The progress in imaging evaluation of liver iron concentration_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHEN Xiaoli ^1,2 ,  SONG Bin ¹ , LI Zhenlin ¹ , HUANG Zixing ¹

1. Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, P. R. China;
2. Department of Radiology, Sichuan Cancer Hospital, Chengdu 610041, P. R. China;

Corresponding author：

SONG Bin, Email: cjr.songbin@vip.163.com

Keywords：

liver iron overload; computed tomography; magnetic resonance imaging; quantitative evaluation; review

DOI：

10.7507/1007-9424.201812035

Video：

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Objective To summarize the methods and research progress of imaging evaluation of liver iron concentration.Methods The current status and progress of different imaging techniques in liver iron overload research were reviewed by studying the relevant literatures at home and abroad. The methods for determining liver iron concentration and their advantages and disadvantages were summarized.Results The imaging methods for determining liver iron concentration mainly included traditional non-enhanced CT and dual energy CT examination, magnetic resonance signal intensity ratio, relative signal intensity index, T2 and R2 values, magnetic resonance spectroscopy, T2^* and R2^* values, susceptibility weighted imaging, and quantitative susceptibility mapping.Conclusion Liver iron quantification imaging method, including dual-energy CT and magnetic resonance imaging could non-invasively and accurately assess the liver iron overload.

Citation： CHEN Xiaoli, SONG Bin, LI Zhenlin, HUANG Zixing. The progress in imaging evaluation of liver iron concentration. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(2): 224-228. doi: 10.7507/1007-9424.201812035 Copy

