pioglitazone-treated type 2 diabetic patients. J Clin Endocrinol Metab 89:200–206

    Article  PubMed  CAS  Google Scholar 

  40. Marra F, Bertolani C (2009) Adipokines in liver diseases. Hepatology 50:957–969

    Article  PubMed  CAS  Google Scholar 

  41. Wu H, Jia W, Bao Y et al (2008) Serum retinol binding protein 4 and nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 79:185–190

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Pôle de Recherche (CHU Dijon, France) and by the ALFEDIAM. We thank Philip Bastable and Sandrine Guiu for revising the English. We thank Prof. Claire Bonithon-Kopp (INSERM U866) and Romain Despalins for assistance with this study.

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Correspondence to Boris Guiu.

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Guiu, B., Crevisy-Girod, E., Binquet, C. et al. Prediction for steatosis in type-2 diabetes: clinico-biological markers versus 1H-MR spectroscopy. Eur Radiol 22, 855–863 (2012). https://doi.org/10.1007/s00330-011-2326-9

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  • DOI: https://doi.org/10.1007/s00330-011-2326-9

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