Intravoxel Incoherent Motion MRI of Rectal Cancer: Correlation of Diffusion and Perfusion Characteristics With Prognostic Tumor Markers.

OBJECTIVE The objective of our study was to evaluate the intravoxel incoherent motion (IVIM)-DWI derived parameters and their relationships with tumor prognostic markers using 3-T MRI in patients with rectal cancer. SUBJECTS AND METHODS Fifty-two patients with histopathologically proven rectal cancer who underwent preoperative pelvic MRI were prospectively enrolled in this study. Diffusion and perfusion parameters including the apparent diffusion coefficient (ADC), pure diffusion coefficient, perfusion fraction, and pseudodiffusion coefficient derived from IVIMDWI were independently measured by two radiologists. Comparisons of IVIM-DWI-derived parameters in patients with different tumor prognostic markers were made using the independent-samples t test, ANOVA, and Mann-Whitney U test. The correlations between IVIM-DWI-derived parameters and tumor grade and tumor stage were further evaluated using Spearman correlation analysis. Interobserver agreement was evaluated using the intraclass correlation coefficient (ICC). RESULTS Excellent interobserver reproducibility was obtained for the IVIM-DWI-derived parameters (range of ICCs with 95% limits of agreement = 0.9309-0.9948, which is narrow). ADC, pseudodiffusion coefficient, and perfusion fraction tended to rise with greater tumor differentiation (r = 0.520, p < 0.001; r = 0.447, p = 0.001; r = 0.354, p = 0.010, respectively). The pure diffusion coefficient and pseudodiffusion coefficient showed a trend of decreasing with increasing tumor stages (r = 0.479, p < 0.001; r = 0.517, p < 0.001). The group of patients with extramural vascular invasion (EMVI) showed lower pseudodiffusion coefficient values than the group of patients with no EMVI (p < 0.05). CONCLUSION IVIM-DWI-derived parameters in patients with rectal cancer, especially the pseudodiffusion coefficient, are associated with tumor grade and tumor stage and show statistically significant differences between subjects with EMVI and those without EMVI. IVIM-DWI-derived parameters would be helpful in predicting tumor aggressiveness and prognosis.

[1]  Rainer Fietkau,et al.  Preoperative versus postoperative chemoradiotherapy for rectal cancer. , 2004, The New England journal of medicine.

[2]  G. Beets,et al.  Diffusion‐weighted MRI in rectal cancer: Apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness , 2012, Journal of magnetic resonance imaging : JMRI.

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

[4]  Hongliang Sun,et al.  Assessment of tumor grade and angiogenesis in colorectal cancer: whole-volume perfusion CT. , 2014, Academic radiology.

[5]  G. Lloyd,et al.  Rectal cancer: prognostic indicators of long-term outcome in patients considered for surgery , 2014, International Journal of Colorectal Disease.

[6]  K. Miyazaki,et al.  Assessment of aggressiveness of rectal cancer using 3-T MRI: correlation between the apparent diffusion coefficient as a potential imaging biomarker and histologic prognostic factors , 2014, Acta radiologica.

[7]  David L Wilson,et al.  Radiofrequency thermal ablation: Correlation of hyperacute MR lesion images with tissue response , 2004, Journal of magnetic resonance imaging : JMRI.

[8]  W. Hohenberger,et al.  Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: results of the German CAO/ARO/AIO-94 randomized phase III trial after a median follow-up of 11 years. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[9]  Petros Martirosian,et al.  Morphological, contrast-enhanced and spin labeling perfusion imaging for monitoring of relapse after RF ablation of renal cell carcinomas , 2005, European Radiology.

[10]  H. Jang,et al.  Preoperative elevation of carcinoembryonic antigen predicts poor tumor response and frequent distant recurrence for patients with rectal cancer who receive preoperative chemoradiotherapy and total mesorectal excision: a multi-institutional analysis in an Asian population , 2013, International Journal of Colorectal Disease.

[11]  Dakeun Lee,et al.  Prognostic stratification by extramural depth of tumor invasion of primary rectal cancer based on the Radiological Society of North America proposal. , 2014, AJR. American journal of roentgenology.

[12]  D. Collins,et al.  Measurement reproducibility of perfusion fraction and pseudodiffusion coefficient derived by intravoxel incoherent motion diffusion-weighted MR imaging in normal liver and metastases , 2013, European Radiology.

[13]  Hermann Brenner,et al.  Colorectal cancer , 2014, The Lancet.

[14]  Caroline Reinhold,et al.  The use of MR imaging in treatment planning for patients with rectal carcinoma: have you checked the "DISTANCE"? , 2013, Radiology.

[15]  N. Bijedic,et al.  Cancer Antigens (CEA and CA 19-9) as Markers of Advanced Stage of Colorectal Carcinoma , 2013, Medical archives.

[16]  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.

[17]  P. T. Phang,et al.  Evaluation of endorectal ultrasound (ERUS) and MRI for prediction of circumferential resection margin (CRM) for rectal cancer. , 2017, American journal of surgery.

[18]  C. V. van Eijck,et al.  The accuracy of MRI, endorectal ultrasonography, and computed tomography in predicting the response of locally advanced rectal cancer after preoperative therapy: A metaanalysis. , 2016, Surgery.

[19]  J. Shetye,et al.  Circumferential Resection Margin as a Prognostic Marker in the Modern Multidisciplinary Management of Rectal Cancer , 2015, Diseases of the colon and rectum.

