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Published in: Clinical & Experimental Metastasis 2/2016

01-02-2016 | Research Paper

Free-breathing 3D diffusion MRI for high-resolution hepatic metastasis characterization in small animals

Authors: Emeline J. Ribot, Aurélien J. Trotier, Charles R. Castets, Benjamin Dallaudière, Eric Thiaudière, Jean-Michel Franconi, Sylvain Miraux

Published in: Clinical & Experimental Metastasis | Issue 2/2016

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Abstract

The goal of this study was to develop a 3D diffusion weighted sequence for free breathing liver imaging in small animals at high magnetic field. Hepatic metastases were detected and the apparent diffusion coefficients (ADC) were measured. A 3D SE-EPI sequence was developed by (i) inserting a water-selective excitation radiofrequency pulse to suppress adipose tissue signal and (ii) bipolar diffusion gradients to decrease the sensitivity to respiration motion. Mice with hepatic metastases were imaged at 7T by applying b values from 200 to 1100 s/mm2. 3D images with high spatial resolution (182 × 156 × 125 µm) were obtained in only 8 min 32 s. The modified DW-SE-EPI sequence allowed to obtain 3D abdominal images of healthy mice with fat SNR 2.5 times lower than without any fat suppression method and sharpness 2.8 times higher than on respiration-triggered images. Due to the high spatial resolution, the core and the periphery of disseminated hepatic metastases were differentiated at high b-values only, demonstrating the presence of edema and proliferating cells (with ADC of 2.65 × 10−3 and 1.55 × 10−3 mm2/s, respectively). Furthermore, these metastases were accurately distinguished from proliferating ones within the same animal at high b-values (mean ADC of 0.38 × 10−3 mm2/s). Metastases of less than 1.7 mm3 diameter were detected. The new 3D SE-EPI sequence enabled to obtain diffusion information within liver metastases. In addition of intra-metastasis heterogeneity, differences in diffusion were measured between metastases within an animal. This sequence could be used to obtain diffusion information at high magnetic field.
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Literature
1.
go back to reference Hompland T, Ellingsen C, Galappathi K, Rofstad EK (2014) DW-MRI in assessment of the hypoxic fraction, interstitial fluid pressure, and metastatic propensity of melanoma xenografts. BMC Cancer 14:92PubMedCentralCrossRefPubMed Hompland T, Ellingsen C, Galappathi K, Rofstad EK (2014) DW-MRI in assessment of the hypoxic fraction, interstitial fluid pressure, and metastatic propensity of melanoma xenografts. BMC Cancer 14:92PubMedCentralCrossRefPubMed
2.
go back to reference Panagiotaki E, Walker-Samuel S, Siow B, Johnson SP, Rajkumar V, Pedley RB, Lythgoe MF, Alexander DC (2014) Noninvasive quantification of solid tumor microstructure using VERDICT MRI. Cancer Res 74(7):1902–1912CrossRefPubMed Panagiotaki E, Walker-Samuel S, Siow B, Johnson SP, Rajkumar V, Pedley RB, Lythgoe MF, Alexander DC (2014) Noninvasive quantification of solid tumor microstructure using VERDICT MRI. Cancer Res 74(7):1902–1912CrossRefPubMed
3.
go back to reference Li X, Jiang H, Niu J, Zheng Y (2014) Correlation of ADC value with pathologic indexes in colorectal tumor homografts in Balb/c mouse. Chin J Cancer Res 26(4):444–450PubMedCentralPubMed Li X, Jiang H, Niu J, Zheng Y (2014) Correlation of ADC value with pathologic indexes in colorectal tumor homografts in Balb/c mouse. Chin J Cancer Res 26(4):444–450PubMedCentralPubMed
4.
go back to reference Yun BL, Cho N, Li M, Jang MH, Park SY, Kang HC, Kim B, Song IC, Moon WK (2014) Intratumoral heterogeneity of breast cancer xenograft models: texture analysis of diffusion-weighted mr imaging. Korean J Radiol 15(5):591–604PubMedCentralCrossRefPubMed Yun BL, Cho N, Li M, Jang MH, Park SY, Kang HC, Kim B, Song IC, Moon WK (2014) Intratumoral heterogeneity of breast cancer xenograft models: texture analysis of diffusion-weighted mr imaging. Korean J Radiol 15(5):591–604PubMedCentralCrossRefPubMed
5.
