Abstract
Objective
To evaluate histogram analysis of intravoxel incoherent motion (IVIM) for discriminating the Gleason grade of prostate cancer (PCa).
Methods
A total of 48 patients pathologically confirmed as having clinically significant PCa (size > 0.5 cm) underwent preoperative DW-MRI (b of 0–900 s/mm2). Data was post-processed by monoexponential and IVIM model for quantitation of apparent diffusion coefficients (ADCs), perfusion fraction f, diffusivity D and pseudo-diffusivity D*. Histogram analysis was performed by outlining entire-tumour regions of interest (ROIs) from histological–radiological correlation. The ability of imaging indices to differentiate low-grade (LG, Gleason score (GS) ≤6) from intermediate/high-grade (HG, GS > 6) PCa was analysed by ROC regression.
Results
Eleven patients had LG tumours (18 foci) and 37 patients had HG tumours (42 foci) on pathology examination. HG tumours had significantly lower ADCs and D in terms of mean, median, 10th and 75th percentiles, combined with higher histogram kurtosis and skewness for ADCs, D and f, than LG PCa (p < 0.05). Histogram D showed relatively higher correlations (ñ = 0.641–0.668 vs. ADCs: 0.544–0.574) with ordinal GS of PCa; and its mean, median and 10th percentile performed better than ADCs did in distinguishing LG from HG PCa.
Conclusion
It is feasible to stratify the pathological grade of PCa by IVIM with histogram metrics. D performed better in distinguishing LG from HG tumour than conventional ADCs.
Key Points
• GS had relatively higher correlation with tumour D than ADCs.
• Difference of histogram D among two-grade tumours was statistically significant.
• D yielded better individual features in demonstrating tumour grade than ADC.
• D* and f failed to determine tumour grade of PCa.
Similar content being viewed by others
References
Ruzsics B, Suranyi P, Kiss P et al (2008) Head-to-head comparison between delayed enhancement and percent infarct mapping for assessment of myocardial infarct size in a canine model. J Magn Reson Imaging 28:1386–1392
Kattan M (2002) Statistical prediction models, artificial neural networks, and the sophism "I am a patient, not a statistic". J Clin Oncol 20:885–887
D'Amico AV, Whittington R, Malkowicz SB et al (1998) Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280:969–974
Cooperberg MR, Pasta DJ, Elkin EP et al (2005) The University of California, San Francisco Cancer of the Prostate Risk Assessment score: a straightforward and reliable preoperative predictor of disease recurrence after radical prostatectomy. J Urol 173:1938–1942
Stephenson AJ, Scardino PT, Eastham JA et al (2006) Preoperative nomogram predicting the 10-year probability of prostate cancer recurrence after radical prostatectomy. J Natl Cancer Inst 98:715–717
Poulakis V, Witzsch U, de Vries R et al (2004) Preoperative neural network using combined magnetic resonance imaging variables, prostate specific antigen, and Gleason score to predict prostate cancer recurrence after radical prostatectomy. Eur Urol 46:571–578
Namiki S, Saito S, Ishidoya S et al (2005) Adverse effect of radical prostatectomy on nocturia and voiding frequency symptoms. Urology 66:147–151
Barentsz JO, Richenberg J, Clements R et al (2012) ESUR prostate MR guidelines 2012. Eur Radiol 22:746–757
deSouza NM, Riches SF, Vanas NJ et al (2008) Diffusion-weighted magnetic resonance imaging: a potential non-invasive marker of tumour aggressiveness in localized prostate cancer. Clin Radiol 63:774–782
Jung SI, Donati OF, Vargas HA, Goldman D, Hricak H, Akin O (2013) Transition zone prostate cancer: incremental value of diffusion-weighted endorectal MR imaging in tumor detection and assessment of aggressiveness. Radiology 269:493–503
Jambor I, Merisaari H, Taimen P et al (2014) Evaluation of different mathematical models for diffusion-weighted imaging of normal prostate and prostate cancer using high b-values: a repeatability study. Magn Reson Med. doi:10.1002/mrm.25323
Merisaari H, Jambor I (2014) Optimization of b-value distribution for four mathematical models of prostate cancer diffusion-weighted imaging using b values up to 2000 s/mm: simulation and repeatability study. Magn Reson Med. doi:10.1002/mrm.25310
