Skip to main content
Log in

Accumulated Hepatic Steatosis Grades Predicted by T2*-IDEAL Fat Fraction

  • Original Article
  • Published:
Journal of Medical and Biological Engineering Aims and scope Submit manuscript

Abstract

Purpose

1H Magnetic resonance spectroscopy (MRS) is currently considered to be the standard for MR-based fat quantification without the need of histopathologic correlation. The purpose of this prospective study was to examine whether T2*-iterative decomposition of water and fat with echo asymmetry and least squares estimation (T2*-IDEAL) technique accurately predicts different hepatic steatosis grades.

Methods

Hepatic fat fraction was quantified by 1H MRS and T2*-IDEAL methods. Geometric homogeneity, intraobserver reliability, and interobserver agreement were examined for T2*-IDEAL method. The relationship between fat fraction measured by T2*I-DEAL (FFIDEAL) and that measured by 1H MRS (FFMRS) was examined by linear regression analysis. Based on 1H MRS, accumulated hepatic steatosis grade including HSF5, HSF15, HSF30, and HSF60, representing hepatic steatosis with fat fraction no less than 5%, 15%, 30%, and 60%, respectively, were calculated. Body mass index and FFIDEAL were used to predict the accumulated hepatic steatosis grade, respectively.

Results

FFMRS and FFIDEAL were 16.36% ± 12.96 and 15.57% ± 11.13, respectively. Linear regression analysis showed that the FFIDEAL was significantly and positively associated with FFMRS (y = 0.8226x + 2.1068, R2 = 0.9181, p < 0.001). The percentage error of FFIDEAL was − 5.2% ± 22.2% for HSF5. FFIDEAL and BMI predicted hepatic steatosis grade HSF5, HSF15, and HSF30 with an AUC of 0.988, 0.967, and 0.996 (all p = 0.0001) for FFIDEAL and 0.742, 0.836, and 0.883 (all p < 0.01) for BMI, respectively.

Conclusion

T2*-IDEAL method accurately predicts the accumulated hepatic steatosis grades with high intraobserver reliability, interobserver agreement, and geometric homogeneity.

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

Similar content being viewed by others

References

  1. Szczepaniak, L. S., Nurenberg, P., Leonard, D., Browning, J. D., Reingold, J. S., Grundy, S., Hobbs, H. H., & Dobbins, R. L. (2005). Magnetic resonance spectroscopy to measure hepatic triglyceride content: Prevalence of hepatic steatosis in the general population. American journal of physiology Endocrinology and metabolism, 288(2), E462–E468. https://doi.org/10.1152/ajpendo.00064.2004.

    Article  CAS  PubMed  Google Scholar 

  2. Cairns, S. R., & Peters, T. J. (1983). Biochemical analysis of hepatic lipid in alcoholic and diabetic and control subjects. Clinical science (London England: 1979), 65(6), 645–652. https://doi.org/10.1042/cs0650645.

    Article  CAS  PubMed  Google Scholar 

  3. Idilman, I. S., Aniktar, H., Idilman, R., Kabacam, G., Savas, B., Elhan, A., Celik, A., Bahar, K., & Karcaaltincaba, M. (2013). Hepatic steatosis: Quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology, 267(3), 767–775. https://doi.org/10.1148/radiol.13121360.

    Article  PubMed  Google Scholar 

  4. Chalasani, N., Younossi, Z., Lavine, J. E., Diehl, A. M., Brunt, E. M., Cusi, K., Charlton, M., & Sanyal, A. J. (2012). The diagnosis and management of non-alcoholic fatty liver disease: Practice Guideline by the American Association for the study of Liver Diseases, American College of Gastroenterology, and the american Gastroenterological Association. Hepatology (Baltimore Md), 55(6), 2005–2023. https://doi.org/10.1002/hep.25762.