go back to reference Squillaci E, Bolacchi F, Altobelli S, Franceschini L, Bergamini A, Cantonetti M, Simonetti G (2014) Pre-treatment staging of multiple myeloma patients: comparison of whole-body diffusion weighted imaging with whole-body T1-weighted contrast-enhanced imaging. Acta Radiol. doi:10.1177/0284185114538792 PubMed Squillaci E, Bolacchi F, Altobelli S, Franceschini L, Bergamini A, Cantonetti M, Simonetti G (2014) Pre-treatment staging of multiple myeloma patients: comparison of whole-body diffusion weighted imaging with whole-body T1-weighted contrast-enhanced imaging. Acta Radiol. doi:10.​1177/​0284185114538792​ PubMed
6.
go back to reference Wang HJ, Pui MH, Guo Y, Li SR, Liu MJ, Guan J, Zhang XL, Feng Y (2014) Value of normalized apparent diffusion coefficient for estimating histological grade of vesical urothelial carcinoma. Clin Radiol 69:727–731CrossRefPubMed Wang HJ, Pui MH, Guo Y, Li SR, Liu MJ, Guan J, Zhang XL, Feng Y (2014) Value of normalized apparent diffusion coefficient for estimating histological grade of vesical urothelial carcinoma. Clin Radiol 69:727–731CrossRefPubMed
7.
go back to reference Roth Y, Tichler T, Kostenich G, Ruiz-Cabello J, Maier SE, Cohen JS, Orenstein A, Mardor Y (2004) High-b-value diffusion-weighted mr imaging for pretreatment prediction and early monitoring of tumor response to therapy in mice. Radiol 232:685–692CrossRef Roth Y, Tichler T, Kostenich G, Ruiz-Cabello J, Maier SE, Cohen JS, Orenstein A, Mardor Y (2004) High-b-value diffusion-weighted mr imaging for pretreatment prediction and early monitoring of tumor response to therapy in mice. Radiol 232:685–692CrossRef
8.
go back to reference Zhao YL, Guo QQ, Yang GG, Wang QD (2014) Early changes in apparent diffusion coefficient as an indicator of response to sorafenib in hepatocellular carcinoma. J Zhejiang University-Science B (Biomed Biotechnol) 15(8):713–719CrossRef Zhao YL, Guo QQ, Yang GG, Wang QD (2014) Early changes in apparent diffusion coefficient as an indicator of response to sorafenib in hepatocellular carcinoma. J Zhejiang University-Science B (Biomed Biotechnol) 15(8):713–719CrossRef
9.
go back to reference Benndorf M, Schelhorn J, Dietzel M, Kaiser WA, Baltzer PAT (2012) Diffusion weighted imaging of liver lesions suspect for metastases: Apparent diffusion coefficient (ADC) values and lesion contrast are independent from Gd-EOB-DTPA administration. Eur J Radiol 81:e849–e853CrossRefPubMed Benndorf M, Schelhorn J, Dietzel M, Kaiser WA, Baltzer PAT (2012) Diffusion weighted imaging of liver lesions suspect for metastases: Apparent diffusion coefficient (ADC) values and lesion contrast are independent from Gd-EOB-DTPA administration. Eur J Radiol 81:e849–e853CrossRefPubMed
10.
