Diffusion-Weighted Intravoxel Incoherent Motion Imaging of Renal Tumors With Histopathologic Correlation

PurposeThe aim of this study was to use intravoxel incoherent motion diffusion-weighted imaging to discriminate subtypes of renal neoplasms and to assess agreement between intravoxel incoherent motion (perfusion fraction, fp) and dynamic contrast-enhanced magnetic resonance imaging (MRI) metrics of tumor vascularity. Subjects and MethodsIn this Health Insurance Portability and Accountability Act–compliant, institutional review board–approved prospective study, 26 patients were imaged at 1.5-T MRI using dynamic contrast-enhanced MRI with high temporal resolution and diffusion-weighted imaging using 8 b values (range, 0-800 s/mm2). Perfusion fraction (fp), tissue diffusivity (Dt), and pseudodiffusivity (Dp) were calculated using biexponential fitting of the diffusion data. Apparent diffusion coefficient (ADC) was calculated with monoexponential fit using 3 b values of 0, 400, and 800 s/mm2. Dynamic contrast-enhanced data were processed with a semiquantitative method to generate model-free parameter cumulative initial area under the curve of gadolinium concentration at 60 seconds (CIAUC60). Perfusion fraction, Dt, Dp, ADC, and CIAUC60 were compared between different subtypes of renal lesions. Perfusion fraction was correlated with CIAUC60. ResultsWe examined 14 clear cell, 4 papillary, 5 chromophobe, and 3 cystic renal cell carcinomas (RCCs). Although fp had higher accuracy (area under the curve, 0.74) for a diagnosis of clear cell RCC compared with Dt or ADC, the combination of fp and Dt had the highest accuracy (area under the curve, 0.78). The combination of fp and Dt diagnosed papillary RCC and cystic RCC with 100% accuracy, and clear cell RCC and chromophobe RCC, with 86.5% accuracy. There was significant strong correlation between fp and CIAUC60 (r = 0.82; P < 0.001). ConclusionIntravoxel incoherent motion parameters fp and Dt can discriminate renal tumor subtypes. Perfusion fraction demonstrates good correlation with CIAUC60 and can assess degree of tumor vascularity without the use of exogenous contrast agent.

[1]  Bram Stieltjes,et al.  Differentiation of Pancreas Carcinoma From Healthy Pancreatic Tissue Using Multiple b-Values: Comparison of Apparent Diffusion Coefficient and Intravoxel Incoherent Motion Derived Parameters , 2009, Investigative radiology.

[2]  A. Prando Renal cell carcinoma : diffusion-weighted MR imaging for subtype differentiation at 3 . 0 , 2011 .

[3]  Steven P Sourbron,et al.  On the scope and interpretation of the Tofts models for DCE‐MRI , 2011, Magnetic resonance in medicine.

[4]  E. Squillaci,et al.  Diffusion-weighted MR imaging in the evaluation of renal tumours. , 2004, Journal of experimental & clinical cancer research : CR.

[5]  B. Taouli,et al.  Diffusion-weighted MR imaging of the liver. , 2010, Radiology.

[6]  Karl-Heinz Herrmann,et al.  Resolving arterial phase and temporal enhancement characteristics in DCE MRM at high spatial resolution with TWIST acquisition , 2011, Journal of magnetic resonance imaging : JMRI.

[7]  Ulrich Mödder,et al.  Statistical evaluation of diffusion‐weighted imaging of the human kidney , 2010, Magnetic resonance in medicine.

[8]  T. Choueiri,et al.  Recent advances in the systemic treatment of metastatic papillary renal cancer , 2009, Expert review of anticancer therapy.

[9]  Ivan Pedrosa,et al.  Magnetic Resonance Imaging–Measured Blood Flow Change after Antiangiogenic Therapy with PTK787/ZK 222584 Correlates with Clinical Outcome in Metastatic Renal Cell Carcinoma , 2008, Clinical Cancer Research.

[10]  Henry Rusinek,et al.  Variability of renal apparent diffusion coefficients: limitations of the monoexponential model for diffusion quantification. , 2010, Radiology.

[11]  R. Lenkinski,et al.  Does arterial spin-labeling MR imaging-measured tumor perfusion correlate with renal cell cancer response to antiangiogenic therapy in a mouse model? , 2009, Radiology.

[12]  H. Rusinek,et al.  Targeted coregistration of abdominal DCE MRI , 2010 .

