ORIGINAL RESEARCH. Correlation of Standard Diffusion-Weighted Imaging and Diffusion Kurtosis Imaging With Distant Metastases of Rectal Carcinoma

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1 ORIGINAL RESEARCH Correlation of Standard Diffusion-Weighted Imaging and Diffusion Kurtosis Imaging With Distant Metastases of Rectal Carcinoma Jing Yu, MD, 1 Dong-Ya Huang, MD, 2 Yan Li, MS, 1 Xin Dai, MS, 1 and Hai-Bin Shi 1 * Purpose: To investigate the correlation of standard diffusion-weighted imaging (DWI) and diffusion kurtosis imaging (DKI) with distant metastases of rectal carcinoma. Materials and Methods: Fifty-eight patients with rectal carcinoma (27 with distant metastasis and 31 with no metastasis) were included in this study. The apparent diffusion coefficient (ADC) value from standard DWI (b values of 0 and 1000 sec/mm 2 ), D app,andk app from DKI (b values of 0, 700, 1400, and 2000 sec/mm 2 ) were acquired with a 3.0T magnetic resonance imaging (MRI) scanner. These quantitative parameters were calculated from the entire tumors. Receiver operating characteristic curve analyses were conducted to assess the utility for discrimination of tumor with distant metastasis and those without metastasis. Parameters were compared using the independent-samples t-test. Results: The histogram metrics 10th percentile of D app (D app-10th ) and ADC values (ADC 10th ) were significantly lower in the distant metastasis group than those without metastasis ( vs mm 2 /s, P ; vs mm 2 /s, P ). D app-10th showed relatively higher area under the curve (AUC) (0.856 vs , P ), and higher specificity (100% vs. 68%) than ADC 10th did for differentiation of lesions with distant metastasis from those without metastasis. Conclusion: DKI was relatively better than standard DWI in discriminating rectal carcinoma with distant metastasis from those without metastasis. J. MAGN. RESON. IMAGING 2016;44: Rectal carcinoma is one of the most commonly diagnosed gastrointestinal malignancies in the world. 1,2 Total mesorectal excision (TME) technique 3 and neoadjuvant chemoradiation (CRT) have improved local control and, in some studies, survival. 4 7 However, the outcome of patients with distant metastasis remains worse. Neither preoperative CRT nor short-course radiotherapy has led to better survival compared with TME alone, possibly because of distant metastasis. 8 Thus, control of distant metastasis is one of the major concerns in the treatment of locally advanced rectal cancer. 9 Some clinical trials including preoperative induction chemotherapy for intense systemic control before standard treatment have been performed on patients with the greatest risk of distant metastasis. 10 Dedicated and multiparametric preoperative rectum magnetic resonance imaging (MRI) has facilitated an increased role for imaging in risk stratification. Specifically, quantitative MRI metrics may serve as noninvasive biomarkers of tumor aggressiveness by reflecting different microstructural configurations of cancer. 11,12 Among recent advances in MRI techniques, diffusion-weighted imaging (DWI) has been increasingly used. Standard DWI can be used to measure the apparent diffusion coefficient (ADC). ADC has been widely used to detect local lymph node metastasis in patients with rectal carcinoma A new diffusion metric, diffusion kurtosis imaging (DKI), first described by Jensen et al in 2005, 16 has become popular. DKI shows the structural connectivity of tissue and View this article online at wileyonlinelibrary.com. DOI: /jmri Received Aug 4, 2015, Accepted for publication Dec 8, The first two authors contributed equally to this work. *Address reprint requests to: H.-B.S., Department of Radiology, First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Rd, Nanjing , China. shihb@njmu.edu.cn From the 1 Department of Radiology, First Affiliated Hospital of Nanjing Medical University, Nanjing, China; and 2 Department of General Surgery, First Affiliated Hospital of Nanjing Medical University, Nanjing, China. VC 2015 Wiley Periodicals, Inc. 221

