Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade.

OBJECTIVE The purpose of our study was to assess the utility of the apparent diffusion coefficient (ADC) in distinguishing low-grade and high-grade clear cell renal cell carcinoma (ccRCC). MATERIALS AND METHODS The cases of 57 patients with pathologically proven ccRCC who underwent preoperative MRI, including diffusion-weighted imaging, were retrospectively assessed. ADC values were obtained from ADC maps calculated using b-value combinations of 0 and 400 s/mm² and of 0 and 800 s/mm² (hereafter referred to as ADC-400 and ADC-800). Lesions were also evaluated for an array of conventional MRI features. A single expert uropathologist reviewed all slides to determine nuclear grade. The utility of ADC for detecting high-grade ccRCC, alone and in combination with conventional MRI features, was assessed using receiver operating characteristic (ROC) analysis and binary logistic regression. RESULTS ADC-400 and ADC-800 were significantly lower among high-grade than among low-grade ccRCC (2.24 ± 0.50 mm²/s vs 1.59 ± 0.57 mm²/s for ADC-400, p < 0.001; 1.85 ± 0.40 mm²/s vs 1.28 ± 0.48 mm²/s for ADC-800; p < 0.001). The area under the ROC curve for identifying high-grade ccRCC using ADC-400 and ADC-800 was 0.801 and 0.824 respectively (p = 0.606), with optimal thresholds, sensitivity, and specificity as follows: ADC-400: 2.17 mm²/s, 88.5%, 64.5% and ADC-800: 1.20 mm²/s, 65.4%, 96.0%. Using multivariate logistic regression, only necrosis (p = 0.0229) and perinephric fat invasion (p = 0.0160) were retained among conventional imaging features as independent risk factors for high-grade ccRCC. The accuracy of the logistic regression model for predicting high-grade ccRCC was significantly improved by inclusion of either ADC-400 (p = 0.0143) or ADC-800 (p = 0.015). CONCLUSION ADC is significantly lower in high-grade ccRCC compared with low-grade ccRCC and increases the accuracy for detecting high-grade ccRCC compared with conventional MRI features alone.

[1]  J. Cheville,et al.  Cancer specific survival for patients with pT3 renal cell carcinoma-can the 2002 primary tumor classification be improved? , 2005, The Journal of urology.

[2]  Matteo Brunelli,et al.  Original and reviewed nuclear grading according to the Fuhrman system , 2005, Cancer.

[3]  R. Uzzo,et al.  Management of small renal masses. , 2009, Seminars in ultrasound, CT, and MR.

[4]  I. Yamada,et al.  Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. , 1999, Radiology.

[5]  E. Barret,et al.  Localized renal cell carcinoma management: an update. , 2008, International braz j urol : official journal of the Brazilian Society of Urology.

[6]  H. Wijkstra,et al.  Changes in the stage and surgical management of renal tumours during 1995–2005: an analysis of the Dutch national histopathology registry , 2008, BJU international.

[7]  B. Ross,et al.  Magnetic Resonance Imaging Determination of Tumor Grade and Early Response to Temozolomide in a Genetically Engineered Mouse Model of Glioma , 2007, Clinical Cancer Research.

[8]  F. Kendel,et al.  Impact of macroscopic tumour necrosis to predict survival of patients with surgically resected renal cell carcinoma , 2008, Scandinavian journal of urology and nephrology.

[9]  L. Bostad,et al.  Renal cell carcinoma: A clinicopathological follow-up study after radical nephrectomy , 2007, Scandinavian journal of urology and nephrology.

[10]  T. Hirai,et al.  Magnetic resonance imaging of pilocytic astrocytomas: usefulness of the minimum apparent diffusion coefficient (adc) value for differentiation from high-grade gliomas , 2008, Acta radiologica.

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

[12]  Toshinori Hirai,et al.  Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus two-parameter pilot method. , 2009, Radiology.

[13]  S. Fuhrman,et al.  Prognostic significance of morphologic parameters in renal cell carcinoma , 1982, The American journal of surgical pathology.

[14]  J. Stoker,et al.  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. , 2009, European journal of radiology.

[15]  M. Jewett,et al.  Renal tumor natural history: the rationale and role for active surveillance. , 2008, The Urologic clinics of North America.

[16]  S. Silverman,et al.  Comparison of percutaneous and surgical approaches to renal tumor ablation: metaanalysis of effectiveness and complication rates. , 2008, Journal of vascular and interventional radiology : JVIR.

[17]  J. Cheville,et al.  Comparison of standardized and nonstandardized nuclear grade of renal cell carcinoma to predict outcome among 2,042 patients. , 2002, American journal of clinical pathology.

