Liver intravoxel incoherent motion (IVIM) magnetic resonance imaging: A comprehensive review of published data on normal values and applications for fibrosis and tumor evaluation

Quantitative Imaging in Medicine and Surgery

Volumn 7, Issue 1, 2017, Pages 59-78

  Li, Yáo T ^a   Cercueil, Jean Pierre ^b   Yuan, Jing ^c   Chen, Weitian ^a   Loffroy, Romaric ^b   Wáng, Yì Xiáng J ^a  

^a Prince of Wales Hospital   (Hong Kong)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c HONG KONG SANATORIUM AND HOSPITAL   (Hong Kong)

Author keywords

Diffusion; Fibrosis; Intravoxel incoherent motion (IVIM); Liver; Magnetic resonance imaging (MRI); Perfusion; Tumour

Indexed keywords

APPARENT DIFFUSION COEFFICIENT; ARTICLE; BREATHING PATTERN; DIAGNOSTIC VALUE; DISEASE CLASSIFICATION; HUMAN; IMAGE PROCESSING; INFORMATION PROCESSING; INTRAVOXEL INCOHERENT MOTION; LIVER FIBROSIS; LIVER PERFUSION; LIVER TUMOR; MAGNETIC FIELD; MEASUREMENT ACCURACY; MONITORING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RADIOLOGICAL PARAMETERS; RESPIRATORY FUNCTION; TUMOR DIFFERENTIATION;

EID: 85014313965     PISSN: 22234292     EISSN: 22234306     Source Type: Journal    
DOI: 10.21037/qims.2017.02.03     Document Type: Article

References (67)

1. Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 1988;168:497-505.
2. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 2007;188:1622-35.
3. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986;161:401-7.
4. Le Bihan D, Turner R. The capillary network: a link between IVIM and classical perfusion. Magn Reson Med 1992;27:171-8.
5. Le Bihan D, Turner R, Moonen CT, Pekar J. Imaging of diffusion and microcirculation with gradient sensitization: design, strategy, and significance. J Magn Reson Imaging 1991;1:7-28.
6. Murphy P, Hooker J, Ang B, Wolfson T, Gamst A, Bydder M, Middleton M, Peterson M, Behling C, Loomba R, Sirlin C. Associations between histologic features of nonalcoholic fatty liver disease (NAFLD) and quantitative diffusion-weighted MRI measurements in adults. J Magn Reson Imaging 2015;41:1629-38.
7. Yamada I, Aung W, Himeno Y, Nakagawa T, Shibuya H. Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. Radiology 1999;210:617-23.
8. Guiu B, Cercueil JP. Liver diffusion-weighted MR imaging: the tower of Babel? Eur Radiol 2011;21:463-7.
9. Guiu B, Petit JM, Capitan V, Aho S, Masson D, Lefevre PH, Favelier S, Loffroy R, Vergès B, Hillon P, Krausé D, Cercueil JP. Intravoxel incoherent motion diffusion-weighted imaging in nonalcoholic fatty liver disease: a 3.0-T MR study. Radiology 2012;265:96-103.
10. Lu PX, Huang H, Yuan J, Zhao F, Chen ZY, Zhang Q, Ahuja AT, Zhou BP, Wáng YX. Decreases in molecular diffusion, perfusion fraction and perfusion-related diffusion in fibrotic livers: a prospective clinical intravoxel incoherent motion MR imaging study. PLoS One 2014;9:e113846.
11. Luciani A, Vignaud A, Cavet M, Nhieu JT, Mallat A, Ruel L, Laurent A, Deux JF, Brugieres P, Rahmouni A. Liver cirrhosis: intravoxel incoherent motion MR imaging - pilot study. Radiology 2008;249:891-9.
12. Patel J, Sigmund EE, Rusinek H, Oei M, Babb JS, Taouli B. Diagnosis of cirrhosis with intravoxel incoherent motion diffusion MRI and dynamic contrast-enhanced MRI alone and in combination: preliminary experience. J Magn Reson Imaging 2010;31:589-600.
13. Grech-Sollars M, Hales PW, Miyazaki K, Raschke F, Rodriguez D, Wilson M, Gill SK, Banks T, Saunders DE, Clayden JD, Gwilliam MN, Barrick TR, Morgan PS, Davies NP, Rossiter J, Auer DP, Grundy R, Leach MO, Howe FA, Peet AC, Clark CA. Multi-centre reproducibility of diffusion MRI parameters for clinical sequences in the brain. NMR Biomed 2015;28:468-85.
14. Wang YX. Medical imaging in pharmaceutical clinical trials: what radiologists should know. Clin Radiol 2005;60:1051-7.
15. Dyvorne HA, Galea N, Nevers T, Fiel MI, Carpenter D, Wong E, Orton M, de Oliveira A, Feiweier T, Vachon ML, Babb JS, Taouli B. Diffusion-weighted imaging of the liver with multiple b values: effect of diffusion gradient polarity and breathing acquisition on image quality and intravoxel incoherent motion parameters - a pilot study. Radiology 2013;266:920-9.
16. Lemke A, Stieltjes B, Schad LR, Laun FB. Toward an optimal distribution of b values for intravoxel incoherent motion imaging. Magn Reson Imaging 2011;29:766-76.
17. Andreou A, Koh DM, Collins DJ, Blackledge M, Wallace T, Leach MO, Orton MR. Measurement reproducibility of perfusion fraction and pseudodiffusion coefficient derived by intravoxel incoherent motion diffusion-weighted MR imaging in normal liver and metastases. Eur Radiol 2013;23:428-34.
18. Chen C, Wang B, Shi D, Fu F, Zhang J, Wen Z, Zhu S, Xu J, Lin Q, Li J, Dou S. Initial study of biexponential model of intravoxel incoherent motion magnetic resonance imaging in evaluation of the liver fibrosis. Chin Med J (Engl) 2014;127:3082-7.