1.	Papanikolaou G, Pantopoulos K. Systemic iron homeostasis and erythropoiesis. IUBMB Life, 2017, 69(6): 399-413.
2.	Golfeyz S, Lewis S, Weisberg IS. Hemochromatosis: pathophysiology, evaluation, and management of hepatic iron overload with a focus on MRI. Expert Rev Gastroenterol Hepatol, 2018, 12(8): 767-778.
3.	Carneiro AAO, Fernandes JP, Zago MA, et al. An alternating current superconductor susceptometric system to evaluate liver iron overload. Rev Sci Instrum, 2003, 74(6): 3098-3103.
4.	Pantopoulos K. Inherited disorders of iron overload. Front Nutr, 2018, 5: 103.
5.	Schönnagel BP, Fischer R, Nielsen P, et al. Iron quantification in iron overload disease using MRI. Rofo, 2013, 185(7): 621-627.
6.	Laroussi N, Mosnier JF, Morel Y, et al. Non alcoholic steatohepatitis: a multifactorial, frequent, paucysymptomatic liver disease with a fibrotic outcome. Gastroenterol Clin Biol, 2002, 26(5): 475-479.
7.	Puliyel M, Sposto R, Berdoukas VA, et al. Ferritin trends do not predict changes in total body iron in patients with transfusional iron overload. Am J Hematol, 2014, 89(4): 391-394.
8.	Angelucci E, Brittenham GM, McLaren CE, et al. Hepatic iron concentration and total body iron stores in thalassemia major. N Engl J Med, 2000, 343(5): 327-331.
9.	Brittenham GM, Badman DG, National institute of diabetes and digestive and kidney diseases (NIDDK) workshop. Noninvasive measurement of iron: report of an NIDDK workshop. Blood, 2003, 101(1): 15-19.
10.	Rose C, Vandevenne P, Bourgeois E, et al. Liver iron content assessment by routine and simple magnetic resonance imaging procedure in highly transfused patients. Eur J Haematol, 2006, 77(2): 145-149.
11.	Deugnier Y, Turlin B. Pathology of hepatic iron overload. World J Gastroenterol, 2007, 13(35): 4755-4760.
12.	Mortele KJ, Ros PR. Imaging of diffuse liver disease. Semin Liver Dis, 2001, 21(2): 195-212.
13.	Boll DT, Merkle EM. Diffuse liver disease: strategies for hepatic CT and MR imaging. Radiographics, 2009, 29(6): 1591-1614.
14.	Alústiza JM, Castiella A, De Juan MD, et al. Iron overload in the liver diagnostic and quantification. Eur J Radiol, 2007, 61(3): 499-506.
15.	王凯旋, 崔诗爽, 靳云鹏, 等. CT 测定肝脏铁含量的研究进展. 国际医学放射学杂志, 2014, 37(5): 434-437.
16.	Joe E, Kim SH, Lee KB, et al. Feasibility and accuracy of dual-source dual-energy CT for noninvasive determination of hepatic iron accumulation. Radiology, 2012, 262(1): 126-135.
17.	Luo XF, Xie XQ, Cheng S, et al. Dual-energy CT for patients suspected of having liver iron overload: can virtual iron content imaging accurately quantify liver iron content? Radiology, 2015, 277(1): 95-103.
18.	Werner S, Krauss B, Haberland U, et al. Dual-energy CT for liver iron quantification in patients with haematological disorders. Eur Radiol, 2018, [Epub ahead of print].
19.	Fischer MA, Reiner CS, Raptis D, et al. Quantification of liver iron content with CT-added value of dual-energy. Eur Radiol, 2011, 21(8): 1727-1732.
20.	Brissot P, Loréal O. Iron metabolism and related genetic diseases: a cleared land, keeping mysteries. J Hepatol, 2016, 64(2): 505-515.
21.	Sarigianni M, Liakos A, Vlachaki E, et al. Accuracy of magnetic resonance imaging in diagnosis of liver iron overload: a systematic review and meta-analysis. Clin Gastroenterol Hepatol, 2015, 13(1): 55-63.
22.	Gandon Y, Olivié D, Guyader D, et al. Non-invasive assessment of hepatic iron stores by MRI. Lancet, 2004, 363(9406): 357-362.
23.	Gandon Y. On-line liver iron quantification. https://imagemed.univ-rennes1.fr/en/mrquantif/online_quantif.php.
24.	Labranche R, Gilbert G, Cerny M, et al. Liver iron quantification with MR imaging: a primer for radiologists. Radiographics, 2018, 38(2): 392-412.
25.	Schieda N, Ramanathan S, Ryan J, et al. Diagnostic accuracy of dual-echo (in- and opposed-phase) T1-weighted gradient recalled echo for detection and grading of hepatic iron using quantitative and visual assessment. Eur Radiol, 2014, 24(7): 1437-1445.
