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Published in: European Radiology 4/2012

Open Access 01-04-2012 | Magnetic Resonance

Effects of microperfusion in hepatic diffusion weighted imaging

Authors: Hildebrand Dijkstra, Paul Baron, Peter Kappert, Matthijs Oudkerk, Paul E. Sijens

Published in: European Radiology | Issue 4/2012

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Abstract

Objective

Clinical hepatic diffusion weighted imaging (DWI) generally relies on mono-exponential diffusion. The aim was to demonstrate that mono-exponential diffusion in the liver is contaminated by microperfusion and that the bi-exponential model is required.

Methods

Nineteen fasting healthy volunteers were examined with DWI (seven b-values) using fat suppression and respiratory triggering (1.5 T). Five different regions in the liver were analysed regarding the mono-exponentially fitted apparent diffusion coefficient (ADC), and the bi-exponential model: molecular diffusion (D slow ), microperfusion (D fast ) and the respective fractions (f slow/fast ). Data were compared using ANOVA and Kruskal–Wallis tests. Simulations were performed by repeating our data analyses, using just the DWI series acquired with b-values approximating those of previous studies.

Results

Median mono-exponentially fitted ADCs varied significantly (P < 0.001) between 1.107 and 1.423 × 10−3 mm2/s for the five regions. Bi-exponential fitted Dslow varied between 0.923 and 1.062 × 10−3 mm2/s without significant differences (P = 0.140). D fast varied significantly, between 17.8 and 46.8 × 10−3 mm2/s (P < 0.001). F-tests showed that the diffusion data fitted the bi-exponential model significantly better than the mono-exponential model (F > 21.4, P < 0.010). These results were confirmed by the simulations.

Conclusion

ADCs of normal liver tissue are significantly dependent on the measurement location because of substantial microperfusion contamination; therefore the bi-exponential model should be used.