    Article  PubMed  Google Scholar 

  5. MMustapic, S., Ziga, S., Matic, V., Bokun, T., Radic, B., Lucijanic, M., Marusic, S., Babic, Z., Grgurevic, I. S., Ziga, S., Matic, V., Bokun, T., Radic, B., Lucijanic, M., Marusic, S., Babic, Z., & Grgurevic, I. (2018). Ultrasound grade of liver steatosis is independently associated with the risk of metabolic syndrome. Canadian Journal of Gastroenterology & Hepatology, 2018, 8490242. https://doi.org/10.1155/2018/8490242

    Article  Google Scholar 

  6. Paige, J. S., Bernstein, G. S., Heba, E., Costa, E. A. C., Fereirra, M., Wolfson, T., Gamst, A. C., Valasek, M. A., Lin, G. Y., Han, A., Erdman, J. W., Jr., O’Brien, W. D., Jr., Andre, M. P., Loomba, R., & Sirlin, C. B. (2017). A pilot comparative study of quantitative Ultrasound, Conventional Ultrasound, and MRI for Predicting Histology-Determined steatosis Grade in adult nonalcoholic fatty liver disease. AJR American journal of roentgenology, 208(5), W168–W177. https://doi.org/10.2214/AJR.16.16726

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hernaez, R., Lazo, M., Bonekamp, S., Kamel, I., Brancati, F. L., Guallar, E., & Clark, J. M. (2011). Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: A meta-analysis. Hepatology (Baltimore Md), 54(3), 1082–1090. https://doi.org/10.1002/hep.24452.

    Article  PubMed  Google Scholar 

  8. Alpern, M. B., Lawson, T. L., Foley, W. D., Perlman, S. J., Reif, L. J., Arevalos, E., & Rimm, A. A. (1986). Focal hepatic masses and fatty infiltration detected by enhanced dynamic CT. Radiology, 158(1), 45–49. https://doi.org/10.1148/radiology.158.1.3940396.

    Article  CAS  PubMed  Google Scholar 

  9. Hamer, O. W., Aguirre, D. A., Casola, G., Lavine, J. E., Woenckhaus, M., & Sirlin, C. B. (2006). Fatty liver: Imaging patterns and pitfalls. Radiographics: a review publication of the Radiological Society of North America Inc, 26(6), 1637–1653. https://doi.org/10.1148/rg.266065004.

    Article  PubMed  Google Scholar 

  10. Boyce, C. J., Pickhardt, P. J., Kim, D. H., Taylor, A. J., Winter, T. C., Bruce, R. J., Lindstrom, M. J., & Hinshaw, J. L. (2010). Hepatic steatosis (fatty liver disease) in asymptomatic adults identified by unenhanced low-dose CT. AJR American journal of roentgenology, 194(3), 623–628. https://doi.org/10.2214/AJR.09.2590.

    Article  PubMed  Google Scholar 

  11. Dixon, W. T. (1984). Simple proton spectroscopic imaging. Radiology, 153(1), 189–194. https://doi.org/10.1148/radiology.153.1.6089263.

    Article  CAS  PubMed  Google Scholar 

  12. Fowler, K. J., Saad, N. E., & Linehan, D. (2015). Imaging approach to hepatocellular carcinoma, cholangiocarcinoma, and metastatic colorectal cancer. Surgical oncology clinics of North America, 24(1), 19–40. https://doi.org/10.1016/j.soc.2014.09.002.

    Article  PubMed  Google Scholar 

  13. Goceri, E., Shah, Z. K., Layman, R., Jiang, X., & Gurcan, M. N. (2016). Quantification of liver fat: A comprehensive review. Computers in biology and medicine, 71, 174–189. https://doi.org/10.1016/j.compbiomed.2016.02.013.

    Article  PubMed  Google Scholar 

  14. Bohte, A. E., van Werven, J. R., Bipat, S., & Stoker, J. (2011). The diagnostic accuracy of US, CT, MRI and 1H-MRS for the evaluation of hepatic steatosis compared with liver biopsy: A meta-analysis. European radiology, 21(1), 87–97. https://doi.org/10.1007/s00330-010-1905-5.

    Article  PubMed  Google Scholar 

  15. Reeder, S. B., Pineda, A. R., Wen, Z., Shimakawa, A., Yu, H., Brittain, J. H., Gold, G. E., Beaulieu, C. H., & Pelc, N. J. (2005). Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL): Application with fast spin-echo imaging. Magnetic resonance in medicine, 54(3), 636–644. https://doi.org/10.1002/mrm.20624.

    Article  PubMed  Google Scholar 

  16. Liu, C. Y., McKenzie, C. A., Yu, H., Brittain, J. H., & Reeder, S. B. (2007). Fat quantification with IDEAL gradient echo imaging: Correction of bias from T(1) and noise. Magnetic resonance in medicine, 58(2), 354–364. https://doi.org/10.1002/mrm.21301.