2 Journal of Magnetic Resonance Imaging TABLE 1. Imaging Protocol for Standard DWI and DKI Sequences Parameter Standard DWI DKI Sequence Single-shot echo planar Single-shot echo planar Orientation Axial bilateral Axial bilateral Repetition time (msec) Echo time (msec) Field of view (mm 2 ) Matrix Section thickness (mm) 5 5 No. of sections No. of signals acquired 3 3 Bandwidth (Hz/pixel) b values (sec/mm 2 ) 0, , 700, 1400, 2000 DWI: diffusion-weighted imaging; DKI: diffusion kurtosis imaging. may contain useful information related to pathophysiology. 17 The use of DKI has been applied in the assessment of tumor aggressiveness of prostate cancer, breast cancer, 11 and cerebral glioma. 21,22 Therefore, the aim of our study was to investigate the correlation of standard DWI and DKI with distant metastases in patients with rectal carcinoma. Materials and Methods Patients The Institutional Review Board of our hospital approved this retrospective study and informed consent was waived. Patients with pathologically confirmed rectal adenocarcinoma at our hospital between September 2013 and December 2014 were screened. Those who were initially investigated via MRI of the rectum and a computed tomography (CT) examination of the chest, abdomen, and pelvis for both local and distant staging, and also followed up FIGURE 1: Flowchart of the study population. with a CT examination of the chest, abdomen, and pelvis at 6 months postdiagnosis, were included in the study. Patients with the following criteria were excluded: 1) patients who loss of follow-up (n 5 41); 2) patients who had undergone prior radiation treatment before MRI examination (n 5 13); or 3) serious artifacts on standard DWI or DKI (n 5 8, one with Parkinson disease, the rest were due to respiratory artifact). When distant metastasis was suspected on initial CT, contrast-enhanced liver MRI or fludeoxyglucosepositron emission tomography/ct (FDG-PET/CT) were used for more precise evaluation. Patients who were found to have distant metastases at initial staging or newly detected metastatic lesions within 6 months after the initial staging workup were considered synchronous metastasis. MRI Protocol All MRI examinations were performed using a 3.0T Siemens MAG- NETOM Avanto (MAGNETOM TrioTim; Siemens, Erlangen, Germany) with 16 elements of the pelvic phased-array coil (location: anterior). Two diffusion sequences (ie, standard DWI and DKI) were performed with comparable parameters (Table 1) using a three-image trace mode to determine the diffusion gradient. Oblique axial T 1 - weighted 2D turbo spin-echo images (repetition time / echo time [TR/TE], 722/11 msec; section thickness, 3.0 mm; intersection gap, 0.3 mm; field of view [FOV], 25 cm; and matrix, ) and sagittal and oblique axial and oblique coronal T 2 -weighted 2D turbo spin-echo images (TR / effective TE, 4000/99 msec; section thickness, 3.0 mm; intersection gap, 0.3 mm; FOV, 25 cm; and matrix, ) were performed before standard DWI and DKI. Image Analysis Two board-certified radiologists (with 10 and 4 years of experience in pelvic MRI, respectively), who were not involved in the patient selection, blinded to the reference standard, independently evaluated the MR image sets. ADC maps were generated from standard DWI with b values of 0 and 1000 sec/mm 2, D app and K app maps were calculated 222 Volume 44, No. 1

3 Yu et al.: Metastases Prediction by Standard DWI and DKI (10 23 mm 2 /s), and K app, a dimensionless parameter, is the apparent kurtosis coefficient. 16 The radiologists manually drew regions of interest (ROIs) along contours of the tumor, covering the whole lesion with exclusion of the necrosis, peripheral fat, and artifact based on T 2 - weighted images as a guide. Histogram analysis of diffusion features (D app, K app, and ADCs) were performed using PASW Statistics 18.0 (SPSS, Chicago, IL). Based on an entire-tumor histogram analysis, the following histogram parameters were derived from D app, K app, and ADC maps: 1) mean; 2) median; 3) kurtosis, which is the degree of peakedness of a distribution; 4) skewness, which is a measure of the degree of asymmetry of a distribution; and 5) 10th and 6) 90th percentiles. Clinicopathologic Examinations Clinical factors were derived from the patients records