Key Points

  • Diffusion weighted MR imaging helps clinicians to differentiate tumours by diffusion properties
  • Fast moving water molecules experience microperfusion, slow molecules diffusion
  • Hepatic diffusion should be measured by bi-exponential models to avoid microperfusion contamination
  • Mono-exponential models are contaminated with microperfusion, resulting in apparent regional diffusion differences
  • Bi-exponential models are necessary to measure diffusion and microperfusion in the liver
Literature
1.
go back to reference Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407PubMed Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407PubMed
2.
go back to reference Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505PubMed Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505PubMed
3.
go back to reference Le Bihan D, Turner R, Moonen CT, Pekar J (1991) Imaging of diffusion and microcirculation with gradient sensitization: design, strategy, and significance. J Magn Reson Imaging 1:7–28PubMedCrossRef Le Bihan D, Turner R, Moonen CT, Pekar J (1991) Imaging of diffusion and microcirculation with gradient sensitization: design, strategy, and significance. J Magn Reson Imaging 1:7–28PubMedCrossRef
4.
go back to reference Müller MF, Prasad P, Siewert B, Nissenbaum MA, Raptopoulos V, Edelman RR (1994) Abdominal diffusion mapping with use of a whole-body echo-planar system. Radiology 190:475–478PubMed Müller MF, Prasad P, Siewert B, Nissenbaum MA, Raptopoulos V, Edelman RR (1994) Abdominal diffusion mapping with use of a whole-body echo-planar system. Radiology 190:475–478PubMed
5.
go back to reference Turner R, Le Bihan D, Maier J, Vavrek R, Hedges LK, Pekar J (1990) Echo-planar imaging of intravoxel incoherent motion. Radiology 177:407–414PubMed Turner R, Le Bihan D, Maier J, Vavrek R, Hedges LK, Pekar J (1990) Echo-planar imaging of intravoxel incoherent motion. Radiology 177:407–414PubMed
6.
go back to reference Namimoto T, Yamashita Y, Sumi S, Tang Y, Takahashi M (1997) Focal liver masses: characterization with diffusion-weighted echo-planar MR imaging. Radiology 204:739–744PubMed Namimoto T, Yamashita Y, Sumi S, Tang Y, Takahashi M (1997) Focal liver masses: characterization with diffusion-weighted echo-planar MR imaging. Radiology 204:739–744PubMed
7.
go back to reference Ichikawa T, Haradome H, Hachiya J, Nitatori T, Araki T (1999) Diffusion-weighted MR imaging with single-shot echo-planar imaging in the upper abdomen: preliminary clinical experience in 61 patients. Abdom Imaging 24:456–461PubMedCrossRef Ichikawa T, Haradome H, Hachiya J, Nitatori T, Araki T (1999) Diffusion-weighted MR imaging with single-shot echo-planar imaging in the upper abdomen: preliminary clinical experience in 61 patients. Abdom Imaging 24:456–461PubMedCrossRef
8.
go back to reference Kim T, Murakami T, Takahashi S, Hori M, Tsuda K, Nakamura H (1999) Diffusion-weighted single-shot echoplanar MR imaging for liver disease. AJR Am J Roentgenol 173:393–398PubMed Kim T, Murakami T, Takahashi S, Hori M, Tsuda K, Nakamura H (1999) Diffusion-weighted single-shot echoplanar MR imaging for liver disease. AJR Am J Roentgenol 173:393–398PubMed
9.
go back to reference Yamada I, Aung W, Himeno Y, Nakagawa T, Shibuya H (1999) Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. Radiology 210:617–623PubMed Yamada I, Aung W, Himeno Y, Nakagawa T, Shibuya H (1999) Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. Radiology 210:617–623PubMed
10.
go back to reference Moteki T, Horikoshi H, Oya N, Aoki J, Endo K (2002) Evaluation of hepatic lesions and hepatic parenchyma using diffusion-weighted reordered turboFLASH magnetic resonance images. J Magn Reson Imaging 15:564–572PubMedCrossRef Moteki T, Horikoshi H, Oya N, Aoki J, Endo K (2002) Evaluation of hepatic lesions and hepatic parenchyma using diffusion-weighted reordered turboFLASH magnetic resonance images. J Magn Reson Imaging 15:564–572PubMedCrossRef
11.
go back to reference Moteki T, Horikoshi H (2006) Evaluation of hepatic lesions and hepatic parenchyma using diffusion-weighted echo-planar MR with three values of gradient b-factor. J Magn Reson Imaging 24:637–645PubMedCrossRef Moteki T, Horikoshi H (2006) Evaluation of hepatic lesions and hepatic parenchyma using diffusion-weighted echo-planar MR with three values of gradient b-factor. J Magn Reson Imaging 24:637–645PubMedCrossRef
12.