[20]  A. Jemal,et al.  Global cancer statistics, 2012 , 2015, CA: a cancer journal for clinicians.

[21]  S. Schoenberg,et al.  Multi-parametric MRI of rectal cancer - do quantitative functional MR measurements correlate with radiologic and pathologic tumor stages? , 2014, European journal of radiology.

[22]  M. Harisinghani,et al.  Apparent diffusion coefficient as a non-invasive predictor of treatment response and recurrence in locally advanced rectal cancer. , 2013, Clinical radiology.

[23]  Rui Bi,et al.  Apparent Diffusion Coefficient (ADC) Value: A Potential Imaging Biomarker That Reflects the Biological Features of Rectal Cancer , 2014, PloS one.

[24]  Weijun Peng,et al.  Extramural depth of tumor invasion at thin‐section MR in rectal cancer: Associating with prognostic factors and ADC value , 2014, Journal of magnetic resonance imaging : JMRI.

[25]  K. Koda,et al.  Quantitative Measurement of Blood Flow Using Perfusion CT for Assessing Clinicopathologic Features and Prognosis in Patients with Rectal Cancer , 2009, Diseases of the colon and rectum.

[26]  B. Choi,et al.  Differentiation of poorly differentiated colorectal adenocarcinomas from well- or moderately differentiated colorectal adenocarcinomas at contrast-enhanced multidetector CT , 2014, Abdominal Imaging.

[27]  C. Compton,et al.  The American Joint Committee on Cancer: the 7th Edition of the AJCC Cancer Staging Manual and the Future of TNM , 2010, Annals of Surgical Oncology.

[28]  E. Venkatraman,et al.  The relationship of pathologic tumor regression grade (TRG) and outcomes after preoperative therapy in rectal cancer. , 2005, International journal of radiation oncology, biology, physics.

[29]  H. Vargas,et al.  Intravoxel Incoherent Motion-derived Histogram Metrics for Assessment of Response after Combined Chemotherapy and Radiation Therapy in Rectal Cancer: Initial Experience and Comparison between Single-Section and Volumetric Analyses. , 2016, Radiology.

[30]  V. Goh,et al.  Can perfusion CT assessment of primary colorectal adenocarcinoma blood flow at staging predict for subsequent metastatic disease? A pilot study , 2008, European Radiology.

[31]  B. Choi,et al.  Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. , 2014, Radiology.

[32]  Lin-Feng Yan,et al.  Intravoxel incoherent motion diffusion-weighted MR imaging of gliomas: efficacy in preoperative grading , 2014, Scientific Reports.

[33]  T. Sasada,et al.  Diffusion-weighted Magnetic Resonance Imaging for Detecting Lymph Node Metastasis of Rectal Cancer , 2011, World Journal of Surgery.

[34]  Bram Stieltjes,et al.  Intravoxel Incoherent Motion (IVIM) Diffusion Imaging in Prostate Cancer - What Does It Add? , 2014, Journal of computer assisted tomography.

[35]  R. Hagger,et al.  Extramural vascular invasion is an adverse prognostic indicator of survival in patients with colorectal cancer , 2009, Colorectal disease : the official journal of the Association of Coloproctology of Great Britain and Ireland.

[36]  Jong Seob Park,et al.  A Circumferential Resection Margin of 1 mm Is a Negative Prognostic Factor in Rectal Cancer Patients With and Without Neoadjuvant Chemoradiotherapy , 2014, Diseases of the colon and rectum.

[37]  S. Park,et al.  Locally advanced rectal cancer: diffusion-weighted MR tumour volumetry and the apparent diffusion coefficient for evaluating complete remission after preoperative chemoradiation therapy , 2013, European Radiology.

[38]  Q. Chan,et al.  Nasopharyngeal carcinoma: comparison of diffusion and perfusion characteristics between different tumour stages using intravoxel incoherent motion MR imaging , 2013, European Radiology.

[39]  Myeong-Jin Kim,et al.  MRI-detected extramural vascular invasion is an independent prognostic factor for synchronous metastasis in patients with rectal cancer , 2015, European Radiology.

[40]  A. Jemal,et al.  Global Cancer Statistics , 2011 .

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

[42]  Eui Jin Hwang,et al.  Intravoxel Incoherent Motion Diffusion-Weighted Imaging of Pancreatic Neuroendocrine Tumors: Prediction of the Histologic Grade Using Pure Diffusion Coefficient and Tumor Size , 2014, Investigative radiology.

[43]  J. Monson,et al.  Preoperative radiotherapy versus selective postoperative chemoradiotherapy in patients with rectal cancer (MRC CR07 and NCIC-CTG C016): a multicentre, randomised trial , 2009, The Lancet.

[44]  A. Wienke,et al.  Correlations between intravoxel incoherent motion (IVIM) parameters and histological findings in rectal cancer: preliminary results , 2017, Oncotarget.

[45]  김영진,et al.  Tumor perfusion-related parameter of diffusion-weighted magnetic resonance imaging: Correlation with histological microvessel density , 2014 .

[46]  A. Toms,et al.  The prognostic significance of MRI-detected extramural venous invasion in rectal carcinoma. , 2014, Clinical radiology.

[47]  Seong-Gi Kim,et al.  In vivo MR measurements of regional arterial and venous blood volume fractions in intact rat brain , 2000, Magnetic resonance in medicine.