11.
go back to reference Van de Looij Y, Mauconduit F, Beaumont M, Valable S, Farion R, Francony G, Payen JF, Lahrech H (2011) Diffusion tensor imaging of diffuse axonal injury in a rat brain trauma model. NMR Biomed 25:93–103CrossRefPubMed Van de Looij Y, Mauconduit F, Beaumont M, Valable S, Farion R, Francony G, Payen JF, Lahrech H (2011) Diffusion tensor imaging of diffuse axonal injury in a rat brain trauma model. NMR Biomed 25:93–103CrossRefPubMed
12.
go back to reference Xue R, Sawada M, Goto S, Hurn PD, Traystman RJ, Van Zijl PCM, Mori S (2001) Rapid three-dimensional diffusion MRI facilitates the study of acute stroke in mice. Magn Reson Med 46:183–188CrossRefPubMed Xue R, Sawada M, Goto S, Hurn PD, Traystman RJ, Van Zijl PCM, Mori S (2001) Rapid three-dimensional diffusion MRI facilitates the study of acute stroke in mice. Magn Reson Med 46:183–188CrossRefPubMed
13.
go back to reference Moffat BA, Chenevert TL, Meyer CR, Mckeevery PE, Hall DE, Hoff BA, Johnson TD, Rehemtulla A, Ross BD (2006) The functional diffusion map: an imaging biomarker for the early prediction of cancer treatment outcome. Neoplasia 8:259–267PubMedCentralCrossRefPubMed Moffat BA, Chenevert TL, Meyer CR, Mckeevery PE, Hall DE, Hoff BA, Johnson TD, Rehemtulla A, Ross BD (2006) The functional diffusion map: an imaging biomarker for the early prediction of cancer treatment outcome. Neoplasia 8:259–267PubMedCentralCrossRefPubMed
14.
go back to reference Harsan LA, Paul D, Schnell S, Kreher BW, Hennig J, Staiger JF, von Elverfeldt D (2010) In vivo diffusion tensor magnetic resonance y imaging and fiber tracking of the mouse brain. NMR Biomed 23:884–896CrossRefPubMed Harsan LA, Paul D, Schnell S, Kreher BW, Hennig J, Staiger JF, von Elverfeldt D (2010) In vivo diffusion tensor magnetic resonance y imaging and fiber tracking of the mouse brain. NMR Biomed 23:884–896CrossRefPubMed
15.
go back to reference Aggarwal M, Mori S, Shimogori T, Blackshaw S, Zhang J (2010) Three-dimensional diffusion tensor microimaging for anatomical characterization of the mouse brain. Magn Reson Med 64:249–261PubMedCentralCrossRefPubMed Aggarwal M, Mori S, Shimogori T, Blackshaw S, Zhang J (2010) Three-dimensional diffusion tensor microimaging for anatomical characterization of the mouse brain. Magn Reson Med 64:249–261PubMedCentralCrossRefPubMed
16.
go back to reference Padhani AR, Liu G, Mu-Koh D, Chenevert TL, Thoeny HC, Takahara T, Dzik-Jurasz A, Ross BD, Van Cauteren M, Collins D et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125PubMedCentralCrossRefPubMed Padhani AR, Liu G, Mu-Koh D, Chenevert TL, Thoeny HC, Takahara T, Dzik-Jurasz A, Ross BD, Van Cauteren M, Collins D et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125PubMedCentralCrossRefPubMed
17.
go back to reference Morris VL, MacDonald IC, Koop S, Schmidt EE, Chambers AF, Groom AC (1993) Early interactions of cancer cells with the microvasculature in mouse liver and muscle during hematogenous metastasis: videomicroscopic analysis. Clin Exp Metastasis 11:377–390CrossRefPubMed Morris VL, MacDonald IC, Koop S, Schmidt EE, Chambers AF, Groom AC (1993) Early interactions of cancer cells with the microvasculature in mouse liver and muscle during hematogenous metastasis: videomicroscopic analysis. Clin Exp Metastasis 11:377–390CrossRefPubMed
18.
go back to reference Kornaat PR, Doornbos J, van der Molen AJ, Kloppenburg M, Nelissen RG, Hogendoorn PCW, Bloem JL (2004) Magnetic resonance imaging of knee cartilage using a water selective balanced steady-state free precession sequence. J Magn Reson Imaging 20:850–856CrossRefPubMed Kornaat PR, Doornbos J, van der Molen AJ, Kloppenburg M, Nelissen RG, Hogendoorn PCW, Bloem JL (2004) Magnetic resonance imaging of knee cartilage using a water selective balanced steady-state free precession sequence. J Magn Reson Imaging 20:850–856CrossRefPubMed
19.