go back to reference Coenegrachts K, Delanote J, Ter Beek L et al (2009) Evaluation of true diffusion, perfusion factor, and apparent diffusion coefficient in non-necrotic liver metastases and uncomplicated liver hemangiomas using black-blood echo planar imaging. Eur J Radiol 69:131–138PubMedCrossRef Coenegrachts K, Delanote J, Ter Beek L et al (2009) Evaluation of true diffusion, perfusion factor, and apparent diffusion coefficient in non-necrotic liver metastases and uncomplicated liver hemangiomas using black-blood echo planar imaging. Eur J Radiol 69:131–138PubMedCrossRef
13.
go back to reference Luciani A, Vignaud A, Cavet M et al (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging–pilot study. Radiology 249:891–899PubMedCrossRef Luciani A, Vignaud A, Cavet M et al (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging–pilot study. Radiology 249:891–899PubMedCrossRef
14.
go back to reference Moteki T, Horikoshi H (2011) Evaluation of noncirrhotic hepatic parenchyma with and without significant portal vein stenosis using diffusion-weighted echo-planar MR on the basis of multiple-perfusion-components theory. Magn Reson Imaging 29:64–73PubMedCrossRef Moteki T, Horikoshi H (2011) Evaluation of noncirrhotic hepatic parenchyma with and without significant portal vein stenosis using diffusion-weighted echo-planar MR on the basis of multiple-perfusion-components theory. Magn Reson Imaging 29:64–73PubMedCrossRef
15.
16.
go back to reference Taouli B, Vilgrain V, Dumont E, Daire JL, Fan B, Menu Y (2003) Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients. Radiology 226:71–78PubMedCrossRef Taouli B, Vilgrain V, Dumont E, Daire JL, Fan B, Menu Y (2003) Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients. Radiology 226:71–78PubMedCrossRef
17.
go back to reference Talwalkar JA, Yin M, Fidler JL, Sanderson SO, Kamath PS, Ehman RL (2008) Magnetic resonance imaging of hepatic fibrosis: emerging clinical applications. Hepatology 47:332–342PubMedCrossRef Talwalkar JA, Yin M, Fidler JL, Sanderson SO, Kamath PS, Ehman RL (2008) Magnetic resonance imaging of hepatic fibrosis: emerging clinical applications. Hepatology 47:332–342PubMedCrossRef
18.
go back to reference Chan JH, Tsui EY, Luk SH et al (2001) Diffusion-weighted MR imaging of the liver: distinguishing hepatic abscess from cystic or necrotic tumor. Abdom Imaging 26:161–165PubMedCrossRef Chan JH, Tsui EY, Luk SH et al (2001) Diffusion-weighted MR imaging of the liver: distinguishing hepatic abscess from cystic or necrotic tumor. Abdom Imaging 26:161–165PubMedCrossRef
19.
go back to reference Mürtz P, Flacke S, Träber F, van den Brink JS, Gieseke J, Schild HH (2002) Abdomen: diffusion-weighted MR imaging with pulse-triggered single-shot sequences. Radiology 224:258–264PubMedCrossRef Mürtz P, Flacke S, Träber F, van den Brink JS, Gieseke J, Schild HH (2002) Abdomen: diffusion-weighted MR imaging with pulse-triggered single-shot sequences. Radiology 224:258–264PubMedCrossRef
20.
go back to reference Boulanger Y, Amara M, Lepanto L et al (2003) Diffusion-weighted MR imaging of the liver of hepatitis C patients. NMR Biomed 16:132–136PubMedCrossRef Boulanger Y, Amara M, Lepanto L et al (2003) Diffusion-weighted MR imaging of the liver of hepatitis C patients. NMR Biomed 16:132–136PubMedCrossRef
21.
go back to reference Bruegel M, Holzapfel K, Gaa J et al (2008) Characterization of focal liver lesions by ADC measurements using a respiratory triggered diffusion-weighted single-shot echo-planar MR imaging technique. Eur Radiol 18:477–485PubMedCrossRef Bruegel M, Holzapfel K, Gaa J et al (2008) Characterization of focal liver lesions by ADC measurements using a respiratory triggered diffusion-weighted single-shot echo-planar MR imaging technique. Eur Radiol 18:477–485PubMedCrossRef
22.
go back to reference Perman WH, Balci NC, Akduman I, Kuntz E (2009) Magnetic resonance measurement of diffusion in the abdomen. Top Magn Reson Imaging 20:99–104PubMedCrossRef Perman WH, Balci NC, Akduman I, Kuntz E (2009) Magnetic resonance measurement of diffusion in the abdomen. Top Magn Reson Imaging 20:99–104PubMedCrossRef
23.
go back to reference Sandrasegaran K, Akisik FM, Lin C et al (2009) Value of diffusion-weighted MRI for assessing liver fibrosis and cirrhosis. AJR Am J Roentgenol 193:1556–1560PubMedCrossRef Sandrasegaran K, Akisik FM, Lin C et al (2009) Value of diffusion-weighted MRI for assessing liver fibrosis and cirrhosis. AJR Am J Roentgenol 193:1556–1560PubMedCrossRef