[18]  S Cerdán,et al.  Molecular crowding and viscosity as determinants of translational diffusion of metabolites in subcellular organelles. , 1999, Archives of biochemistry and biophysics.

[19]  D. Jacqmin,et al.  [Reproducibility of Fuhrman nuclear grade: advantages of a two-grade system]. , 2006, Progres en urologie : journal de l'Association francaise d'urologie et de la Societe francaise d'urologie.

[20]  Mahul B. Amin,et al.  Prognostic Impact of Histologic Subtyping of Adult Renal Epithelial Neoplasms: An Experience of 405 Cases , 2002, The American journal of surgical pathology.

[21]  Toshinori Hirai,et al.  Usefulness of diffusion‐weighted MRI with echo‐planar technique in the evaluation of cellularity in gliomas , 1999, Journal of magnetic resonance imaging : JMRI.

[22]  C. Kim,et al.  High-b-value diffusion-weighted imaging at 3 T to detect prostate cancer: comparisons between b values of 1,000 and 2,000 s/mm2. , 2010, AJR. American journal of roentgenology.

[23]  E. Squillaci,et al.  Malignant renal neoplasms: correlation between ADC values and cellularity in diffusion weighted magnetic resonance imaging at 3 T , 2008, La radiologia medica.

[24]  C. Zuiani,et al.  Relevance of b‐values in evaluating liver fibrosis: A study in healthy and cirrhotic subjects using two single‐shot spin‐echo echo‐planar diffusion‐weighted sequences , 2008, Journal of magnetic resonance imaging : JMRI.

[25]  A. Fergany,et al.  Minimally invasive surgery for renal cell carcinoma , 2009, Expert review of anticancer therapy.

[26]  H. Lang,et al.  Reproductibilité du grade nucléaire de Fuhrman Avantages d'un regroupement en deux grades , 2006 .

[27]  J. Cadeddu,et al.  Intermediate comparison of partial nephrectomy and radiofrequency ablation for clinical T1a renal tumours , 2007, BJU international.

[28]  S. Bektaş,et al.  Intraobserver and Interobserver Variability of Fuhrman and Modified Fuhrman Grading Systems for Conventional Renal Cell Carcinoma , 2009, The Kaohsiung journal of medical sciences.

[29]  Gary Liney,et al.  Correlation of diffusion‐weighted magnetic resonance data with cellularity in prostate cancer , 2009, BJU international.

[30]  G. Einarsson,et al.  Histological subtyping and nuclear grading of renal cell carcinoma and their implications for survival: a retrospective nation-wide study of 629 patients. , 2005, European urology.

[31]  R. Uzzo,et al.  Optimal management of localized renal cell carcinoma: surgery, ablation, or active surveillance. , 2009, Journal of the National Comprehensive Cancer Network : JNCCN.

[32]  Mazhar Husain,et al.  Biological correlates of diffusivity in brain abscess , 2005, Magnetic resonance in medicine.

[33]  S. Pahernik,et al.  Prognostic stratification of localized renal cell carcinoma by tumor size. , 2008, The Journal of urology.

[34]  S. Boorjian,et al.  The evolving management of small renal masses , 2009, Current oncology reports.

[35]  A. Belldegrun,et al.  Prognostic factors for renal cell carcinoma with tumor thrombus extension. , 2007, The Journal of urology.

[36]  B. Lane,et al.  Active surveillance of renal masses in elderly patients. , 2008, The Journal of urology.

[37]  M. Kitajima,et al.  Cerebral gliomas: prospective comparison of multivoxel 2D chemical-shift imaging proton MR spectroscopy, echoplanar perfusion and diffusion-weighted MRI , 2002, Neuroradiology.

[38]  N. Rofsky,et al.  MR classification of renal masses with pathologic correlation , 2008, European Radiology.

[39]  B. Delahunt Advances and controversies in grading and staging of renal cell carcinoma , 2009, Modern Pathology.

[40]  R. Uzzo,et al.  Predicting growth of solid renal masses under active surveillance. , 2008, Urologic oncology.

[41]  Gaetano Mobilio,et al.  Prognostic Value of Renal Cell Carcinoma Nuclear Grading: Multivariate Analysis of 333 Cases , 2001, Urologia Internationalis.

[42]  M Jayson,et al.  Increased incidence of serendipitously discovered renal cell carcinoma. , 1998, Urology.

[43]  N. Bulakbaşı,et al.  The Added Value of the Apparent Diffusion Coefficient Calculation to Magnetic Resonance Imaging in the Differentiation and Grading of Malignant Brain Tumors , 2004, Journal of computer assisted tomography.

[44]  Maamoun M Al-Aynati,et al.  Interobserver and intraobserver variability using the Fuhrman grading system for renal cell carcinoma. , 2003, Archives of pathology & laboratory medicine.

