Skip to main content
Log in

Mapping of liver fat with triple-echo gradient echo imaging: validation against 3.0-T proton MR spectroscopy

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

The purpose of this study was to validate a magnetic resonance imaging (MRI) technique for mapping liver fat, using 1H magnetic resonance spectroscopy (1H-MRS) as the reference standard. In 91 patients with type 2 diabetes, 3.0-T single-voxel point-resolved 1H-MRS was used to calculate the liver fat fraction (LFF) from the water (4.76 ppm) and methylene (1.33 ppm) peaks, corrected for T1 and T2 decays. LFF (corrected for T1 and T2* decays) was also obtained from the mean signal intensity on a map built from a triple-echo (consecutive in-phase, opposed-phase, and in-phase echo times) breath-hold gradient echo sequence, using basic image calculation functions (arithmetic mean, subtraction, division, multiplication by a numerical factor). Mean LFF was 8.9% (range, 0.9–33.5) by MRI and 8.8% (range, 0–34.1) by 1H-MRS. Pearson’s coefficient was 0.976 (P < 0.0001) and Lin’s coefficient was 0.975 (P < 0.0001). Liver segment had no significant influence. With Bland–Altman analysis, 95.6% (87/91) of data points were within the limits of agreement. Given its excellent agreement with 1H-MRS, our mapping technique can be used for visual and quantitative evaluation of liver fat in everyday practice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, Musso A, De Paolis P, Capussotti L, Salizzoni M, Rizzetto M (2002) Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 123:134–140

    Article  PubMed  Google Scholar 

  2. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40:1387–1395

    Article  PubMed  Google Scholar 

  3. Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, Hobbs HH, Dobbins RL (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 

  4. Bellentani S, Saccoccio G, Masutti F, Croce LS, Brandi G, Sasso F, Cristanini G, Tiribelli C (2000) Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 132:112–117

    PubMed  CAS  Google Scholar 

  5. Targher G, Bertolini L, Rodella S, Tessari R, Zenari L, Lippi G, Arcaro G (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 

  6. Johnson NA, Walton DW, Sachinwalla T, Thompson CH, Smith K, Ruell PA, Stannard SR, George J (2008) Noninvasive assessment of hepatic lipid composition: advancing understanding and management of fatty liver disorders. Hepatology 47:1513–1523

    Article  PubMed  CAS  Google Scholar 

  7. Cowin GJ, Jonsson JR, Bauer JD, Ash S, Ali A, Osland EJ, Purdie DM, Clouston AD, Powell EE, Galloway GJ (2008) Magnetic resonance imaging and spectroscopy for monitoring liver steatosis. J Magn Reson Imaging 28:937–945

    Article  PubMed  Google Scholar 

  8. Guiu B, Petit JM, Loffroy R, Ben Salem D, Aho S, Masson D, Hillon P, Krause D, Cercueil JP (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 

  9. Kim H, Taksali SE, Dufour S, Befroy D, Goodman TR, Petersen KF, Shulman GI, Caprio S, Constable RT (2008) Comparative MR study of hepatic fat quantification using single-voxel proton spectroscopy, two-point dixon and three-point IDEAL. Magn Reson Med 59:521–527

    Article  PubMed  CAS  Google Scholar 

  10. Reeder SB, Hargreaves BA, Yu H, Brittain JH (2005) Homodyne reconstruction and IDEAL water–fat decomposition. Magn Reson Med 54:586–593

    Article  PubMed  Google Scholar 

  11. Browning JD (2006) Statins and hepatic steatosis: perspectives from the Dallas Heart Study. Hepatology 44:466–471

    Article  PubMed  CAS  Google Scholar 

  12. Irwan R, Edens MA, Sijens PE (2008) Assessment of the variations in fat content in normal liver using a fast MR imaging method in comparison with results obtained by spectroscopic imaging. Eur Radiol 18:806–813

    Article  PubMed  Google Scholar 

  13. Korenblat KM, Fabbrini E, Mohammed BS, Klein S (2008) Liver, muscle, and adipose tissue insulin action is directly related to intrahepatic triglyceride content in obese subjects. Gastroenterology 134:1369–1375