    Article  PubMed  Google Scholar 

  17. Yu, H., McKenzie, C. A., Shimakawa, A., Vu, A. T., Brau, A. C., Beatty, P. J., Pineda, A. R., Brittain, J. H., & Reeder, S. B. (2007). Multiecho reconstruction for simultaneous water-fat decomposition and T2* estimation. Journal of magnetic resonance imaging: JMRI, 26(4), 1153–1161. https://doi.org/10.1002/jmri.21090.

    Article  PubMed  Google Scholar 

  18. Yokoo, T., Serai, S. D., Pirasteh, A., Bashir, M. R., Hamilton, G., Hernando, D., Hu, H. H., Hetterich, H., Kühn, J. P., Kukuk, G. M., Loomba, R., Middleton, M. S., Obuchowski, N. A., Song, J. S., Tang, A., Wu, X., Reeder, S. B., & Sirlin, C. B. (2018). Linearity, Bias, and Precision of hepatic Proton Density Fat Fraction measurements by using MR Imaging: A Meta-analysis. Radiology, 286(2), 486–498. https://doi.org/10.1148/radiol.2017170550. & RSNA-QIBA PDFF Biomarker Committee

    Article  PubMed  Google Scholar 

  19. Haufe, W. M., Wolfson, T., Hooker, C. A., Hooker, J. C., Covarrubias, Y., Schlein, A. N., Hamilton, G., Middleton, M. S., Angeles, J. E., Hernando, D., Reeder, S. B., Schwimmer, J. B., & Sirlin, C. B. (2017). Accuracy of PDFF estimation by magnitude-based and complex-based MRI in children with MR spectroscopy as a reference. Journal of magnetic resonance imaging: JMRI, 46(6), 1641–1647. https://doi.org/10.1002/jmri.25699.

    Article  PubMed  Google Scholar 

  20. Kim, H. J., Cho, H. J., Kim, B., You, M. W., Lee, J. H., Huh, J., & Kim, J. K. (2019). Accuracy and precision of proton density fat fraction measurement across field strengths and scan intervals: A phantom and human study. Journal of magnetic resonance imaging: JMRI, 50(1), 305–314. https://doi.org/10.1002/jmri.26575.

    Article  PubMed  Google Scholar 

  21. Weiss, K. L., Richards, C. R., Sun, D., & Weiss, J. L. (2009). Subminute fat-water-separated dual-echo automated spine survey iterative scan technique. AJNR American journal of neuroradiology, 30(10), 1840–1846. https://doi.org/10.3174/ajnr.A1619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Takasu, M., Tani, C., Sakoda, Y., Ishikawa, M., Tanitame, K., Date, S., Akiyama, Y., Sakai, A., Asaoku, H., Kajima, T., & Awai, K. (2012). Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL) imaging of multiple myeloma: Initial clinical efficiency results. European radiology, 22(5), 1114–1121. https://doi.org/10.1007/s00330-011-2351-8.

    Article  PubMed  Google Scholar 

  23. Chang, H. C., Juan, C. J., Chiu, H. C., Cheng, C. C., Chiu, S. C., Liu, Y. J., Chung, H. W., & Hsu, H. H. (2014). Effects of gender, age, and body mass index on fat contents and apparent diffusion coefficients in healthy parotid glands: An MRI evaluation. European radiology, 24(9), 2069–2076. https://doi.org/10.1007/s00330-014-3265-z.

    Article  PubMed  Google Scholar 

  24. Chang, H. C., Juan, C. J., Chiu, H. C., Liu, Y. J., Cheng, C. C., Chiu, S. C., Chen, C. Y., Huang, G. S., & Chung, H. W. (2013). Parotid fat contents in healthy subjects evaluated with iterative decomposition with echo asymmetry and least squares fat-water separation. Radiology, 267(3), 918–923. https://doi.org/10.1148/radiol.12112599.

    Article  PubMed  Google Scholar 

  25. Su, G. Y., Wang, C. B., Hu, H., Liu, J., Ding, H. Y., Xu, X. Q., & Wu, F. Y. (2019). Effect of laterality, gender, age and body mass index on the fat fraction of salivary glands in healthy volunteers: Assessed using iterative decomposition of water and fat with echo asymmetry and least-squares estimation method. Dento maxillo facial radiology, 48(3), 20180263. https://doi.org/10.1259/dmfr.20180263.