26.	Virtanen JM, Pudas TK, Ratilainen JA, et al. Iron overload: accuracy of in-phase and out-of-phase MRI as a quick method to evaluate liver iron load in haematological malignancies and chronic liver disease. Br J Radiol, 2012, 85(1014): e162-e167.
27.	Jensen JH, Chandra R. Theory of nonexponential NMR signal decay in liver with iron overload or superparamagnetic iron oxide particles. Magn Reson Med, 2002, 47(6): 1131-1138.
28.	Health R. FerriScan: MRI measurement of liver iron concentration. http://www.resonancehealth.com/products/ferriscan-mri-measurement-of-liver-iron-concentration.html.
29.	St Pierre TG, Clark PR, Chua-anusorn W, et al. Noninvasive measurement and imaging of liver iron concentrations using proton magnetic resonance. Blood, 2005, 105(2): 855-861.
30.	Peng P, Huang Z, Long L, et al. Liver iron quantification by 3 tesla MRI: calibration on a rabbit model. J Magn Reson Imaging, 2013, 38(6): 1585-1590.
31.	Dixon RM, Styles P, al-Refaie FN, et al. Assessment of hepatic iron overload in thalassemic patients by magnetic resonance spectroscopy. Hepatology, 1994, 19(4): 904-910.
32.	Wang ZJ, Haselgrove JC, Martin MB, et al. Evaluation of iron overload by single voxel MRS measurement of liver T2. J Magn Reson Imaging, 2002, 15(4): 395-400.
33.	Pineda N, Sharma P, Xu Q, et al. Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at ¹H MR spectroscopy–a rapid and accurate technique. Radiology, 2009, 252(2): 568-576.
34.	Satkunasingham J, Besa C, Bane O, et al. Liver fat quantification: comparison of dual-echo and triple-echo chemical shift MRI to MR spectroscopy. Eur J Radiol, 2015, 84(8): 1452-1458.
35.	Lin H, Fu C, Kannengiesser S, et al. Quantitative analysis of hepatic iron in patients suspected of coexisting iron overload and steatosis using multi-echo single-voxel magnetic resonance spectroscopy: comparison with fat-saturated multi-echo gradient echo sequence. J Magn Reson Imaging, 2018, 48(1): 205-213.
36.	周燚, 宋彬, 胡富碧, 等. 磁共振定量技术在腹部实质性脏器铁过载中的研究进展. 中国普外基础与临床杂志, 2017, 24(9): 1139-1144.
37.	Horng DE, Hernando D, Reeder SB. Quantification of liver fat in the presence of iron overload. J Magn Reson Imaging, 2017, 45(2): 428-439.
38.	Wood JC, Enriquez C, Ghugre N, et al. MRI R2 and R2^* mapping accurately estimates hepatic iron concentration in transfusion-dependent thalassemia and sickle cell disease patients. Blood, 2005, 106(4): 1460-1465.
39.	Garbowski MW, Carpenter JP, Smith G, et al. Biopsy-based calibration of T2^* magnetic resonance for estimation of liver iron concentration and comparison with R2 Ferriscan. J Cardiovasc Magn Reson, 2014, 16: 40.
40.	Hankins JS, McCarville MB, Loeffler RB, et al. R2^* magnetic resonance imaging of the liver in patients with iron overload. Blood, 2009, 113(20): 4853-4855.
41.	Serai SD, Fleck RJ, Quinn CT, et al. Retrospective comparison of gradient recalled echo R2^* and spin-echo R2 magnetic resonance analysis methods for estimating liver iron content in children and adolescents. Pediatr Radiol, 2015, 45(11): 1629-1634.
42.	Krafft AJ, Loeffler RB, Song R, et al. Quantitative ultrashort echo time imaging for assessment of massive iron overload at 1.5 and3 Tesla. Magn Reson Med, 2017, 78(5): 1839-1851.
43.	Doyle EK, Toy K, Valdez B, et al. Ultra-short echo time images quantify high liver iron. Magn Reson Med, 2018, 79(3): 1579-1585.
44.	Sharma SD, Fischer R, Schoennagel BP, et al. MRI-based quantitative susceptibility mapping (QSM) and R2^* mapping of liver iron overload: comparison with SQUID-based biomagnetic liver susceptometry. Magn Reson Med, 2017, 78(1): 264-270.
45.	Schweser F, Deistung A, Reichenbach JR. Foundations of MRI phase imaging and processing for Quantitative Susceptibility Mapping (QSM). Z Med Phys, 2016, 26(1): 6-34.
46.	Wang Y, Liu T. Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med, 2015, 73(1): 82-101.
47.	Sharma SD, Hernando D, Horng DE, et al. Quantitative susceptibility mapping in the abdomen as an imaging biomarker of hepatic iron overload. Magn Reson Med, 2015, 74(3): 673-683.