[45]  F. Sánchez-Martín,et al.  Small Renal Masses: Incidental Diagnosis, Clinical Symptoms, and Prognostic Factors , 2009, Advances in urology.

[46]  J. Cheville,et al.  Stage pT1 conventional (clear cell) renal cell carcinmoa: pathological features associated with cancer specific survival. , 2001, The Journal of urology.

[47]  Bin Wang,et al.  Diffusion‐weighted imaging of prostate cancer: Correlation between apparent diffusion coefficient values and tumor proliferation , 2009, Journal of magnetic resonance imaging : JMRI.

[48]  R. Montironi,et al.  Prognostic role of Fuhrman grade and vascular endothelial growth factor in pT1a clear cell carcinoma in partial nephrectomy specimens. , 2005, The Journal of urology.

[49]  B. Delahunt,et al.  Outcome prediction for renal cell carcinoma: evaluation of prognostic factors for tumours divided according to histological subtype , 2007, Pathology.

[50]  Toshihiro Kumabe,et al.  Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. , 2006, Radiology.

[51]  Christian Coulange,et al.  Prognostic value of nuclear grade of renal cell carcinoma , 1995, Cancer.

[52]  G. Haber,et al.  Minimally invasive nephron-sparing surgery , 2008, Current opinion in urology.

[53]  Gary P Liney,et al.  Correlation of ADC and T2 Measurements With Cell Density in Prostate Cancer at 3.0 Tesla , 2009, Investigative radiology.

[54]  D. Jacqmin,et al.  Multicenter determination of optimal interobserver agreement using the Fuhrman grading system for renal cell carcinoma , 2005, Cancer.

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

[56]  F. Saad,et al.  The current management of small renal masses , 2009, Current opinion in supportive and palliative care.

[57]  Hiroshi Honda,et al.  Usefulness of apparent diffusion coefficient map in diagnosing prostate carcinoma: Correlation with stepwise histopathology , 2008, Journal of magnetic resonance imaging : JMRI.

[58]  James M Provenzale,et al.  Lymphomas and high-grade astrocytomas: comparison of water diffusibility and histologic characteristics. , 2002, Radiology.

[59]  D. Collins,et al.  Diffusion-weighted MRI in the body: applications and challenges in oncology. , 2007, AJR. American journal of roentgenology.

[60]  芳映 野々村 Relationship between bone marrow cellularity and apparent diffusion coefficient , 2001 .

[61]  B. Delahunt,et al.  Nucleolar Grade But Not Fuhrman Grade is Applicable to Papillary Renal Cell Carcinoma , 2006, The American journal of surgical pathology.

[62]  Faiza Admiraal-Behloul,et al.  Reproducibility of brain ADC histograms , 2004, European Radiology.

[63]  L. Medeiros,et al.  Renal cell carcinoma. Prognostic significance of morphologic parameters in 121 cases , 1988, Cancer.

[64]  R. M. Hsu,et al.  Small renal cell carcinomas: correlation of size with tumor stage, nuclear grade, and histologic subtype. , 2004, AJR. American journal of roentgenology.

[65]  B. Delahunt,et al.  Morphologic typing of papillary renal cell carcinoma: comparison of growth kinetics and patient survival in 66 cases. , 2001, Human pathology.

[66]  Katsuyoshi Ito,et al.  Apparent diffusion coefficient values in peripheral and transition zones of the prostate: Comparison between normal and malignant prostatic tissues and correlation with histologic grade , 2008, Journal of magnetic resonance imaging : JMRI.

[67]  L. True The time for accurate Fuhrman grading of renal cell carcinomas has arrived. , 2002, American journal of clinical pathology.

[68]  B. Delahunt,et al.  Fuhrman Grading is not Appropriate for Chromophobe Renal Cell Carcinoma , 2007, The American journal of surgical pathology.

[69]  I. Gill,et al.  The evolving presentation of renal carcinoma in the United States: trends from the Surveillance, Epidemiology, and End Results program. , 2006, The Journal of urology.

[70]  Inderbir S Gill,et al.  A critical analysis of the actual role of minimally invasive surgery and active surveillance for kidney cancer. , 2010, European urology.

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

[72]  Juan Alvarez-Linera,et al.  Predicting the Histopathological Grade of Cerebral Gliomas Using High b value MR DW Imaging at 3‐Tesla , 2008, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[73]  R C McKinstry,et al.  Evaluating pediatric brain tumor cellularity with diffusion-tensor imaging. , 2001, AJR. American journal of roentgenology.

[74]  R. Uzzo,et al.  Focal therapy for kidney cancer: a systematic review , 2009, Current opinion in urology.