go back to reference Gamper U, Boesiger P, Kozerke S (2007) Diffusion imaging of the in vivo heart using spin echoes-considerations on bulk motion sensitivity. Magn Reson Med 57:331–337CrossRefPubMed Gamper U, Boesiger P, Kozerke S (2007) Diffusion imaging of the in vivo heart using spin echoes-considerations on bulk motion sensitivity. Magn Reson Med 57:331–337CrossRefPubMed
20.
go back to reference Koh DM, Collins DJ (2007) Diffusion-weighted MRI in the body: applications and challenges in oncology. Am J Roentgenol 188:1622–1635CrossRef Koh DM, Collins DJ (2007) Diffusion-weighted MRI in the body: applications and challenges in oncology. Am J Roentgenol 188:1622–1635CrossRef
22.
go back to reference Alexander AL, Tsuruda JS, Parker DL (1997) Elimination of Eddy current artifacts in diffusion-weighted echo-planar images: the use of bipolar gradients. Magn Reson Med 38:1016–1021CrossRefPubMed Alexander AL, Tsuruda JS, Parker DL (1997) Elimination of Eddy current artifacts in diffusion-weighted echo-planar images: the use of bipolar gradients. Magn Reson Med 38:1016–1021CrossRefPubMed
23.
go back to reference Buonocore MH, Zhu DC (2001) Image-based ghost correction for interleaved EPI. Magn Reson Med 45:96–108CrossRefPubMed Buonocore MH, Zhu DC (2001) Image-based ghost correction for interleaved EPI. Magn Reson Med 45:96–108CrossRefPubMed
24.
go back to reference Larson AC, Kellman P, Arai A, Hirsch GA, McVeigh E, Li D, Simonetti OP (2005) Preliminary investigation of respiratory self-gating for free-breathing segmented cine MRI. Magn Reson Med 53:159–168PubMedCentralCrossRefPubMed Larson AC, Kellman P, Arai A, Hirsch GA, McVeigh E, Li D, Simonetti OP (2005) Preliminary investigation of respiratory self-gating for free-breathing segmented cine MRI. Magn Reson Med 53:159–168PubMedCentralCrossRefPubMed
25.
go back to reference Ribot EJ, Duriez TJ, Trotier AJ, Thiaudiere E, Franconi JM, Miraux S (2014) Self-gated bSSFP sequences to detect iron-labeled cancer cells and/or metastases in vivo in mouse liver at 7 Tesla. J Magn Reson Imaging. doi:10.1002/jmri.24688 Ribot EJ, Duriez TJ, Trotier AJ, Thiaudiere E, Franconi JM, Miraux S (2014) Self-gated bSSFP sequences to detect iron-labeled cancer cells and/or metastases in vivo in mouse liver at 7 Tesla. J Magn Reson Imaging. doi:10.​1002/​jmri.​24688
26.
go back to reference Yuan J, Madore B, Panych LP (2011) Fat–water selective excitation in balanced steady-state free precession using short spatial–spectral RF pulses. J Magn Reson 208:219–224PubMedCentralCrossRefPubMed Yuan J, Madore B, Panych LP (2011) Fat–water selective excitation in balanced steady-state free precession using short spatial–spectral RF pulses. J Magn Reson 208:219–224PubMedCentralCrossRefPubMed
27.
go back to reference Zhou IY, Gao DS, Chow AM, Fan S, Cheung MM, Ling C, Liu X, Cao P, Guo H, Man K et al (2014) Effect of diffusion time on liver DWI: an experimental study of normal and fibrotic livers. Magn Reson Med 72:1389–1396CrossRefPubMed Zhou IY, Gao DS, Chow AM, Fan S, Cheung MM, Ling C, Liu X, Cao P, Guo H, Man K et al (2014) Effect of diffusion time on liver DWI: an experimental study of normal and fibrotic livers. Magn Reson Med 72:1389–1396CrossRefPubMed
28.