1. Papanikolaou G, Pantopoulos K. Systemic iron homeostasis and erythropoiesis. IUBMB Life, 2017, 69(6): 399-413.
2. Golfeyz S, Lewis S, Weisberg IS. Hemochromatosis: pathophysiology, evaluation, and management of hepatic iron overload with a focus on MRI. Expert Rev Gastroenterol Hepatol, 2018, 12(8): 767-778.
3. Carneiro AAO, Fernandes JP, Zago MA, et al. An alternating current superconductor susceptometric system to evaluate liver iron overload. Rev Sci Instrum, 2003, 74(6): 3098-3103.
4. Pantopoulos K. Inherited disorders of iron overload. Front Nutr, 2018, 5: 103.
5. Schönnagel BP, Fischer R, Nielsen P, et al. Iron quantification in iron overload disease using MRI. Rofo, 2013, 185(7): 621-627.
6. Laroussi N, Mosnier JF, Morel Y, et al. Non alcoholic steatohepatitis: a multifactorial, frequent, paucysymptomatic liver disease with a fibrotic outcome. Gastroenterol Clin Biol, 2002, 26(5): 475-479.
7. Puliyel M, Sposto R, Berdoukas VA, et al. Ferritin trends do not predict changes in total body iron in patients with transfusional iron overload. Am J Hematol, 2014, 89(4): 391-394.
8. Angelucci E, Brittenham GM, McLaren CE, et al. Hepatic iron concentration and total body iron stores in thalassemia major. N Engl J Med, 2000, 343(5): 327-331.
9. Brittenham GM, Badman DG, National institute of diabetes and digestive and kidney diseases (NIDDK) workshop. Noninvasive measurement of iron: report of an NIDDK workshop. Blood, 2003, 101(1): 15-19.
10. Rose C, Vandevenne P, Bourgeois E, et al. Liver iron content assessment by routine and simple magnetic resonance imaging procedure in highly transfused patients. Eur J Haematol, 2006, 77(2): 145-149.
11. Deugnier Y, Turlin B. Pathology of hepatic iron overload. World J Gastroenterol, 2007, 13(35): 4755-4760.
12. Mortele KJ, Ros PR. Imaging of diffuse liver disease. Semin Liver Dis, 2001, 21(2): 195-212.
13. Boll DT, Merkle EM. Diffuse liver disease: strategies for hepatic CT and MR imaging. Radiographics, 2009, 29(6): 1591-1614.
14. Alústiza JM, Castiella A, De Juan MD, et al. Iron overload in the liver diagnostic and quantification. Eur J Radiol, 2007, 61(3): 499-506.
15. 王凯旋, 崔诗爽, 靳云鹏, 等. CT 测定肝脏铁含量的研究进展. 国际医学放射学杂志, 2014, 37(5): 434-437.
16. Joe E, Kim SH, Lee KB, et al. Feasibility and accuracy of dual-source dual-energy CT for noninvasive determination of hepatic iron accumulation. Radiology, 2012, 262(1): 126-135.
17. Luo XF, Xie XQ, Cheng S, et al. Dual-energy CT for patients suspected of having liver iron overload: can virtual iron content imaging accurately quantify liver iron content? Radiology, 2015, 277(1): 95-103.
18. Werner S, Krauss B, Haberland U, et al. Dual-energy CT for liver iron quantification in patients with haematological disorders. Eur Radiol, 2018, [Epub ahead of print].
19. Fischer MA, Reiner CS, Raptis D, et al. Quantification of liver iron content with CT-added value of dual-energy. Eur Radiol, 2011, 21(8): 1727-1732.
20. Brissot P, Loréal O. Iron metabolism and related genetic diseases: a cleared land, keeping mysteries. J Hepatol, 2016, 64(2): 505-515.
21. Sarigianni M, Liakos A, Vlachaki E, et al. Accuracy of magnetic resonance imaging in diagnosis of liver iron overload: a systematic review and meta-analysis. Clin Gastroenterol Hepatol, 2015, 13(1): 55-63.
22. Gandon Y, Olivié D, Guyader D, et al. Non-invasive assessment of hepatic iron stores by MRI. Lancet, 2004, 363(9406): 357-362.
23. Gandon Y. On-line liver iron quantification. https://imagemed.univ-rennes1.fr/en/mrquantif/online_quantif.php.
24. Labranche R, Gilbert G, Cerny M, et al. Liver iron quantification with MR imaging: a primer for radiologists. Radiographics, 2018, 38(2): 392-412.
25. Schieda N, Ramanathan S, Ryan J, et al. Diagnostic accuracy of dual-echo (in- and opposed-phase) T1-weighted gradient recalled echo for detection and grading of hepatic iron using quantitative and visual assessment. Eur Radiol, 2014, 24(7): 1437-1445.
26. Virtanen JM, Pudas TK, Ratilainen JA, et al. Iron overload: accuracy of in-phase and out-of-phase MRI as a quick method to evaluate liver iron load in haematological malignancies and chronic liver disease. Br J Radiol, 2012, 85(1014): e162-e167.