    Article  PubMed  Google Scholar 

  26. Campo, C. A., Hernando, D., Schubert, T., Bookwalter, C. A., Pay, A. J. V., & Reeder, S. B. (2017). Standardized Approach for ROI-Based measurements of Proton Density Fat Fraction and R2* in the liver. AJR American journal of roentgenology, 209(3), 592–603. https://doi.org/10.2214/AJR.17.17812.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Selzner, M., & Clavien, P. A. (2001). Fatty liver in liver transplantation and surgery. Seminars in liver disease, 21(1), 105–113. https://doi.org/10.1055/s-2001-12933.

    Article  CAS  PubMed  Google Scholar 

  28. Lee, S. G. (2015). A complete treatment of adult living donor liver transplantation: A review of surgical technique and current challenges to expand indication of patients. American journal of transplantation: official journal of the American Society of Transplantation and the American Society of Transplant Surgeons, 15(1), 17–38. https://doi.org/10.1111/ajt.12907.

    Article  PubMed  Google Scholar 

  29. Brunt, E. M., Janney, C. G., Di Bisceglie, A. M., Neuschwander-Tetri, B. A., & Bacon, B. R. (1999). Nonalcoholic steatohepatitis: A proposal for grading and staging the histological lesions. The American journal of gastroenterology, 94(9), 2467–2474. https://doi.org/10.1111/j.1572-0241.1999.01377.x.

    Article  CAS  PubMed  Google Scholar 

  30. Tang, A., Tan, J., Sun, M., Hamilton, G., Bydder, M., Wolfson, T., Gamst, A. C., Middleton, M., Brunt, E. M., Loomba, R., Lavine, J. E., Schwimmer, J. B., & Sirlin, C. B. (2013). Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology, 267(2), 422–431. https://doi.org/10.1148/radiol.12120896.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Linares, I., Hamar, M., Selzner, N., & Selzner, M. (2019). Steatosis in liver transplantation: Current Limitations and future strategies. Transplantation, 103(1), 78–90. https://doi.org/10.1097/TP.0000000000002466.

    Article  PubMed  Google Scholar 

  32. Sanyal, A. J., Chalasani, N., Kowdley, K. V., McCullough, A., Diehl, A. M., Bass, N. M., Neuschwander-Tetri, B. A., Lavine, J. E., Tonascia, J., Unalp, A., Van Natta, M., Clark, J., Brunt, E. M., Kleiner, D. E., Hoofnagle, J. H., Robuck, P. R., NASH CRN. (2010). Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. The New England Journal of Medicine, 362(18), 1675–1685. https://doi.org/10.1056/NEJMoa0907929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wildman-Tobriner, B., Middleton, M. M., Moylan, C. A., Rossi, S., Flores, O., Chang, Z. A., Abdelmalek, M. F., Sirlin, C. B., & Bashir, M. R. (2018). Association between magnetic resonance Imaging-Proton Density Fat Fraction and Liver Histology features in patients with nonalcoholic fatty liver disease or nonalcoholic steatohepatitis. Gastroenterology, 155(5), 1428–1435e2. https://doi.org/10.1053/j.gastro.2018.07.018.

    Article  PubMed  Google Scholar 

  34. Décarie, P. O., Lepanto, L., Billiard, J. S., Olivié, D., Murphy-Lavallée, J., Kauffmann, C., & Tang, A. (2011). Fatty liver deposition and sparing: A pictorial review. Insights into imaging, 2(5), 533–538. https://doi.org/10.1007/s13244-011-0112-5.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Ratziu, V., Charlotte, F., Heurtier, A., Gombert, S., Giral, P., Bruckert, E., Grimaldi, A., Capron, F., Poynard, T., & LIDO Study Group. (2005). Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology, 128(7), 1898–1906. https://doi.org/10.1053/j.gastro.2005.03.084.

    Article  PubMed  Google Scholar 

  36. Qayyum, A., Goh, J. S., Kakar, S., Yeh, B. M., Merriman, R. B., & Coakley, F. V. (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(2), 507–511. https://doi.org/10.1148/radiol.2372040539.