24.
go back to reference Dale BM, Braithwaite AC, Boll DT, Merkle EM (2010) Field strength and diffusion encoding technique affect the apparent diffusion coefficient measurements in diffusion-weighted imaging of the abdomen. Invest Radiol 45:104–108PubMedCrossRef Dale BM, Braithwaite AC, Boll DT, Merkle EM (2010) Field strength and diffusion encoding technique affect the apparent diffusion coefficient measurements in diffusion-weighted imaging of the abdomen. Invest Radiol 45:104–108PubMedCrossRef
25.
go back to reference Nasu K, Kuroki Y, Sekiguchi R, Kazama T, Nakajima H (2006) Measurement of the apparent diffusion coefficient in the liver: is it a reliable index for hepatic disease diagnosis? Radiat Med 24:438–444PubMedCrossRef Nasu K, Kuroki Y, Sekiguchi R, Kazama T, Nakajima H (2006) Measurement of the apparent diffusion coefficient in the liver: is it a reliable index for hepatic disease diagnosis? Radiat Med 24:438–444PubMedCrossRef
26.
go back to reference Kiliçkesmez O, Yirik G, Bayramoğlu S, Cimilli T, Aydin S (2008) Non-breath-hold high b-value diffusion-weighted MRI with parallel imaging technique: apparent diffusion coefficient determination in normal abdominal organs. Diagn Interv Radiol 14:83–87PubMed Kiliçkesmez O, Yirik G, Bayramoğlu S, Cimilli T, Aydin S (2008) Non-breath-hold high b-value diffusion-weighted MRI with parallel imaging technique: apparent diffusion coefficient determination in normal abdominal organs. Diagn Interv Radiol 14:83–87PubMed
28.
go back to reference Lagarias JC, Reeds JA, Wright MH, Wright PE (1998) Convergence properties of the Nelder-Mead Simplex method in low dimensions. SIAM J Optim 9:112–147CrossRef Lagarias JC, Reeds JA, Wright MH, Wright PE (1998) Convergence properties of the Nelder-Mead Simplex method in low dimensions. SIAM J Optim 9:112–147CrossRef
29.
go back to reference Hampel FR (1974) The influence curve and its role in robust estimation. J Am Statist Assoc 69:383–393CrossRef Hampel FR (1974) The influence curve and its role in robust estimation. J Am Statist Assoc 69:383–393CrossRef
30.
go back to reference Yoshikawa T, Kawamitsu H, Mitchell DG et al (2006) ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol 187:1521–1530PubMedCrossRef Yoshikawa T, Kawamitsu H, Mitchell DG et al (2006) ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol 187:1521–1530PubMedCrossRef
31.
go back to reference Guiu B, Cercueil JP (2011) Liver diffusion-weighted MR imaging: the tower of Babel? Eur Radiol 21:463–467PubMedCrossRef Guiu B, Cercueil JP (2011) Liver diffusion-weighted MR imaging: the tower of Babel? Eur Radiol 21:463–467PubMedCrossRef
32.
go back to reference Chow LC, Bammer R, Moseley ME, Sommer FG (2003) Single breath-hold diffusion-weighted imaging of the abdomen. J Magn Reson Imaging 18:377–382PubMedCrossRef Chow LC, Bammer R, Moseley ME, Sommer FG (2003) Single breath-hold diffusion-weighted imaging of the abdomen. J Magn Reson Imaging 18:377–382PubMedCrossRef
33.
go back to reference Baron P, Dorrius MD, Kappert P, Oudkerk M, Sijens PE (2010) Diffusion-weighted imaging of normal fibroglandular breast tissue: influence of microperfusion and fat suppression technique on the apparent diffusion coefficient. NMR Biomed 23:399–405PubMed Baron P, Dorrius MD, Kappert P, Oudkerk M, Sijens PE (2010) Diffusion-weighted imaging of normal fibroglandular breast tissue: influence of microperfusion and fat suppression technique on the apparent diffusion coefficient. NMR Biomed 23:399–405PubMed
34.
go back to reference Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125PubMed Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125PubMed
35.
go back to reference Zhang JL, Sigmund EE, Chandarana H et al (2010) Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. Radiology 254:783–792PubMedCrossRef Zhang JL, Sigmund EE, Chandarana H et al (2010) Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. Radiology 254:783–792PubMedCrossRef
36.
go back to reference Koh DM, Scurr E, Collins DJ et al (2006) Colorectal hepatic metastases: quantitative measurements using single-shot echo-planar diffusion-weighted MR imaging. Eur Radiol 16:1898–1905PubMedCrossRef Koh DM, Scurr E, Collins DJ et al (2006) Colorectal hepatic metastases: quantitative measurements using single-shot echo-planar diffusion-weighted MR imaging. Eur Radiol 16:1898–1905PubMedCrossRef
37.