Tamura C, Shinmoto H, Soga S et al (2014) Diffusion kurtosis imaging study of prostate cancer: preliminary findings. J Magn Reson Imaging 40:723–729
Quentin M, Pentang G, Schimmoller L et al (2014) Feasibility of diffusional kurtosis tensor imaging in prostate MRI for the assessment of prostate cancer: preliminary results. Magn Reson Imaging 32:880–885
Vargas HA, Akin O, Franiel T et al (2011) Diffusion-weighted endorectal MR imaging at 3 T for prostate cancer: tumor detection and assessment of aggressiveness. Radiology 259:775–784
Langer DL, van der Kwast TH, Evans AJ et al (2010) Prostate tissue composition and MR measurements: investigating the relationships between ADC, T2, K(trans), v(e), and corresponding histologic features. Radiology 255:485–494
Turkbey B, Shah VP, Pang Y et al (2011) Is apparent diffusion coefficient associated with clinical risk scores for prostate cancers that are visible on 3-T MR images? Radiology 258:488–495
Hambrock T, Somford DM, Huisman HJ et al (2011) Relationship between apparent diffusion coefficients at 3.0-T MR imaging and Gleason grade in peripheral zone prostate cancer. Radiology 259(2):453–461
Morgan VA, Riches SF, Thomas K et al (2011) Diffusion-weighted magnetic resonance imaging for monitoring prostate cancer progression in patients managed by active surveillance. Br J Radiol 84:31–37
Park SY, Kim CK, Park BK, Lee HM, Lee KS (2011) Prediction of biochemical recurrence following radical prostatectomy in men with prostate cancer by diffusion-weighted magnetic resonance imaging: initial results. Eur Radiol 21:1111–1118
Quentin M, Blondin D, Klasen J et al (2012) Comparison of different mathematical models of diffusion-weighted prostate MR imaging. Magn Reson Imaging 30:1468–1474
Pang Y, Turkbey B, Bernardo M et al (2013) Intravoxel incoherent motion MR imaging for prostate cancer: an evaluation of perfusion fraction and diffusion coefficient derived from different b-value combinations. Magn Reson Med 69:553–562
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 168:497–505
Le Bihan D (2008) Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology 249:748–752
Klauss M, Lemke A, Grunberg K et al (2011) Intravoxel incoherent motion MRI for the differentiation between mass forming chronic pancreatitis and pancreatic carcinoma. Invest Radiol 46:57–63
Sumi M, Van Cauteren M, Sumi T, Obara M, Ichikawa Y, Nakamura T (2012) Salivary gland tumors: use of intravoxel incoherent motion MR imaging for assessment of diffusion and perfusion for the differentiation of benign from malignant tumors. Radiology 263:770–777
Sigmund EE, Vivier PH, Sui D et al (2012) Intravoxel incoherent motion and diffusion-tensor imaging in renal tissue under hydration and furosemide flow challenges. Radiology 263:758–769
Shinmoto H, Tamura C, Soga S et al (2012) An intravoxel incoherent motion diffusion-weighted imaging study of prostate cancer. AJR Am J Roentgenol 199:W496–W500
Riches SF, Hawtin K, Charles-Edwards EM, de Souza NM (2009) Diffusion-weighted imaging of the prostate and rectal wall: comparison of biexponential and monoexponential modelled diffusion and associated perfusion coefficients. NMR Biomed 22:318–325
Wang H, Cheng L, Zhang X et al (2010) Renal cell carcinoma: diffusion-weighted MR imaging for subtype differentiation at 3.0 T. Radiology 257:135–143
Rosenkrantz AB, Niver BE, Fitzgerald EF, Babb JS, Chandarana H, Melamed J (2010) Utility of the apparent diffusion coefficient for distinguishing clear cell renal cell carcinoma of low and high nuclear grade. AJR Am J Roentgenol 195:W344–W351
Kyriazi S, Collins DJ, Messiou C et al (2011) Metastatic ovarian and primary peritoneal cancer: assessing chemotherapy response with diffusion-weighted MR imaging–value of histogram analysis of apparent diffusion coefficients. Radiology 261:182–192
Wang S, Kim S, Zhang Y et al (2012) Determination of grade and subtype of meningiomas by using histogram analysis of diffusion-tensor imaging metrics. Radiology 262:584–592
Pope WB, Kim HJ, Huo J et al (2009) Recurrent glioblastoma multiforme: ADC histogram analysis predicts response to bevacizumab treatment. Radiology 252:182–189