27. Jensen JH, Chandra R. Theory of nonexponential NMR signal decay in liver with iron overload or superparamagnetic iron oxide particles. Magn Reson Med, 2002, 47(6): 1131-1138.
28. Health R. FerriScan: MRI measurement of liver iron concentration. http://www.resonancehealth.com/products/ferriscan-mri-measurement-of-liver-iron-concentration.html.
29. St Pierre TG, Clark PR, Chua-anusorn W, et al. Noninvasive measurement and imaging of liver iron concentrations using proton magnetic resonance. Blood, 2005, 105(2): 855-861.
30. Peng P, Huang Z, Long L, et al. Liver iron quantification by 3 tesla MRI: calibration on a rabbit model. J Magn Reson Imaging, 2013, 38(6): 1585-1590.
31. Dixon RM, Styles P, al-Refaie FN, et al. Assessment of hepatic iron overload in thalassemic patients by magnetic resonance spectroscopy. Hepatology, 1994, 19(4): 904-910.
32. Wang ZJ, Haselgrove JC, Martin MB, et al. Evaluation of iron overload by single voxel MRS measurement of liver T2. J Magn Reson Imaging, 2002, 15(4): 395-400.
33. Pineda N, Sharma P, Xu Q, et al. Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at ¹H MR spectroscopy–a rapid and accurate technique. Radiology, 2009, 252(2): 568-576.
34. Satkunasingham J, Besa C, Bane O, et al. Liver fat quantification: comparison of dual-echo and triple-echo chemical shift MRI to MR spectroscopy. Eur J Radiol, 2015, 84(8): 1452-1458.
35. Lin H, Fu C, Kannengiesser S, et al. Quantitative analysis of hepatic iron in patients suspected of coexisting iron overload and steatosis using multi-echo single-voxel magnetic resonance spectroscopy: comparison with fat-saturated multi-echo gradient echo sequence. J Magn Reson Imaging, 2018, 48(1): 205-213.
36. 周燚, 宋彬, 胡富碧, 等. 磁共振定量技术在腹部实质性脏器铁过载中的研究进展. 中国普外基础与临床杂志, 2017, 24(9): 1139-1144.
37. Horng DE, Hernando D, Reeder SB. Quantification of liver fat in the presence of iron overload. J Magn Reson Imaging, 2017, 45(2): 428-439.
38. Wood JC, Enriquez C, Ghugre N, et al. MRI R2 and R2^* mapping accurately estimates hepatic iron concentration in transfusion-dependent thalassemia and sickle cell disease patients. Blood, 2005, 106(4): 1460-1465.
39. Garbowski MW, Carpenter JP, Smith G, et al. Biopsy-based calibration of T2^* magnetic resonance for estimation of liver iron concentration and comparison with R2 Ferriscan. J Cardiovasc Magn Reson, 2014, 16: 40.
40. Hankins JS, McCarville MB, Loeffler RB, et al. R2^* magnetic resonance imaging of the liver in patients with iron overload. Blood, 2009, 113(20): 4853-4855.
41. Serai SD, Fleck RJ, Quinn CT, et al. Retrospective comparison of gradient recalled echo R2^* and spin-echo R2 magnetic resonance analysis methods for estimating liver iron content in children and adolescents. Pediatr Radiol, 2015, 45(11): 1629-1634.
42. Krafft AJ, Loeffler RB, Song R, et al. Quantitative ultrashort echo time imaging for assessment of massive iron overload at 1.5 and3 Tesla. Magn Reson Med, 2017, 78(5): 1839-1851.
43. Doyle EK, Toy K, Valdez B, et al. Ultra-short echo time images quantify high liver iron. Magn Reson Med, 2018, 79(3): 1579-1585.
44. Sharma SD, Fischer R, Schoennagel BP, et al. MRI-based quantitative susceptibility mapping (QSM) and R2^* mapping of liver iron overload: comparison with SQUID-based biomagnetic liver susceptometry. Magn Reson Med, 2017, 78(1): 264-270.
45. Schweser F, Deistung A, Reichenbach JR. Foundations of MRI phase imaging and processing for Quantitative Susceptibility Mapping (QSM). Z Med Phys, 2016, 26(1): 6-34.
46. Wang Y, Liu T. Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med, 2015, 73(1): 82-101.
47. Sharma SD, Hernando D, Horng DE, et al. Quantitative susceptibility mapping in the abdomen as an imaging biomarker of hepatic iron overload. Magn Reson Med, 2015, 74(3): 673-683.

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CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

The progress in imaging evaluation of liver iron concentration

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