go back to reference Chow AM, Gao DS, Fan SJ, Qiao Z, Lee FY, Yang J, Man K, Wu EX (2012) Liver fibrosis: an intravoxel incoherent motion (IVIM) study. J Magn Reson Imaging 36:159–167CrossRefPubMed Chow AM, Gao DS, Fan SJ, Qiao Z, Lee FY, Yang J, Man K, Wu EX (2012) Liver fibrosis: an intravoxel incoherent motion (IVIM) study. J Magn Reson Imaging 36:159–167CrossRefPubMed
29.
go back to reference Lee Y, Kim H (2014) Assessment of diffusion tensor MR imaging (DTI) in liver fibrosis with minimal confounding effect of hepatic steatosis. Magn Reson Med. doi:10.1002/mrm.25253 Lee Y, Kim H (2014) Assessment of diffusion tensor MR imaging (DTI) in liver fibrosis with minimal confounding effect of hepatic steatosis. Magn Reson Med. doi:10.​1002/​mrm.​25253
30.
go back to reference Lee HJ, Luci JJ, Tantawy MN, Lee H, Nam KT, Peterson TE, Price RR (2013) Detecting peritoneal dissemination of ovarian cancer in mice by DWIBS. Magn Reson Imaging 31:227–234PubMedCentralCrossRefPubMed Lee HJ, Luci JJ, Tantawy MN, Lee H, Nam KT, Peterson TE, Price RR (2013) Detecting peritoneal dissemination of ovarian cancer in mice by DWIBS. Magn Reson Imaging 31:227–234PubMedCentralCrossRefPubMed
31.
go back to reference Sun J, Zhang XP, Li XT, Tang L, Cui Y, Zhang XY, Sun YS (2014) Applicable apparent diffusion coefficient of an orthotopic mouse model of gastric cancer by improved clinical MRI diffusion weighted imaging. Sci Rep 4:6072PubMedCentralPubMed Sun J, Zhang XP, Li XT, Tang L, Cui Y, Zhang XY, Sun YS (2014) Applicable apparent diffusion coefficient of an orthotopic mouse model of gastric cancer by improved clinical MRI diffusion weighted imaging. Sci Rep 4:6072PubMedCentralPubMed
32.
go back to reference Hennel F (1998) Image-based reduction of artifacts in multishot echo-planar imaging. J Magn Reson 134:206–213CrossRefPubMed Hennel F (1998) Image-based reduction of artifacts in multishot echo-planar imaging. J Magn Reson 134:206–213CrossRefPubMed
33.
go back to reference Dou J, Reese TG, Tseng WYI, Wedeen VJ (2002) Cardiac diffusion MRI without motion effects. Magn Reson Med 48:105–114CrossRefPubMed Dou J, Reese TG, Tseng WYI, Wedeen VJ (2002) Cardiac diffusion MRI without motion effects. Magn Reson Med 48:105–114CrossRefPubMed
34.
go back to reference Anderson SW, Soto JA, Milch HN, Ozonoff A, O’Brien M, Hamilton JA, Jara HJ (2011) Effect of disease progression on liver apparent diffusion coefficient values in a Murine model of NASH at 11.7 Tesla MRI. J Magn Reson Imaging 33:882–888CrossRefPubMed Anderson SW, Soto JA, Milch HN, Ozonoff A, O’Brien M, Hamilton JA, Jara HJ (2011) Effect of disease progression on liver apparent diffusion coefficient values in a Murine model of NASH at 11.7 Tesla MRI. J Magn Reson Imaging 33:882–888CrossRefPubMed
35.
go back to reference Wagner M, Maggiori L, Ronot M, Paradis V, Vilgrain V, Panis Y, Van Beers BE (2013) Diffusion-weighted and T2-weighted MR imaging for colorectal liver metastases detection in a rat model at 7 T: a comparative study using histological examination as reference. Eur Radiol 23:2156–2164CrossRefPubMed Wagner M, Maggiori L, Ronot M, Paradis V, Vilgrain V, Panis Y, Van Beers BE (2013) Diffusion-weighted and T2-weighted MR imaging for colorectal liver metastases detection in a rat model at 7 T: a comparative study using histological examination as reference. Eur Radiol 23:2156–2164CrossRefPubMed
36.