including age and gender. Histopathological information was obtained from pathology reports. We assessed depth of invasion (T stage), lymph TABLE 2. Summary of Clinicopathologic characteristics of included lesions Clinicopathologic characteristics No. (%) a Gender Male 35 (60.34%) Female 23 (39.66%) Age (63.79%) > (36.21%) Histological T stage pt1 1 (2.33%) pt2 19 (44.18%) pt3 22 (51.16%) pt4 1 (2.33%) Histological N stage FIGURE 2: A 70-year-old woman with rectal carcinoma who developed early lung metastasis. a: T 2 -weighted turbo spinecho (TSE) sagittal image demonstrated a mass (arrow) in the upper part of rectum. b: Signal of mass was high on DW image (arrow). c: Small lung metastasis (arrow) developed in the right lower lung on follow-up chest CT at 5 months after total mesorectal excision. from DKI with b values of 0, 700, 1400, and 2000 sec/mm 2 using in-house developed software (FireVoxel; CAI2R, New York University, NY). The relationship between signal intensity of DKI and b-values can be expressed by S ðbþ 5S 0 e 2bDapp11 6b 2 D 2 appk app, where S is the signal intensity (arbitrary units), b is the b value (sec/mm 2 ), D app is the apparent diffusion parameter of Gaussian distribution Negative 15(34.88%) Positive 28(65.12%) Histological grade Well differentiated 1 (2.33%) Moderately differentiated 17 (39.53%) Poorly differentiated 25 (58.14%) Distant metastasis Negative 27 (46.55%) Positive 31 (53.45%) a Data are number of patients, with percentages in parentheses. July

4 Journal of Magnetic Resonance Imaging FIGURE 3: A 48-year-old man with rectal carcinoma who had liver metastasis at initial staging. a: OnT 2 -weighted turbo spin-echo (TSE) sagittal image, a mass was seen. Postcontrast axial CT (b: arterial phase; c: venous phase) showed a peripherally enhancing nodular lesion in the right lobe of the liver. The color-coded D app map (d) and ADC map (f) shows mixed green and blue color in the corresponding tumor with D app of s/mm 2 and ADC of s/mm 2. The color-coded K app map (e) shows mixed red and green color in the corresponding tumor with a K app value of node metastasis (N stage), and tumor differentiation grade (well, moderately, and poorly differentiated). Statistical Analysis Statistical packages (PASW Statistics 18.0 SPSS; MedCalc, v. 11.5, Mariakerke, Belgium; and R, v ) were used to perform the statistical analyses. Interobserver variability for the two readings (D app and K app measurements on DKI) was analyzed by calculating the intraclass correlation coefficient (ICC) for single measurements (0 0.20, poor correlation; , fair correlation; , moderate correlation; , good correlation; and , excellent correlation). Receiver operating characteristic (ROC) curve analyses were conducted to assess and compare ADC, D app, and K app in terms of their utility for discrimination of tumor with distant metastasis and those without distant metastasis. For the ROC analyses, sensitivity and specificity were calculated by using a threshold criterion determined as that value that would maximize the average of sensitivity and specificity. The normality and homoscedasticity of the multiparametric imaging data were tested using the Q-Q plots and the Levene tests. Data satisfying the assumption were subjected to independent-sample t-test. Data not satisfying the assumption (kurtosis and skewness) were analyzed using the Mann Whitney U-test. Spearman correlation analysis was performed to investigate the correlations between ADC, D app, K app and histopathological factors. P values less than 0.05 were considered statistically significant. Results Patients In total, 241 patients with rectal adenocarcinoma were assessed. Among all patients, 27 patients were confirmed to have distant metastases (male: 17, female: 10; median age 56 years, range years). Among the metastases group, 21 patients had metastases at initial staging and 6 patients were detected with metastatic lesions during follow-up within 6 months. The rest were confirmed to have no distant metastasis by CT examination of the chest, abdomen, and pelvis at 6 months postdiagnosis. Thirtyone were randomly chosen as a control group (male: 18, female: 13; median age 62 years, range years) (Fig. 1). Hepatic metastases were the most common metastases (17 patients, 63%) followed by lung metastases (eight patients, 30%). Two patients (7%) had both liver and lung metastases (Fig. 2). Distant lymph node metastases and adrenal gland metastases was not observed. Distant metastases were confirmed pathologically by surgery in 12 patients and by sequential radiologic follow-up in 15 patients. Among the enrolled 58 patients, 28 patients underwent curative surgery without neoadjuvant treatment (26 patients 224 Volume 44, No. 1

