Journal Article
. 2013 Nov;40(4).
doi: 10.1002/jmri.24462.

Intravoxel incoherent motion diffusion-weighted MRI at 3.0 T differentiates malignant breast lesions from benign lesions and breast parenchyma

Louisa Bokacheva 1 Jennifer B Kaplan  Dilip D Giri  Sujata Patil  Merlin Gnanasigamani  C Gregory Nyman  Joseph O Deasy  Elizabeth A Morris  Sunitha B Thakur  
Affiliations
  • PMID: 24273096
  •     36 References
  •     36 citations

Abstract

Purpose: To study the differentiation of malignant breast lesions from benign lesions and fibroglandular tissue (FGT) using apparent diffusion coefficient (ADC) and intravoxel incoherent motion (IVIM) parameters.

Materials And Methods: This retrospective study included 26 malignant and 14 benign breast lesions in 35 patients who underwent diffusion-weighted MRI at 3.0T and nine b-values (0-1000 s/mm(2) ). ADC and IVIM parameters (perfusion fraction fp , pseudodiffusion coefficient Dp , and true diffusion coefficient Dd ) were determined in lesions and FGT. For comparison, IVIM was also measured in 16 high-risk normal patients. A predictive model was constructed using linear discriminant analysis. Lesion discrimination based on ADC and IVIM parameters was assessed using receiver operating characteristic (ROC) and area under the ROC curve (AUC).

Results: In FGT of normal subjects, fp was 1.1 ± 1.1%. In malignant lesions, fp (6.4 ± 3.1%) was significantly higher than in benign lesions (3.1 ± 3.3%, P = 0.0025) or FGT (1.5 ± 1.2%, P < 0.001), and Dd ((1.29 ± 0.28) × 10(-3) mm(2) /s) was lower than in benign lesions ((1.56 ± 0.28) × 10(-3) mm(2) /s, P = 0.011) or FGT ((1.86 ± 0.34) × 10(-3) mm(2) /s, P < 0.001). A combination of Dd and fp provided higher AUC for discrimination between malignant and benign lesions (0.84) or FGT (0.97) than ADC (0.72 and 0.86, respectively).

Conclusion: The IVIM parameters provide accurate identification of malignant lesions.

Keywords: benign breast lesions; breast cancer; diffusion-weighted imaging; intravoxel incoherent motion.