    Article  PubMed  CAS  Google Scholar 

  14. Kotronen A, Juurinen L, Hakkarainen A, Westerbacka J, Corner A, Bergholm R, Yki-Jarvinen H (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 

  15. Machann J, Thamer C, Schnoedt B, Stefan N, Haring HU, Claussen CD, Fritsche A, Schick F (2006) Hepatic lipid accumulation in healthy subjects: a comparative study using spectral fat-selective MRI and volume-localized 1H-MR spectroscopy. Magn Reson Med 55:913–917

    Article  PubMed  CAS  Google Scholar 

  16. O'Regan DP, Callaghan MF, Wylezinska-Arridge M, Fitzpatrick J, Naoumova RP, Hajnal JV, Schmitz SA (2008) Liver fat content and T2*: simultaneous measurement by using breath-hold multiecho MR imaging at 3.0 T-feasibility. Radiology 247:550–557

    Article  PubMed  Google Scholar 

  17. 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 

  18. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D (2001) Java-based graphical user interface for the MRUI quantitation package. Magma 12:141–152

    Article  PubMed  CAS  Google Scholar 

  19. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310

    PubMed  CAS  Google Scholar 

  20. Lin LI (1989) A concordance correlation coefficient to evaluate reproducibility. Biometrics 45:255–268

    Article  PubMed  CAS  Google Scholar 

  21. de Bazelaire CM, Duhamel GD, Rofsky NM, Alsop DC (2004) MR imaging relaxation times of abdominal and pelvic tissues measured in vivo at 3.0 T: preliminary results. Radiology 230:652–659

    Article  PubMed  Google Scholar 

  22. Hussain HK, Chenevert TL, Londy FJ, Gulani V, Swanson SD, McKenna BJ, Appelman HD, Adusumilli S, Greenson JK, Conjeevaram HS (2005) Hepatic fat fraction: MR imaging for quantitative measurement and display-early experience. Radiology 237:1048–1055

    Article  PubMed  Google Scholar 

  23. Alustiza JM, Castiella A (2008) Liver fat and iron at in-phase and opposed-phase MR imaging. Radiology 246:641

    Article  PubMed  Google Scholar 

  24. Westphalen AC, Qayyum A, Yeh BM, Merriman RB, Lee JA, Lamba A, Lu Y, Coakley FV (2007) Liver fat: effect of hepatic iron deposition on evaluation with opposed-phase MR imaging. Radiology 242:450–455

    Article  PubMed  Google Scholar 

  25. Guiu B, Loffroy R, Cercueil JP, Krause D (2008) Multiecho MR imaging and proton MR spectroscopy for liver fat quantification. Radiology 249:1081

    Article  PubMed  Google Scholar 

  26. Bydder M, Yokoo T, Hamilton G, Middleton MS, Chavez AD, Schwimmer JB, Lavine JE, Sirlin CB (2008) Relaxation effects in the quantification of fat using gradient echo imaging. Magn Reson Imaging 26:347–359

    Article  PubMed  Google Scholar 

  27. Mehta SR, Thomas EL, Bell JD, Johnston DG, Taylor-Robinson SD (2008) Non-invasive means of measuring hepatic fat content. World J Gastroenterol 14:3476–3483

    Article  PubMed  Google Scholar 

  28. Park SH, Kim PN, Kim KW, Lee SW, Yoon SE, Park SW, Ha HK, Lee MG, Hwang S, Lee SG, Yu ES, Cho EY (2006) Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology 239:105–112

    Article  PubMed  Google Scholar 

  29. Fischbach F, Schirmer T, Thormann M, Freund T, Ricke J, Bruhn H (2008) Quantitative proton magnetic resonance spectroscopy of the normal liver and malignant hepatic lesions at 3.0 Tesla. Eur Radiol 18(11):2549–2558

    Article  PubMed  CAS  Google Scholar 

  30. Thomsen C, Becker U, Winkler K, Christoffersen P, Jensen M, Henriksen O (1994) Quantification of liver fat using magnetic resonance spectroscopy. Magnetic resonance imaging 12:487–495