    Article  PubMed  Google Scholar 

  37. Hsu, H. W., Tsang, L. L., Yap, A., Huang, T. L., Chen, T. Y., Lin, T. S., Concejero, A. M., Ou, S. Y., Yu, C. Y., Chen, C. L., & Cheng, Y. F. (2011). Magnetic resonance cholangiography in living donor liver transplantation. Transplantation, 92(1), 94–99. https://doi.org/10.1097/TP.0b013e31821c1e33.

    Article  PubMed  Google Scholar 

  38. Hu, H. H., Kim, H. W., Nayak, K. S., & Goran, M. I. (2010). Comparison of fat-water MRI and single-voxel MRS in the assessment of hepatic and pancreatic fat fractions in humans. Obesity (Silver Spring Md), 18(4), 841–847. https://doi.org/10.1038/oby.2009.352.

    Article  PubMed  Google Scholar 

  39. Chen, C. L., Fan, S. T., Lee, S. G., Makuuchi, M., & Tanaka, K. (2003). Living-donor liver transplantation: 12 years of experience in Asia. Transplantation, 75(3 Suppl), S6–S11. https://doi.org/10.1097/01.TP.0000046533.93621.C7

    Article  PubMed  Google Scholar 

  40. McCormack, L., Dutkowski, P., El-Badry, A. M., & Clavien, P. A. (2011). Liver transplantation using fatty livers: Always feasible? Journal of hepatology, 54(5), 1055–1062. https://doi.org/10.1016/j.jhep.2010.11.004.

    Article  PubMed  Google Scholar 

  41. Luca, L., Westbrook, R., & Tsochatzis, E. A. (2015). Metabolic and cardiovascular complications in the liver transplant recipient. Annals of gastroenterology, 28(2), 183–192.

    PubMed  PubMed Central  Google Scholar 

  42. de Baere, T., Roche, A., Elias, D., Lasser, P., Lagrange, C., & Bousson, V. (1996). Preoperative portal vein embolization for extension of hepatectomy indications. Hepatology (Baltimore Md), 24(6), 1386–1391. https://doi.org/10.1053/jhep.1996.v24.pm0008938166.

    Article  PubMed  Google Scholar 

  43. Baba, Y., Hayashi, S., Nagasato, K., Higashi, M., Tosuji, N., Sonoda, S., & Yoshiura, T. (2018). Oxidative stress induced by portal vein embolization in fatty liver: Experimental study of a nonalcoholic steatohepatitis model. Biomedical reports, 9(4), 357–363. https://doi.org/10.3892/br.2018.1141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Chiang, H. J., Chang, W. P., Chiang, H. W., Lazo, M. Z., Chen, T. Y., Ou, H. Y., Tsang, L. L., Huang, T. L., Chen, C. L., & Cheng, Y. F. (2016). Magnetic resonance spectroscopy in living-donor liver transplantation. Transplantation Proceedings, 48(4), 1003–1006. https://doi.org/10.1016/j.transproceed.2015.10.068

    Article  PubMed  Google Scholar 

  45. Peng, C. J., Yuan, D., Li, B., Wei, Y. G., Yan, L. N., Wen, T. F., Zhao, J. C., Yang, J. Y., Wang, W. T., & Xu, M. Q. (2009). Body mass index evaluating donor hepatic steatosis in living donor liver transplantation. Transplantation Proceedings, 41(9), 3556–3559. https://doi.org/10.1016/j.transproceed.2009.06.235

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Yan-Chang Chen for his assistance in performing MRI experiments.

Funding

No funding was received for this research.

Author information

Authors and Affiliations

Authors

Contributions

Conception and design—C-HL and C-JJ; collection and assembly of data—C-HL, H-CC, W-CL, T-PL, and C-HJ; data analysis and interpretation—C-HL, C-JJ, H-CC, and Y-JL; manuscript writing—All authors; final approval of manuscript—All authors.

Corresponding author

Correspondence to Chun-Jung Juan.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical Approval

This study was approved by the institutional review board of Tri-Service General Hospital (TSGHIRB 099-05-265).

Additional information

Publisher’s Note

Springer nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, CH., Chang, HC., Liu, YJ. et al. Accumulated Hepatic Steatosis Grades Predicted by T2*-IDEAL Fat Fraction. J. Med. Biol. Eng. 43, 706–714 (2023). https://doi.org/10.1007/s40846-023-00819-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40846-023-00819-7

Keywords

Navigation