Breast lesions: correlation of contrast medium enhancement patterns on MR images with histopathologic findings and tumor angiogenesis.
L D Buadu, J Murakami, +6 authors, S Ohno.
Radiology, 1996 Sep 01; 200(3). PMID: 8756909
Highly Cited.
Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging.
I Yamada, W Aung, +2 authors, H Shibuya.
Radiology, 1999 Apr 20; 210(3). PMID: 10207458
Highly Cited.
ADC mapping of benign and malignant breast tumors.
Reiko Woodhams, Keiji Matsunaga, +6 authors, Kazushige Hayakawa.
Magn Reson Med Sci, 2005 Aug 30; 4(1). PMID: 16127252
Quantitative diffusion imaging in breast cancer: a clinical prospective study.
Erika Rubesova, Anne-Sophie Grell, +3 authors, Marc Lemort.
J Magn Reson Imaging, 2006 Jun 21; 24(2). PMID: 16786565
Functional evaluation of transplanted kidneys with diffusion-weighted and BOLD MR imaging: initial experience.
Harriet C Thoeny, Dominik Zumstein, +7 authors, Peter Vermathen.
Radiology, 2006 Nov 23; 241(3). PMID: 17114628
DCEMRI of breast lesions: is kinetic analysis equally effective for both mass and nonmass-like enhancement?
Sanaz A Jansen, Xiaobing Fan, +4 authors, Gillian M Newstead.
Med Phys, 2008 Aug 14; 35(7). PMID: 18697535    Free PMC article.
Liver cirrhosis: intravoxel incoherent motion MR imaging--pilot study.
Alain Luciani, Alexandre Vignaud, +7 authors, Alain Rahmouni.
Radiology, 2008 Nov 18; 249(3). PMID: 19011186
Highly Cited.
Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations.
Anwar R Padhani, Guoying Liu, +11 authors, Peter L Choyke.
Neoplasia, 2009 Feb 04; 11(2). PMID: 19186405    Free PMC article.
Highly Cited.
Diffusion-weighted imaging of normal fibroglandular breast tissue: influence of microperfusion and fat suppression technique on the apparent diffusion coefficient.
Paul Baron, Monique D Dorrius, +2 authors, Paul E Sijens.
NMR Biomed, 2010 Feb 05; 23(4). PMID: 20131313
An in vivo verification of the intravoxel incoherent motion effect in diffusion-weighted imaging of the abdomen.
Andreas Lemke, Frederik B Laun, +2 authors, Lothar R Schad.
Magn Reson Med, 2010 Jul 29; 64(6). PMID: 20665824
Intravoxel incoherent motion imaging of tumor microenvironment in locally advanced breast cancer.
E E Sigmund, G Y Cho, +7 authors, L Moy.
Magn Reson Med, 2011 Feb 03; 65(5). PMID: 21287591    Free PMC article.
Toward an optimal distribution of b values for intravoxel incoherent motion imaging.
Andreas Lemke, Bram Stieltjes, Lothar R Schad, Frederik B Laun.
Magn Reson Imaging, 2011 May 10; 29(6). PMID: 21549538
Highly Cited.
Diffusion-weighted imaging of the breast: principles and clinical applications.
Reiko Woodhams, Saadallah Ramadan, +5 authors, Yusuke Inoue.
Radiographics, 2011 Jul 20; 31(4). PMID: 21768239
Optimization of b-value sampling for diffusion-weighted imaging of the kidney.
Jeff L Zhang, Eric E Sigmund, +4 authors, Vivian S Lee.
Magn Reson Med, 2011 Jun 28; 67(1). PMID: 21702062    Free PMC article.
Interstitial fluid pressure correlates with intravoxel incoherent motion imaging metrics in a mouse mammary carcinoma model.
Sungheon Kim, Lindsey Decarlo, +7 authors, Eric E Sigmund.
NMR Biomed, 2011 Nov 11; 25(5). PMID: 22072561    Free PMC article.
Salivary gland tumors: use of intravoxel incoherent motion MR imaging for assessment of diffusion and perfusion for the differentiation of benign from malignant tumors.
Misa Sumi, Marc Van Cauteren, +3 authors, Takashi Nakamura.
Radiology, 2012 Mar 27; 263(3). PMID: 22447854
Intravoxel incoherent motion and diffusion-tensor imaging in renal tissue under hydration and furosemide flow challenges.
Eric E Sigmund, Pierre-Hugues Vivier, +8 authors, Hersh Chandarana.
Radiology, 2012 Apr 24; 263(3). PMID: 22523327
Extension of the intravoxel incoherent motion model to non-gaussian diffusion in head and neck cancer.
Yonggang Lu, Jacobus F A Jansen, +3 authors, Amita Shukla-Dave.
J Magn Reson Imaging, 2012 Jul 25; 36(5). PMID: 22826198    Free PMC article.
Intravoxel incoherent motion MR imaging for prostate cancer: an evaluation of perfusion fraction and diffusion coefficient derived from different b-value combinations.
Yuxi Pang, Baris Turkbey, +6 authors, Peter L Choyke.
Magn Reson Med, 2012 Apr 11; 69(2). PMID: 22488794    Free PMC article.
On shimming approaches in 3T breast MRI.