Peng Y, Jiang Y, Yang C et al (2013) Quantitative analysis of multiparametric prostate MR images: differentiation between prostate cancer and normal tissue and correlation with Gleason score—a computer-aided diagnosis development study. Radiology 267:787–796
Oto A, Yang C, Kayhan A et al (2011) Diffusion-weighted and dynamic contrast-enhanced MRI of prostate cancer: correlation of quantitative MR parameters with Gleason score and tumor angiogenesis. AJR Am J Roentgenol 197:1382–1390
DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845
Hambrock T, Hoeks C, Hulsbergen-van de Kaa C et al (2012) Prospective assessment of prostate cancer aggressiveness using 3-T diffusion-weighted magnetic resonance imaging-guided biopsies versus a systematic 10-core transrectal ultrasound prostate biopsy cohort. Eur Urol 61:177–184
Dopfert J, Lemke A, Weidner A, Schad LR (2011) Investigation of prostate cancer using diffusion-weighted intravoxel incoherent motion imaging. Magn Reson Imaging 29:1053–1058
Ocak I, Bernardo M, Metzger G et al (2007) Dynamic contrast-enhanced MRI of prostate cancer at 3 T: a study of pharmacokinetic parameters. AJR Am J Roentgenol 189:849
Zelhof B, Pickles M, Liney G et al (2009) Correlation of diffusion-weighted magnetic resonance data with cellularity in prostate cancer. BJU Int 103:883–888
Gibbs P, Liney GP, Pickles MD, Zelhof B, Rodrigues G, Turnbull LW (2009) Correlation of ADC and T2 measurements with cell density in prostate cancer at 3.0 Tesla. Invest Radiol 44:572–576
Woodfield CA, Tung GA, Grand DJ, Pezzullo JA, Machan JT, Renzulli JF 2nd (2010) Diffusion-weighted MRI of peripheral zone prostate cancer: comparison of tumor apparent diffusion coefficient with Gleason score and percentage of tumor on core biopsy. AJR Am J Roentgenol 194:W316–W322
Sinha AA, Quast BJ, Reddy PK et al (2004) Microvessel density as a molecular marker for identifying high-grade prostatic intraepithelial neoplasia precursors to prostate cancer. Exp Mol Pathol 77:153–159
Ren J, Huan Y, Wang H et al (2008) Dynamic contrast-enhanced MRI of benign prostatic hyperplasia and prostatic carcinoma: correlation with angiogenesis. Clin Radiol 63:153–159
Schlemmer HP, Merkle J, Grobholz R et al (2004) Can pre-operative contrast-enhanced dynamic MR imaging for prostate cancer predict microvessel density in prostatectomy specimens? Eur Radiol 14:309–317
Kiessling F, Lichy M, Grobholz R et al (2004) Simple models improve the discrimination of prostate cancers from the peripheral gland by T1-weighted dynamic MRI. Eur Radiol 14:1793–1801
Cazares LH, Drake RR, Esquela-Kirscher A, Lance RS, Semmes OJ, Troyer DA (2010) Molecular pathology of prostate cancer. Cancer Biomark 9:441–459
Fournier G, Valeri A, Mangin P, Cussenot O (2004) Prostate cancer. Epidemiology. Risk factors. Pathology. Ann Urol (Paris) 38:187–206
Tozer DJ, Jager HR, Danchaivijitr N et al (2007) Apparent diffusion coefficient histograms may predict low-grade glioma subtype. NMR Biomed 20:49–57
Kang Y, Choi SH, Kim YJ et al (2011) Gliomas: Histogram analysis of apparent diffusion coefficient maps with standard- or high-b-value diffusion-weighted MR imaging–correlation with tumor grade. Radiology 261:882–890
Rosenkrantz AB, Sigmund EE, Johnson G et al (2012) Prostate cancer: feasibility and preliminary experience of a diffusional kurtosis model for detection and assessment of aggressiveness of peripheral zone cancer. Radiology 264:126–135
Acknowledgments
The scientific guarantor of this publication is Hai-Bin Shi, M.D. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. One of the authors has significant statistical expertise. No complex statistical methods were necessary for this paper. Institutional review board approval was obtained. Written informed consent was waived by the institutional review board.
Methodology: retrospective, case-control study/diagnostic or prognostic study, performed at one institution
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, YD., Wang, Q., Wu, CJ. et al. The Histogram Analysis of Diffusion-Weighted Intravoxel Incoherent Motion (IVIM) Imaging for Differentiating the Gleason grade of Prostate Cancer. Eur Radiol 25, 994–1004 (2015). https://doi.org/10.1007/s00330-014-3511-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-014-3511-4