5 Yu et al.: Metastases Prediction by Standard DWI and DKI TABLE 3. Histogram ADC, D app, and K app Among Rectal Carcinoma: With Distant Metastasis vs. Without Distant Metastasis Variable With distant metastases Without distant metastases P value Histogram ADC a Mean Median th* th Kurtosis Skewness a Histogram D app Mean* Median* th* th Kurtosis Skewness b Histogram K app Mean Median th th Kurtosis Skewness a Unit of mm 2 /s for ADC and D app ; b Unit of for K app. *Statistical differences; ADC: apparent diffusion coefficient; D app : apparent diffusion parameter; K app : apparent kurtosis coefficient. underwent TME and two underwent transanal excision), 15 patients underwent chemotherapy or chemoradiotherapy only, and 15 patients underwent surgery after neoadjuvant treatment. Clinical and histopathological information of the enrolled patients are summarized in Table 2. Summary of Metrics Derived From Standard DWI and DKI The interobserver agreement (ICC) for D app-median, D app-mean, D app-10th, D app-90th, K app-median, K app-mean, K app-10th, and K app-90th was (95% confidence interval [CI], ), (95% CI, ), (95% FIGURE 4: Boxplots show ADC 10th and D app-10th in lesions with distant metastasis and without distant metastasis. a,b: ADC 10th and D app-10th were significantly lower in the lesions with distant metastasis than in the lesions without distant metastasis ( vs mm 2 /s, P ; vs , P ; respectively). July

6 Journal of Magnetic Resonance Imaging TABLE 4. Correlation Between ADC, D app, and K app and Histopathological Factors Variable Histological T stage Histological N stage Histological grade Distant metastasis r (P value) r (P value) r (P value) r (P value) Histogram ADC 10th (0.310) (0.490) (0.351) (0.033)* Histogram D app Mean (0.245) (0.458) (0.077) (0.023)* Median (0.234) (0.631) (0.125) (0.019)* 10th (0.161) (0.250) (0.191) (<0.001)* Histogram K app Kurtosis 0.329(0.047)* (0.942) 0.019(0.909) 0.265(0.078) *Statistical differences; ADC: apparent diffusion coefficient; D app : apparent diffusion parameter; K app : apparent kurtosis coefficient. CI, ), (95% CI, ), (95% CI, ), (95% CI, ), (95% CI, ), and (95% CI, ), respectively. The software successfully generated parametric ADC, D app, and K app maps and histogram distributions in all patients, with sample patients shown in Fig. 3. A summary of the histogram metrics ADC, D app,and K app is provided in Table 3 and Fig. 4. D app-mean, D app-median, and D app-10th were significantly lower in the lesions with distant metastasis than in the lesions without distant metastasis ( vs ; vs ; vs , mm 2 /s respectively; P ). ADC 10th were significantly lower in the lesions with distant metastasis than in the lesions FIGURE 5: Graph shows receiver operating characteristic curves to assess utility of ADC 10th and D app-10th for discriminating lesions with distant metastasis from those without distant metastasis. AUC was for ADC 10th and for D app-10th. without distant metastasis ( vs mm 2 /s, respectively; P ). The correlations between ADC, D app, K app and histopathological factors are provided in Table 4. The ADC 10th, D app-mean, D app-median, and D app-10th correlated significantly with distant metastasis. Kurtosis of K app was also correlated with histological T stage. No statistically significant correlations were found for D app, K app, and ADC values in tumors of different histological N stage and differentiation grade. Diagnosis Performance of Metrics Derived From Standard DWI and DKI Table 5 demonstrates the results of the ROC analysis of ADC, D app, and K app in