Ileana Hancu, Ambey Govenkar, Robert E Lenkinski, Seung-Kyun Lee.
Magn Reson Med, 2012 May 05; 69(3). PMID: 22556115    Free PMC article.
In vivo intravoxel incoherent motion measurements in the human placenta using echo-planar imaging at 0.5 T.
R J Moore, B Issa, +7 authors, P A Gowland.
Magn Reson Med, 2000 Feb 19; 43(2). PMID: 10680695
Breast cancer: regional blood flow and blood volume measured with magnetic susceptibility-based MR imaging--initial results.
Jean-Paul Delille, Priscilla J Slanetz, +2 authors, Leoncio Garrido.
Radiology, 2002 May 09; 223(2). PMID: 11997568
In vivo diffusion-weighted MRI of the breast: potential for lesion characterization.
Shantanu Sinha, Flora Anne Lucas-Quesada, +2 authors, Lawrence W Bassett.
J Magn Reson Imaging, 2002 Jul 12; 15(6). PMID: 12112520
Differentiation of clinically benign and malignant breast lesions using diffusion-weighted imaging.
Yong Guo, You-Quan Cai, +5 authors, Jia-Hong Gao.
J Magn Reson Imaging, 2002 Aug 31; 16(2). PMID: 12203765
Highly Cited.
MRI of occult breast carcinoma in a high-risk population.
Elizabeth A Morris, Laura Liberman, +4 authors, D David Dershaw.
AJR Am J Roentgenol, 2003 Aug 23; 181(3). PMID: 12933450
Further observations on prognostic factors in cancer of the female breast.
S J Cutler, M M Black, +2 authors, C Freeman.
Cancer, 1969 Oct 01; 24(4). PMID: 4309690
MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders.
D Le Bihan, E Breton, +3 authors, M Laval-Jeantet.
Radiology, 1986 Nov 01; 161(2). PMID: 3763909
Highly Cited.
Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging.
D Le Bihan, E Breton, +3 authors, M Laval-Jeantet.
Radiology, 1988 Aug 01; 168(2). PMID: 3393671
Highly Cited.
Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up.
C W Elston, I O Ellis.
Histopathology, 1991 Nov 01; 19(5). PMID: 1757079
Highly Cited.
In vivo measurement of diffusion and pseudo-diffusion in skeletal muscle at rest and after exercise.
D Morvan.
Magn Reson Imaging, 1995 Jan 01; 13(2). PMID: 7739360
Diffusion-weighted magnetic resonance imaging of breast lesions: first experiences at 3 T.
Gladys G Lo, Victor Ai, +6 authors, Daisy Chien.
J Comput Assist Tomogr, 2009 Feb 04; 33(1). PMID: 19188787
Diffusion-weighted MR for differentiation of breast lesions at 3.0 T: how does selection of diffusion protocols affect diagnosis?
Wolfgang Bogner, Stephan Gruber, +6 authors, Siegfried Trattnig.
Radiology, 2009 Aug 26; 253(2). PMID: 19703869
Quantitative diffusion-weighted imaging as an adjunct to conventional breast MRI for improved positive predictive value.
Savannah C Partridge, Wendy B DeMartini, +3 authors, Constance D Lehman.
AJR Am J Roentgenol, 2009 Nov 26; 193(6). PMID: 19933670
Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification.
Jeff L Zhang, Eric E Sigmund, +5 authors, Vivian S Lee.
Radiology, 2010 Jan 22; 254(3). PMID: 20089719    Free PMC article.
Differentiation of pancreas carcinoma from healthy pancreatic tissue using multiple b-values: comparison of apparent diffusion coefficient and intravoxel incoherent motion derived parameters.
Andreas Lemke, Frederik B Laun, +5 authors, Bram Stieltjes.
Invest Radiol, 2009 Oct 20; 44(12). PMID: 19838121
Apparent diffusion coefficient values for discriminating benign and malignant breast MRI lesions: effects of lesion type and size.
Savannah C Partridge, Christiane D Mullins, +4 authors, Constance D Lehman.
AJR Am J Roentgenol, 2010 May 22; 194(6). PMID: 20489111
Comparison of fitting methods and b-value sampling strategies for intravoxel incoherent motion in breast cancer.
Gene Young Cho, Linda Moy, +7 authors, Eric E Sigmund.
Magn Reson Med, 2014 Oct 11; 74(4). PMID: 25302780    Free PMC article.
Decreases in molecular diffusion, perfusion fraction and perfusion-related diffusion in fibrotic livers: a prospective clinical intravoxel incoherent motion MR imaging study.
Pu-Xuan Lu, Hua Huang, +6 authors, Yì-Xiáng J Wáng.
PLoS One, 2014 Dec 02; 9(12). PMID: 25436458    Free PMC article.
Whole-body intravoxel incoherent motion imaging.
Lukas Filli, Moritz C Wurnig, +3 authors, Andreas Boss.
Eur Radiol, 2015 Jan 13; 25(7). PMID: 25576232
Intravoxel Incoherent Motion Diffusion-weighted Magnetic Resonance Imaging for Monitoring the Early Response to ZD6474 from Nasopharyngeal Carcinoma in Nude Mouse.