19. Leporq B, Saint-Jalmes H, Rabrait C, Pilleul F, Guillaud O, Dumortier J, Scoazec JY, Beuf O. Optimization of intra-voxel incoherent motion imaging at 3.0 Tesla for fast liver examination. J Magn Reson Imaging 2015;41:1209-17.
20. Taimouri V, Afacan O, Perez-Rossello JM, Callahan MJ, Mulkern RV, Warfield SK, Freiman M. Spatially constrained incoherent motion method improves diffusion-weighted MRI signal decay analysis in the liver and spleen. Med Phys 2015;42:1895-903.
21. Wurnig MC, Kenkel D, Filli L, Boss A. A Standardized Parameter-Free Algorithm for Combined Intravoxel Incoherent Motion and Diffusion Kurtosis Analysis of Diffusion Imaging Data. Invest Radiol 2016;51:203-10.
22. Jerome NP, Orton MR, d'Arcy JA, Collins DJ, Koh DM, Leach MO. Comparison of free-breathing with navigator-controlled acquisition regimes in abdominal diffusion-weighted magnetic resonance images: Effect on ADC and IVIM statistics. J Magn Reson Imaging 2014;39:235-40.
23. Lee Y, Lee SS, Kim N, Kim E, Kim YJ, Yun SC, Kühn B, Kim IS, Park SH, Kim SY, Lee MG. Intravoxel incoherent motion diffusion-weighted MR imaging of the liver: effect of triggering methods on regional variability and measurement repeatability of quantitative parameters. Radiology 2015;274:405-15.
24. Regini F, Colagrande S, Mazzoni LN, Busoni S, Matteuzzi B, Santini P, Wyttenbach R. Assessment of Liver Perfusion by IntraVoxel Incoherent Motion (IVIM) Magnetic Resonance-Diffusion-Weighted Imaging: Correlation With Phase-Contrast Portal Venous Flow Measurements. J Comput Assist Tomogr 2015;39:365-72.
25. Carter JH, Welch CS, Barron RE. Changes in the hepatic blood vessels in cirrhosis of the liver. Surg Gynecol Obstet 1961;113:133-7.
26. Bearn AG, Billing B, Sherlock S.The effect of adrenaline and noradrenaline on hepatic blood flow and splanchnic carbohydrate metabolism in man. J Physiol 1951;115:430-41.
27. Loisance DY, Lenriot JP. Critical review of methods of measurement of hepatic blood flow in animal experimentation and human clinical practice. Coeur Med Interne 1972;11:547-57.
28. Chow PK, Yu WK, Soo KC, Chan ST. The measurement of liver blood flow: a review of experimental and clinical methods. J Surg Res 2003;112:1-11.
29. Greenway CV, Stark RD. Hepatic vascular bed. Physiol Rev 1971;51:23-65.
30. Strandell T, Erwald R, Kulling KG, Lundbergh P, Marions O, Wiechel KL. Measurement of dual hepatic blood flow in awake patients. J Appl Physiol 1973;35:755-61.
31. Magalotti D, Volta U, Bonfiglioli A, Ramilli S, Berzigotti A, Zoli M. Splanchnic haemodynamics in patients with coeliac disease: effects of a gluten-free diet. Dig Liver Dis 2003;35:262-8.
32. Glick Z, Wickler SJ, Stern JS, Horwitz BA. Regional blood flow in rats after a single low-protein, high-carbohydrate test meal. Am J Physiol 1984;247:R160-6.
33. Lemke A, Laun FB, Simon D, Stieltjes B, Schad LR. An in vivo verification of the intravoxel incoherent motion effect in diffusion-weighted imaging of the abdomen. Magn Reson Med 2010;64:1580-5.
34. ter Voert EE, Delso G, Porto M, Huellner M, Veit-Haibach P. Intravoxel Incoherent Motion Protocol Evaluation and Data Quality in Normal and Malignant Liver Tissue and Comparison to the Literature. Invest Radiol 2016;51:90-9.
35. Hectors SJ, Wagner M, Besa C, Bane O, Dyvorne HA, Fiel MI, Zhu H, Donovan M, Taouli B. Intravoxel incoherent motion diffusion-weighted imaging of hepatocellular carcinoma: Is there a correlation with flow and perfusion metrics obtained with dynamic contrast-enhanced MRI? J Magn Reson Imaging 2016;44:856-64.
36. Taouli B, Beer AJ, Chenevert T, Collins D, Lehman C, Matos C, Padhani AR, Rosenkrantz AB, Shukla-Dave A, Sigmund E, Tanenbaum L, Thoeny H, Thomassin-Naggara I, Barbieri S, Corcuera-Solano I, Orton M, Partridge SC, Koh DM. Diffusion-weighted imaging outside the brain: Consensus statement from an ISMRM-sponsored workshop. J Magn Reson Imaging 2016;44:521-40.