go back to reference Perera M, Ribot EJ, Percy DB, McFadden C, Simedrea C, Palmieri D, Chambers AF, Foster PJ (2012) In vivo magnetic resonance imaging for investigating the development and distribution of experimental brain metastases due to breast cancer. Trans Oncol 5(3):217–225CrossRef Perera M, Ribot EJ, Percy DB, McFadden C, Simedrea C, Palmieri D, Chambers AF, Foster PJ (2012) In vivo magnetic resonance imaging for investigating the development and distribution of experimental brain metastases due to breast cancer. Trans Oncol 5(3):217–225CrossRef
37.
go back to reference Radermacher KA, Magat J, Bouzin C, Laurent S, Dresselaers T, Himmelreich U, Boutry S, Mahieu I, Vander Elst L, Feron O et al (2012) Multimodal assessment of early tumor response to chemotherapy: comparison between diffusion-weighted MRI, 1H-MR spectroscopy of choline and USPIO particles targeted at cell death. NMR Biomed 25:514–522CrossRefPubMed Radermacher KA, Magat J, Bouzin C, Laurent S, Dresselaers T, Himmelreich U, Boutry S, Mahieu I, Vander Elst L, Feron O et al (2012) Multimodal assessment of early tumor response to chemotherapy: comparison between diffusion-weighted MRI, 1H-MR spectroscopy of choline and USPIO particles targeted at cell death. NMR Biomed 25:514–522CrossRefPubMed
38.
go back to reference Budde MD, Gold E, Jordan EK, Frank JA (2012) Differential microstructure and physiology of brain and bone metastases in a rat breast cancer model by diffusion and dynamic contrast enhanced MRI. Clin Exp Metastasis 29:51–62PubMedCentralCrossRefPubMed Budde MD, Gold E, Jordan EK, Frank JA (2012) Differential microstructure and physiology of brain and bone metastases in a rat breast cancer model by diffusion and dynamic contrast enhanced MRI. Clin Exp Metastasis 29:51–62PubMedCentralCrossRefPubMed
39.
go back to reference Sun XJ, Quan XY, Huang FH, Xu YK (2005) Quantitative evaluation of diffusion-weighted magnetic resonance imaging of focal hepatic lesions. World J Gastroenterol 11(41):6535–6537PubMedCentralCrossRefPubMed Sun XJ, Quan XY, Huang FH, Xu YK (2005) Quantitative evaluation of diffusion-weighted magnetic resonance imaging of focal hepatic lesions. World J Gastroenterol 11(41):6535–6537PubMedCentralCrossRefPubMed
40.
go back to reference Speck O, Stadler J, Zaitsev M (2008) High resolution single-shot EPI at 7T. Magn Reson Mater Phy 21:73–86CrossRef Speck O, Stadler J, Zaitsev M (2008) High resolution single-shot EPI at 7T. Magn Reson Mater Phy 21:73–86CrossRef
41.
go back to reference Freidlin RZ, Kakareka JW, Pohida TJ, Komlosh ME, Basser PJ (2012) A spin echo sequence with a single-sided bipolar diffusion gradient pulse to obtain snapshot diffusion weighted images in moving media. J Magn Reson 221:24–31PubMedCentralCrossRefPubMed Freidlin RZ, Kakareka JW, Pohida TJ, Komlosh ME, Basser PJ (2012) A spin echo sequence with a single-sided bipolar diffusion gradient pulse to obtain snapshot diffusion weighted images in moving media. J Magn Reson 221:24–31PubMedCentralCrossRefPubMed
Metadata
Title
Free-breathing 3D diffusion MRI for high-resolution hepatic metastasis characterization in small animals
Authors
Emeline J. Ribot
Aurélien J. Trotier
Charles R. Castets
Benjamin Dallaudière
Eric Thiaudière
Jean-Michel Franconi
Sylvain Miraux
Publication date
01-02-2016
Publisher
Springer Netherlands
Published in
Clinical & Experimental Metastasis / Issue 2/2016
Print ISSN: 0262-0898
Electronic ISSN: 1573-7276
DOI
https://doi.org/10.1007/s10585-015-9766-6

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