[13]  Apurva A Desai,et al.  Sorafenib in advanced clear-cell renal-cell carcinoma. , 2007, The New England journal of medicine.

[14]  F Stacul,et al.  Diffusion-weighted MRI in the evaluation of renal lesions: preliminary results. , 2004, The British journal of radiology.

[15]  E. Karadeli,et al.  Evaluation of malignant and benign renal lesions using diffusion-weighted MRI with multiple b values , 2012, Acta radiologica.

[16]  J. Cheville,et al.  Histological subtype is an independent predictor of outcome for patients with renal cell carcinoma. , 2010, The Journal of urology.

[17]  Ivan Pedrosa,et al.  Renal cell carcinoma: dynamic contrast-enhanced MR imaging for differentiation of tumor subtypes--correlation with pathologic findings. , 2009, Radiology.

[18]  E Macaluso,et al.  Anisotropic anomalous diffusion assessed in the human brain by scalar invariant indices , 2010, Magnetic resonance in medicine.

[19]  J L Warren,et al.  Rising incidence of renal cell cancer in the United States. , 1999, JAMA.

[20]  Ravi S. Menon,et al.  Theoretical and Experimental Optimization of Laser Speckle Contrast Imaging for High Specificity to Brain Microcirculation , 2007, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  Henry Rusinek,et al.  Quantitative determination of Gd‐DTPA concentration in T1‐weighted MR renography studies , 2007, Magnetic resonance in medicine.

[22]  B. Stieltjes,et al.  Investigation of renal lesions by diffusion-weighted magnetic resonance imaging applying intravoxel incoherent motion-derived parameters--initial experience. , 2012, European journal of radiology.

[23]  Henry Rusinek,et al.  Intravoxel incoherent motion and diffusion-tensor imaging in renal tissue under hydration and furosemide flow challenges. , 2012, Radiology.

[24]  Han Wen,et al.  In vivo study of microcirculation in canine myocardium using the IVIM method † , 2003, Magnetic resonance in medicine.

[25]  G. Larry Bretthorst,et al.  On the use of bayesian probability theory for analysis of exponential decay date: An example taken from intravoxel incoherent motion experiments , 1993, Magnetic resonance in medicine.

[26]  S. Brockstedt,et al.  Perfusion-related parameters in intravoxel incoherent motion MR imaging compared with CBV and CBF measured by dynamic susceptibility-contrast MR technique , 2001, Acta radiologica.

[27]  Qun Chen,et al.  Optimal k‐space sampling for dynamic contrast‐enhanced MRI with an application to MR renography , 2009, Magnetic resonance in medicine.

[28]  María A Fernández-Seara,et al.  When Perfusion Meets Diffusion: in vivo Measurement of Water Permeability in Human Brain , 2007, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  P. Grenier,et al.  MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. , 1986, Radiology.

[30]  Hersh Chandarana,et al.  Comparison of Biexponential and Monoexponential Model of Diffusion Weighted Imaging in Evaluation of Renal Lesions: Preliminary Experience , 2010, Investigative radiology.

[31]  J. Helpern,et al.  MRI quantification of non‐Gaussian water diffusion by kurtosis analysis , 2010, NMR in biomedicine.

[32]  Makoto Obara,et al.  Salivary gland tumors: use of intravoxel incoherent motion MR imaging for assessment of diffusion and perfusion for the differentiation of benign from malignant tumors. , 2012, Radiology.

[33]  N. Rofsky,et al.  MR imaging of renal masses: correlation with findings at surgery and pathologic analysis. , 2008, Radiographics : a review publication of the Radiological Society of North America, Inc.

[34]  U. Sinha,et al.  Imaging the microcirculatory proton fraction of muscle with diffusion-weighted echo-planar imaging. , 2000, Academic radiology.

[35]  Aitao Guo,et al.  Renal cell carcinoma: diffusion-weighted MR imaging for subtype differentiation at 3.0 T. , 2010, Radiology.

[36]  Qun Chen,et al.  Optimization of b‐value sampling for diffusion‐weighted imaging of the kidney , 2012, Magnetic resonance in medicine.

[37]  J. Babb,et al.  T1 hyperintense renal lesions: characterization with diffusion-weighted MR imaging versus contrast-enhanced MR imaging. , 2009, Radiology.

[38]  David C. Alsop,et al.  Arterial spin labeling blood flow magnetic resonance imaging for the characterization of metastatic renal cell carcinoma1 , 2005 .