go back to reference Kandpal H, Sharma R, Madhusudhan KS, Kapoor KS (2009) Respiratory-triggered versus breath-hold diffusion-weighted MRI of liver lesions: comparison of image quality and apparent diffusion coefficient values. AJR Am J Roentgenol 192:915–922PubMedCrossRef Kandpal H, Sharma R, Madhusudhan KS, Kapoor KS (2009) Respiratory-triggered versus breath-hold diffusion-weighted MRI of liver lesions: comparison of image quality and apparent diffusion coefficient values. AJR Am J Roentgenol 192:915–922PubMedCrossRef
38.
go back to reference Kwee TC, Takahara T, Niwa T et al (2009) Influence of cardiac motion on diffusion-weighted magnetic resonance imaging of the liver. MAGMA 22:319–325PubMedCrossRef Kwee TC, Takahara T, Niwa T et al (2009) Influence of cardiac motion on diffusion-weighted magnetic resonance imaging of the liver. MAGMA 22:319–325PubMedCrossRef
39.
go back to reference Nasu K, Kuroki Y, Fujii H, Minami M (2007) Hepatic pseudo-anisotropy: a specific artifact in hepatic diffusion-weighted images obtained with respiratory triggering. MAGMA 20:205–211PubMedCrossRef Nasu K, Kuroki Y, Fujii H, Minami M (2007) Hepatic pseudo-anisotropy: a specific artifact in hepatic diffusion-weighted images obtained with respiratory triggering. MAGMA 20:205–211PubMedCrossRef
40.
go back to reference Su BY, Jin ZY, Liu W et al (2010) Features of eight segments of liver perfusion with the second generation dual-source computed tomography. Acta Acad Med Sin 32:655–658 Su BY, Jin ZY, Liu W et al (2010) Features of eight segments of liver perfusion with the second generation dual-source computed tomography. Acta Acad Med Sin 32:655–658
41.
go back to reference Scharf J, Kemmling A, Hess T, Mehrabi A, Kauffmann G, Groden C, Brix G (2007) Assessment of hepatic perfusion in transplanted livers by pharmacokinetic analysis of dynamic magnetic resonance measurements. Invest Radiol 42:224–229PubMedCrossRef Scharf J, Kemmling A, Hess T, Mehrabi A, Kauffmann G, Groden C, Brix G (2007) Assessment of hepatic perfusion in transplanted livers by pharmacokinetic analysis of dynamic magnetic resonance measurements. Invest Radiol 42:224–229PubMedCrossRef
42.
go back to reference Tutcu S, Serter S, Kaya Y, Kara E, Neşe N, Pekindil G, Coşkun T (2010) Hepatic perfusion changes in an experimental model of acute pancreatitis: evaluation by perfusion CT. Eur J Radiol 75:203–206PubMedCrossRef Tutcu S, Serter S, Kaya Y, Kara E, Neşe N, Pekindil G, Coşkun T (2010) Hepatic perfusion changes in an experimental model of acute pancreatitis: evaluation by perfusion CT. Eur J Radiol 75:203–206PubMedCrossRef
43.
go back to reference Schmucker DL (2005) Age-related changes in liver structure and function: implications for disease? Exp Gerontol 40:650–659PubMedCrossRef Schmucker DL (2005) Age-related changes in liver structure and function: implications for disease? Exp Gerontol 40:650–659PubMedCrossRef
44.
45.
go back to reference Pasquinelli F, Belli G, Mazzoni LN, Grazioli L, Colagrande S (2011) Magnetic resonance diffusion-weighted imaging: quantitative evaluation of age-related changes in healthy liver parenchyma. Magn Reson Imaging 29:805–812PubMedCrossRef Pasquinelli F, Belli G, Mazzoni LN, Grazioli L, Colagrande S (2011) Magnetic resonance diffusion-weighted imaging: quantitative evaluation of age-related changes in healthy liver parenchyma. Magn Reson Imaging 29:805–812PubMedCrossRef
46.
go back to reference Gourtsoyianni S, Papanikolaou N, Yarmenitis S, Maris T, Karantanas A, Gourtsoyiannis N (2008) Respiratory gated diffusion-weighted imaging of the liver: value of apparent diffusion coefficient measurements in the differentiation between most commonly encountered benign and malignant focal liver lesions. Eur Radiol 18:486–492PubMedCrossRef Gourtsoyianni S, Papanikolaou N, Yarmenitis S, Maris T, Karantanas A, Gourtsoyiannis N (2008) Respiratory gated diffusion-weighted imaging of the liver: value of apparent diffusion coefficient measurements in the differentiation between most commonly encountered benign and malignant focal liver lesions. Eur Radiol 18:486–492PubMedCrossRef
Metadata
Title
Effects of microperfusion in hepatic diffusion weighted imaging
Authors
Hildebrand Dijkstra
Paul Baron
Peter Kappert
Matthijs Oudkerk
Paul E. Sijens
Publication date
01-04-2012
Publisher
Springer-Verlag
Published in
European Radiology / Issue 4/2012
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-011-2313-1

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