37. Barbieri S, Donati OF, Froehlich JM, Thoeny HC. Comparison of Intravoxel Incoherent Motion Parameters across MR Imagers and Field Strengths: Evaluation in Upper Abdominal Organs. Radiology 2016;279:784-94.
38. Barbieri S, Donati OF, Froehlich JM, Thoeny HC. Impact of the calculation algorithm on biexponential fitting of diffusion-weighted MRI in upper abdominal organs. Magn Reson Med 2016;75:2175-84.
39. Pekar J, Moonen CT, van Zijl PC. On the precision of diffusion/perfusion imaging by gradient sensitization. Magn Reson Med 1992;23:122-9.
40. Kakite S, Dyvorne H, Besa C, Cooper N, Facciuto M, Donnerhack C, Taouli B. Hepatocellular carcinoma: short-term reproducibility of apparent diffusion coefficient and intravoxel incoherent motion parameters at 3.0T. J Magn Reson Imaging 2015;41:149-56.
41. Wurnig MC, Donati OF, Ulbrich E, Filli L, Kenkel D, Thoeny HC, Boss A. Systematic analysis of the intravoxel incoherent motion threshold separating perfusion and diffusion effects: Proposal of a standardized algorithm. Magn Reson Med 2015;74:1414-22.
42. Zhu L, Cheng Q, Luo W, Bao L, Guo G. A comparative study of apparent diffusion coefficient and intravoxel incoherent motion-derived parameters for the characterization of common solid hepatic tumors. Acta Radiol 2015;56:1411-8.
43. Dyvorne H, Jajamovich G, Kakite S, Kuehn B, Taouli B. Intravoxel incoherent motion diffusion imaging of the liver: optimal b-value subsampling and impact on parameter precision and reproducibility. Eur J Radiol 2014;83:2109-13.
44. Delattre BM, Viallon M, Wei H, Zhu YM, Feiweier T, Pai VM, Wen H, Croisille P. In vivo cardiac diffusion-weighted magnetic resonance imaging: quantification of normal perfusion and diffusion coefficients with intravoxel incoherent motion imaging. Invest Radiol 2012;47:662-70.
45. Hayashi T, Miyati T, Takahashi J, Fukuzawa K, Sakai H, Tano M, Saitoh S. Diffusion analysis with triexponential function in liver cirrhosis. J Magn Reson Imaging 2013;38:148-53.
46. Chung SR, Lee SS, Kim N, Yu ES, Kim E, Kühn B, Kim IS. Intravoxel incoherent motion MRI for liver fibrosis assessment: a pilot study. Acta Radiol 2015;56:1428-36.
47. Leitão HS, Doblas S, d'Assignies G, Garteiser P, Daire JL, Paradis V, Geraldes CF, Vilgrain V, Van Beers BE. Fat deposition decreases diffusion parameters at MRI: a study in phantoms and patients with liver steatosis. Eur Radiol 2013;23:461-7.
48. Cercueil JP, Petit JM, Nougaret S, Soyer P, Fohlen A, Pierredon-Foulongne MA, Schembri V, Delhom E, Schmidt S, Denys A, Aho S, Guiu B. Intravoxel incoherent motion diffusion-weighted imaging in the liver: comparison of mono-, bi-and tri-exponential modelling at 3.0-T. Eur Radiol 2015;25:1541-50.
49. Gurney-Champion OJ, Froeling M, Klaassen R, Runge JH, Bel A, van Laarhoven HW, Stoker J, Nederveen AJ. Minimizing the Acquisition Time for Intravoxel Incoherent Motion Magnetic Resonance Imaging Acquisitions in the Liver and Pancreas. Invest Radiol 2016;51:211-20.
50. Cui Y, Dyvorne H, Besa C, Cooper N, Taouli B. IVIM Diffusion-weighted Imaging of the Liver at 3.0T: Comparison with 1.5T. Eur J Radiol Open 2015;2:123-8.
51. Ichikawa S, Motosugi U, Morisaka H, Sano K, Ichikawa T, Enomoto N, Matsuda M, Fujii H, Onishi H. MRI-based staging of hepatic fibrosis: Comparison of intravoxel incoherent motion diffusion-weighted imaging with magnetic resonance elastography. J Magn Reson Imaging 2015;42:204-10.