[39]  J. Lynch,et al.  Increasing incidence of all stages of kidney cancer in the last 2 decades in the United States: an analysis of surveillance, epidemiology and end results program data. , 2002, The Journal of urology.

[40]  A. Luciani,et al.  Liver Cirrhosis : Intravoxel Incoherent Motion MR Imaging — Pilot Study 1 , 2008 .

[41]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.

[42]  Baris Turkbey,et al.  Intravoxel incoherent motion MR imaging for prostate cancer: An evaluation of perfusion fraction and diffusion coefficient derived from different b‐value combinations , 2013, Magnetic resonance in medicine.

[43]  Reducing the influence of b‐value selection on diffusion‐weighted imaging of the prostate: Evaluation of a revised monoexponential model within a clinical setting , 2012, Journal of magnetic resonance imaging : JMRI.

[44]  Danny C. Kim,et al.  Free-Breathing Radial 3D Fat-Suppressed T1-Weighted Gradient Echo Sequence: A Viable Alternative for Contrast-Enhanced Liver Imaging in Patients Unable to Suspend Respiration , 2011, Investigative radiology.

[45]  Seong-Gi Kim,et al.  Quantification of cerebral arterial blood volume using arterial spin labeling with intravoxel incoherent motion‐sensitive gradients , 2006, Magnetic resonance in medicine.

[46]  Bram Stieltjes,et al.  Toward an optimal distribution of b values for intravoxel incoherent motion imaging. , 2011, Magnetic resonance imaging.

[47]  N. Obuchowski,et al.  Enhancement characteristics of papillary renal neoplasms revealed on triphasic helical CT of the kidneys. , 2002, AJR. American journal of roentgenology.

[48]  Joanna Leadbetter,et al.  Magnetic Resonance Imaging Measurements of the Response of Murine and Human Tumors to the Vascular-Targeting Agent ZD6126 , 2004, Clinical Cancer Research.

[49]  K. Flaherty,et al.  Pilot study of DCE-MRI to predict progression-free survival with sorafenib therapy in renal cell carcinoma , 2008, Cancer biology & therapy.

[50]  H. Rusinek,et al.  Diagnosis of cirrhosis with intravoxel incoherent motion diffusion MRI and dynamic contrast‐enhanced MRI alone and in combination: Preliminary experience , 2010, Journal of magnetic resonance imaging : JMRI.

[51]  D. Le Bihan,et al.  Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. , 1988, Radiology.

[52]  Areen K. Al-Bashir,et al.  Dynamic contrast-enhanced magnetic resonance imaging of vascular changes induced by sunitinib in papillary renal cell carcinoma xenograft tumors. , 2009, Neoplasia.

[53]  Bachir Taouli,et al.  Renal lesions: characterization with diffusion-weighted imaging versus contrast-enhanced MR imaging. , 2009, Radiology.

[54]  J. Cheville,et al.  Comparisons of Outcome and Prognostic Features Among Histologic Subtypes of Renal Cell Carcinoma , 2003, The American journal of surgical pathology.

[55]  Benjamin M Yeh,et al.  Dynamic contrast-enhanced magnetic resonance imaging as a pharmacodynamic measure of response after acute dosing of AG-013736, an oral angiogenesis inhibitor, in patients with advanced solid tumors: results from a phase I study. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[56]  Paul Russo,et al.  Prognostic impact of histological subtype on surgically treated localized renal cell carcinoma. , 2009, The Journal of urology.

[57]  Hedvig Hricak,et al.  Renal masses: characterization with diffusion-weighted MR imaging--a preliminary experience. , 2008, Radiology.

[58]  Bram Stieltjes,et al.  An in vivo verification of the intravoxel incoherent motion effect in diffusion‐weighted imaging of the abdomen , 2010, Magnetic resonance in medicine.

[59]  D. Sodickson,et al.  Intravoxel incoherent motion imaging of tumor microenvironment in locally advanced breast cancer , 2011, Magnetic resonance in medicine.

[60]  J. Lam,et al.  Renal cell carcinoma 2005: new frontiers in staging, prognostication and targeted molecular therapy. , 2005, The Journal of urology.

[61]  Bram Stieltjes,et al.  Intravoxel Incoherent Motion MRI for the Differentiation Between Mass Forming Chronic Pancreatitis and Pancreatic Carcinoma , 2011, Investigative radiology.

[62]  E. Kocakoç,et al.  Ability and utility of diffusion-weighted MRI with different b values in the evaluation of benign and malignant renal lesions. , 2011, Clinical radiology.