Yanfen Cui, Caiyuan Zhang, +5 authors, Dengbin Wang.
Sci Rep, 2015 Nov 18; 5. PMID: 26574153    Free PMC article.
Multiparametric MR Imaging of Breast Cancer.
Habib Rahbar, Savannah C Partridge.
Magn Reson Imaging Clin N Am, 2015 Nov 29; 24(1). PMID: 26613883    Free PMC article.
Review.
Evaluation of breast cancer using intravoxel incoherent motion (IVIM) histogram analysis: comparison with malignant status, histological subtype, and molecular prognostic factors.
Gene Young Cho, Linda Moy, +5 authors, Eric E Sigmund.
Eur Radiol, 2015 Nov 30; 26(8). PMID: 26615557    Free PMC article.
Intravoxel incoherent motion MR imaging for breast lesions: comparison and correlation with pharmacokinetic evaluation from dynamic contrast-enhanced MR imaging.
Chunling Liu, Kun Wang, +5 authors, Changhong Liang.
Eur Radiol, 2016 Feb 13; 26(11). PMID: 26863896
Intravoxel incoherent motion diffusion-weighted MR imaging of breast cancer: association with histopathological features and subtypes.
Yunju Kim, Kyounglan Ko, +4 authors, Boram Park.
Br J Radiol, 2016 May 21; 89(1063). PMID: 27197744    Free PMC article.
Diffusion-weighted imaging reflects variable cellularity and stromal density present in breast fibroadenomas.
Sana Parsian, Nadia V Giannakopoulos, +3 authors, Savannah C Partridge.
Clin Imaging, 2016 Jul 06; 40(5). PMID: 27379441    Free PMC article.
Quantitative apparent diffusion coefficient measurement obtained by 3.0Tesla MRI as a potential noninvasive marker of tumor aggressiveness in breast cancer.
Manuela Durando, Lucas Gennaro, +7 authors, Sunitha B Thakur.
Eur J Radiol, 2016 Aug 10; 85(9). PMID: 27501902    Free PMC article.
A comparison of fitting algorithms for diffusion-weighted MRI data analysis using an intravoxel incoherent motion model.
Roberta Fusco, Mario Sansone, Antonella Petrillo.
MAGMA, 2016 Sep 28; 30(2). PMID: 27670762
Diffusion-weighted breast MRI: Clinical applications and emerging techniques.
Savannah C Partridge, Noam Nissan, +2 authors, Eric E Sigmund.
J Magn Reson Imaging, 2016 Oct 01; 45(2). PMID: 27690173    Free PMC article.
Highly Cited. Review.
Statistical assessment of bi-exponential diffusion weighted imaging signal characteristics induced by intravoxel incoherent motion in malignant breast tumors.
Jing Yuan, Oi Lei Wong, +3 authors, Polly S Y Cheung.
Quant Imaging Med Surg, 2016 Oct 07; 6(4). PMID: 27709078    Free PMC article.
Voxelwise analysis of simultaneously acquired and spatially correlated 18 F-fluorodeoxyglucose (FDG)-PET and intravoxel incoherent motion metrics in breast cancer.
Jason Ostenson, Akshat C Pujara, +13 authors, Eric E Sigmund.
Magn Reson Med, 2016 Oct 26; 78(3). PMID: 27779790    Free PMC article.
The potential of multiparametric MRI of the breast.
Katja Pinker, Thomas H Helbich, Elizabeth A Morris.
Br J Radiol, 2016 Nov 03; 90(1069). PMID: 27805423    Free PMC article.
Review.
Microstructural models for diffusion MRI in breast cancer and surrounding stroma: an ex vivo study.
Colleen Bailey, Bernard Siow, +7 authors, David J Hawkes.
NMR Biomed, 2016 Dec 22; 30(2). PMID: 28000292    Free PMC article.
Intravoxel incoherent motion diffusion-weighted magnetic resonance imaging of focal vertebral bone marrow lesions: initial experience of the differentiation of nodular hyperplastic hematopoietic bone marrow from malignant lesions.
Sunghoon Park, Kyu-Sung Kwack, +3 authors, Jae Ho Kim.
Skeletal Radiol, 2017 Mar 08; 46(5). PMID: 28265697
Optimization of intra-voxel incoherent motion measurement in diffusion-weighted imaging of breast cancer.
Wenjing Chen, Juan Zhang, +2 authors, Jian-Ming Zhu.
J Appl Clin Med Phys, 2017 Mar 30; 18(3). PMID: 28349630    Free PMC article.
A preliminary exploration of the intravoxel incoherent motion applied in the preoperative evaluation of mediastinal lymph node metastasis of lung cancer.
Xin Ye, Shuo Chen, +6 authors, Hui Li.
J Thorac Dis, 2017 May 20; 9(4). PMID: 28523162    Free PMC article.
Intravoxel Incoherent Motion Diffusion for Identification of Breast Malignant and Benign Tumors Using Chemometrics.
Fengnong Chen, Pulan Chen, Hamed Hamid Muhammed, Juan Zhang.
Biomed Res Int, 2017 Jun 21; 2017. PMID: 28630864    Free PMC article.