52. Gambarota G, Hitti E, Leporq B, Saint-Jalmes H, Beuf O. Eliminating the blood-flow confounding effect in intravoxel incoherent motion (IVIM) using the non-negative least square analysis in liver. Magn Reson Med 2017;77:310-7.
53. Filli L, Wurnig MC, Luechinger R, Eberhardt C, Guggenberger R, Boss A. Whole-body intravoxel incoherent motion imaging. Eur Radiol 2015;25:2049-58.
54. Zhang J, Guo Y, Tan X, Zheng Z, He M, Xu J, Mei Y, Zhang J, Zhao X, Wang C, Feng Y, Chan Q, Wu Y, Xu Y. MRI-based estimation of liver function by intravoxel incoherent motion diffusion-weighted imaging. Magn Reson Imaging 2016;34:1220-5.
55. França M, Martí-Bonmatí L, Alberich-Bayarri Á, Oliveira P, Guimaraes S, Oliveira J, Amorim J, Gonzalez JS, Vizcaíno JR, Miranda HP. Evaluation of fibrosis and inflammation in diffuse liver diseases using intravoxel incoherent motion diffusion-weighted MR imaging. Abdom Radiol (NY) 2016 . [Epub ahead of print]. doi: 10.1007/s00261-016-0899-0
56. Neil JJ, Bretthorst GL. On the use of Bayesian probability theory for analysis of exponential decay data: an example taken from intravoxel incoherent motion experiments. Magn Reson Med 1993;29:642-7.
57. Zhang Y, Jin N, Deng J, Guo Y, White SB, Yang GY, Omary RA, Larson AC. Intra-voxel incoherent motion MRI in rodent model of diethylnitrosamine-induced liver fibrosis. Magn Reson Imaging 2013;31:1017-21.
58. Chow AM, Gao DS, Fan SJ, Qiao Z, Lee FY, Yang J, Man K, Wu EX. Liver fibrosis: an intravoxel incoherent motion (IVIM) study. J Magn Reson Imaging 2012;36:159-67.
59. Joo I, Lee JM, Yoon JH, Jang JJ, Han JK, Choi BI. Nonalcoholic fatty liver disease: intravoxel incoherent motion diffusion-weighted MR imaging-an experimental study in a rabbit model. Radiology 2014;270:131-40.
60. Wang YX, Deng M. Medical imaging in new drug clinical development. J Thorac Dis 2010;2:245-52.
61. Joo I, Lee JM, Han JK, Choi BI. Intravoxel incoherent motion diffusion-weighted MR imaging for monitoring the therapeutic efficacy of the vascular disrupting agent CKD-516 in rabbit VX2 liver tumors. Radiology 2014;272:417-26.
62. Joo I, Lee JM, Grimm R, Han JK, Choi BI. Monitoring Vascular Disrupting Therapy in a Rabbit Liver Tumor Model: Relationship between Tumor Perfusion Parameters at IVIM Diffusion-weighted MR Imaging and Those at Dynamic Contrast-enhanced MR Imaging. Radiology 2016;278:104-13.
63. Yang SH, Lin J, Lu F, Han ZH, Fu CX, Lv P, Liu H, Gao DM. Evaluation of antiangiogenic and antiproliferative effects of sorafenib by sequential histology and intravoxel incoherent motion diffusion-weighted imaging in an orthotopic hepatocellular carcinoma xenograft model. J Magn Reson Imaging 2017;45:270-80.
64. Pieper CC, Sprinkart AM, Meyer C, König R, Schild HH, Kukuk GM, Mürtz P. Evaluation of a Simplified Intravoxel Incoherent Motion (IVIM) Analysis of Diffusion-Weighted Imaging for Prediction of Tumor Size Changes and Imaging Response in Breast Cancer Liver Metastases Undergoing Radioembolization: A Retrospective Single Center Analysis. Medicine (Baltimore) 2016;95:e3275.
65. Menezes-Reis R, Salmon CE, Bonugli GP, Mazoroski D, Tamashiro MH, Savarese LG, Nogueira-Barbosa MH. Lumbar intervertebral discs T2 relaxometry and T1ρ relaxometry correlation with age in asymptomatic young adults. Quant Imaging Med Surg 2016;6:402-12.
66. Wang YX, Zhao F, Griffith JF, Mok GS, Leung JC, Ahuja AT, Yuan J. T1rho and T2 relaxation times for lumbar disc degeneration: an in vivo comparative study at 3.0-Tesla MRI. Eur Radiol 2013;23:228-34.
67. Klauss M, Mayer P, Maier-Hein K, Laun FB, Mehrabi A, Kauczor HU, Stieltjes B. IVIM-diffusion-MRI for the differentiation of solid benign and malign hypervascular liver lesions-Evaluation with two different MR scanners. Eur J Radiol 2016;85:1289-94.