    Article  PubMed  CAS  Google Scholar 

  31. Kim SH, Lee JM, Han JK, Lee JY, Lee KH, Han CJ, Jo JY, Yi NJ, Suh KS, Shin KS, Jo SY, Choi BI (2006) Hepatic macrosteatosis: predicting appropriateness of liver donation by using MR imaging-correlation with histopathologic findings. Radiology 240:116–129

    Article  PubMed  Google Scholar 

  32. Borra RJ, Salo S, Dean K, Lautamaki R, Nuutila P, Komu M, Parkkola R (2009) Nonalcoholic fatty liver disease: rapid evaluation of liver fat content with in-phase and out-of-phase MR imaging. Radiology 250:130–136

    Article  PubMed  Google Scholar 

  33. Gastaldelli A, Cusi K, Pettiti M, Hardies J, Miyazaki Y, Berria R, Buzzigoli E, Sironi AM, Cersosimo E, Ferrannini E, Defronzo RA (2007) Relationship between hepatic/visceral fat and hepatic insulin resistance in nondiabetic and type 2 diabetic subjects. Gastroenterology 133:496–506

    Article  PubMed  CAS  Google Scholar 

  34. Lautamaki R, Borra R, Iozzo P, Komu M, Lehtimaki T, Salmi M, Jalkanen S, Airaksinen KE, Knuuti J, Parkkola R, Nuutila P (2006) Liver steatosis coexists with myocardial insulin resistance and coronary dysfunction in patients with type 2 diabetes. Am J Physiol Endocrinol Metab 291:E282–E290

    Article  PubMed  CAS  Google Scholar 

  35. Qayyum A, Goh JS, Kakar S, Yeh BM, Merriman RB, Coakley FV (2005) Accuracy of liver fat quantification at MR imaging: comparison of out-of-phase gradient-echo and fat-saturated fast spin-echo techniques-initial experience. Radiology 237:507–511

    Article  PubMed  Google Scholar 

  36. Iannaccone R, Piacentini F, Murakami T, Paradis V, Belghiti J, Hori M, Kim T, Durand F, Wakasa K, Monden M, Nakamura H, Passariello R, Vilgrain V (2007) Hepatocellular carcinoma in patients with nonalcoholic fatty liver disease: helical CT and MR imaging findings with clinical-pathologic comparison. Radiology 243:422–430

    Article  PubMed  Google Scholar 

  37. Stark DD, Wittenberg J, Middleton MS, Ferrucci JT (1986) Liver metastases: detection by phase-contrast MR imaging. Radiology 158:327–332

    PubMed  CAS  Google Scholar 

  38. Safanda J, Fakan F (1981) Histochemical and biochemical observations of the spleen in atypical Niemann–Pick disease and in idiopathic thrombocytopenic purpura. Acta Histochem 68:164–175

    PubMed  CAS  Google Scholar 

  39. Yu JS, Chung JJ, Kim JH, Kim KW (2007) Fat-containing nodules in the cirrhotic liver: chemical shift MRI features and clinical implications. AJR Am J Roentgenol 188:1009–1016

    Article  PubMed  Google Scholar 

  40. Yu JS, Park JG, Jeong EK, Park MS, Kim KW (2007) Hepatic MRI using the double-echo chemical shift phase-selective gradient-echo technique. AJR Am J Roentgenol 188:W49–W56

    Article  PubMed  Google Scholar 

  41. Merriman RB, Ferrell LD, Patti MG, Weston SR, Pabst MS, Aouizerat BE, Bass NM (2006) Correlation of paired liver biopsies in morbidly obese patients with suspected nonalcoholic fatty liver disease. Hepatology 44:874–880

    Article  PubMed  Google Scholar 

  42. Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, Grimaldi A, Capron F, Poynard T (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128:1898–1906

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the publicly funded organization Direction de la Recherche Clinique at the Dijon University Hospital, Dijon, France.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Boris Guiu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guiu, B., Loffroy, R., Petit, JM. et al. Mapping of liver fat with triple-echo gradient echo imaging: validation against 3.0-T proton MR spectroscopy. Eur Radiol 19, 1786–1793 (2009). https://doi.org/10.1007/s00330-009-1330-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-009-1330-9

Keywords

Navigation