Apparent diffusion coefficient in estrogen receptor-positive and lymph node-negative invasive breast cancers at 3.0T DW-MRI: A potential predictor for an oncotype Dx test recurrence score.
Sunitha B Thakur, Manuela Durando, +5 authors, Elizabeth A Morris.
J Magn Reson Imaging, 2017 Jun 24; 47(2). PMID: 28640531    Free PMC article.
Intravoxel incoherent motion (IVIM) histogram biomarkers for prediction of neoadjuvant treatment response in breast cancer patients.
Gene Y Cho, Lucas Gennaro, +8 authors, Sunitha B Thakur.
Eur J Radiol Open, 2017 Sep 01; 4. PMID: 28856177    Free PMC article.
DWI in the Assessment of Breast Lesions.
Savannah C Partridge, Nita Amornsiripanitch.
Top Magn Reson Imaging, 2017 Sep 30; 26(5). PMID: 28961569    Free PMC article.
Clinical role of breast MRI now and going forward.
D Leithner, G J Wengert, +4 authors, K Pinker.
Clin Radiol, 2017 Dec 13; 73(8). PMID: 29229179    Free PMC article.
Review.
Diffusion-Weighted Imaging With Apparent Diffusion Coefficient Mapping for Breast Cancer Detection as a Stand-Alone Parameter: Comparison With Dynamic Contrast-Enhanced and Multiparametric Magnetic Resonance Imaging.
Katja Pinker, Linda Moy, +8 authors, Thomas H Helbich.
Invest Radiol, 2018 Apr 06; 53(10). PMID: 29620604    Free PMC article.
Intravoxel Incoherent Motion Diffusion-Weighted Imaging of Primary Rectal Carcinoma: Correlation with Histopathology.
Baolan Lu, Xinyue Yang, +3 authors, Shenping Yu.
Med Sci Monit, 2018 Apr 22; 24. PMID: 29679528    Free PMC article.
Quantitative evaluation of intravoxel incoherent motion diffusion-weighted imaging (IVIM) for differential diagnosis and grading prediction of benign and malignant breast lesions.
Xijin Mao, Xuexue Zou, +2 authors, Jing Du.
Medicine (Baltimore), 2018 Jun 29; 97(26). PMID: 29952951    Free PMC article.
Intravoxel incoherent motion magnetic resonance imaging for breast cancer: A comparison with benign lesions and evaluation of heterogeneity in different tumor regions with prognostic factors and molecular classification.
Ming Zhao, Kuang Fu, +6 authors, Jiawei Tian.
Oncol Lett, 2018 Sep 27; 16(4). PMID: 30250578    Free PMC article.
Can apparent diffusion coefficient (ADC) distinguish breast cancer from benign breast findings? A meta-analysis based on 13 847 lesions.
Alexey Surov, Hans Jonas Meyer, Andreas Wienke.
BMC Cancer, 2019 Oct 17; 19(1). PMID: 31615463    Free PMC article.
Diffusion-weighted imaging of the breast-a consensus and mission statement from the EUSOBI International Breast Diffusion-Weighted Imaging working group.
Pascal Baltzer, Ritse M Mann, +11 authors, EUSOBI international Breast Diffusion-Weighted Imaging working group.
Eur Radiol, 2019 Dec 02; 30(3). PMID: 31786616    Free PMC article.
Optimization of intravoxel incoherent motion (IVIM): variability of parameters measurements using a reduced distribution of b values for breast tumors analysis.
Natacha Raissa Doudou, Yajie Liu, +3 authors, Shaowu Wang.
MAGMA, 2019 Oct 02; 33(2). PMID: 31571014
Discrimination of Malignant and Benign Breast Lesions Using Quantitative Multiparametric MRI: A Preliminary Study.
Kurt Li, Archana Machireddy, +6 authors, Wei Huang.
Tomography, 2020 Jun 18; 6(2). PMID: 32548291    Free PMC article.
The role of histogram analysis in diffusion-weighted imaging in the differential diagnosis of benign and malignant breast lesions.
Ya-Nan Jin, Yan Zhang, +3 authors, Xiao-Ning Shao.
BMC Med Inform Decis Mak, 2020 Sep 23; 20(1). PMID: 32957985    Free PMC article.
Intravoxel Incoherent Motion Diffusion-Weighted Imaging for Quantitative Differentiation of Breast Tumors: A Meta-Analysis.
Jianye Liang, Sihui Zeng, +6 authors, Ni He.
Front Oncol, 2020 Nov 17; 10. PMID: 33194733    Free PMC article.
Systematic Review.
Breast Tumor Detection and Classification Using Intravoxel Incoherent Motion Hyperspectral Imaging Techniques.
Si-Wa Chan, Yung-Chieh Chang, +8 authors, Chin-Yao Lin.
Biomed Res Int, 2019 Aug 31; 2019. PMID: 31467888    Free PMC article.
Multidimensional Diffusion Magnetic Resonance Imaging for Characterization of Tissue Microstructure in Breast Cancer Patients: A Prospective Pilot Study.
Isaac Daimiel Naranjo, Alexis Reymbaut, +7 authors, Katja Pinker-Domenig.
Cancers (Basel), 2021 Apr 04; 13(7). PMID: 33807205    Free PMC article.