differentiating lesions with distant metastasis from those without metastasis. For the DKI measurements, in comparison with histogram-derived quantitative parameters, D app-10th resulted in highest AUCs of (P < ), with sensitivity of 60.0% and specificity of 100.0%, respectively. D app-10th showed significantly higher AUC (0.856 vs , P ), and higher specificity (100.0% vs. 68.0%) for differentiation of rectal tumor with distant metastasis from those without metastasis than ADC 10th did (Fig. 5). Discussion In the present study we successfully performed DKI to distinguish patients with distant metastasis from those without distant metastasis and found D app to be significantly lower in lesions with distant metastasis than in the lesions without distant metastasis. Negative correlations were found between D app and distant metastasis. A possible explanation is that there is more marked variation in cell size and shape within more aggressive rectal tumors (with distant metastasis) in comparison with less aggressive rectal tumors. 23 In more aggressive tumor tissues, the increased cellularity usually leads to more barriers within the tissues, which disturbs the 226 Volume 44, No. 1

7 Yu et al.: Metastases Prediction by Standard DWI and DKI TABLE 5. Receiver Operating Characteristic Analysis of ADC, D app, and K app for Discriminating Rectal Carcinoma With Distant Metastasis From Those Without Distant Metastasis Variable Cutoff value AUC Sensitivity (%) Specificity (%) p value Histogram ADC a Mean ( ) 33.3 ( ) 48.0 ( ) Median ( ) 33.3 ( ) 44.0 ( ) th ( ) 60.0 ( ) 68.0 ( ) th > ( ) 66.7 ( ) 72.0 ( ) Kurtosis > ( ) 52.9( ) 72.0 ( ) Skewness ( ) 35.3( ) 76.0 ( ) a Histogram D app Mean ( ) 60.0 ( ) 76.0 ( ) Median ( ) 50.0 ( ) 80.0 ( ) th ( ) 60.0 ( ) ( ) < th ( ) 25.0 ( ) 96.0 ( ) Kurtosis > ( ) 65.0 ( ) 56.0.( ) Skewness > ( ) 80.0 ( ) 52.0 ( ) b Histogram K app Mean ( ) 70.0 ( ) 60.0 ( ) Median ( ) 70.0 ( ) 60.0 ( ) th ( ) 70.0 ( ) 64.0 ( ) th > ( ) 65.0 ( ) 60.0 ( ) Kurtosis > ( ) 70.0 ( ) 68.0 ( ) Skewness ( ) 35.0 ( ) ( ) a Unit of mm 2 /s for ADC and D app. b Unit of for K app ; ADC: apparent diffusion coefficient; D app : apparent diffusion parameter; K app : apparent kurtosis coefficient; AUC: area under curve. regular balance between the extracellular and cellular fractions, leading to higher restriction of water diffusion. 23 ADC 10th values showed similar behavior, which was significantly lower in the lesions with distant metastasis. However, regarding the comparison of the ADC from a standard DWI model and D app from DKI model, we demonstrated improved goodness of D app for discriminating distant metastasis. The higher AUC and specificity with the DKI model than that with the standard DWI model can be attributed to the following reasons. First, one limitation of the standard DWI model includes the assumption that water diffusion follows Gaussian behavior, whereas the DKI model incorporates an attempt to depict water diffusion as a non-gaussian phenomenon. Second, the cellular microstructure is more complex and heterogeneous in high-grade malignant tumors than low-grade tumors. Third, vigorous cell mitosis and strong proliferative ability in malignancy can increase the cell density in each voxel and then affect water diffusion. The results of this study also imply that parameters derived from DKI may serve as an effective image-based indicator in the differentiation of T stages. As expected, an inverse correlation between D app and T stage and positive correlation between kurtosis of K app and T stage were observed in this study. However, the present study did not find significant correlation between tumor histological differentiation grades and lymph node metastasis with parameters. These findings are partially consistent with those reported by Sun et al. 24 The inconsistent results between the reported studies may be due to the small sample size. The present study was limited by a small number of welldifferentiated carcinomas. Preoperative identification of distant metastasis is important because the outcome of such patients is worse. 9 This finding affects treatment decision-making. Patients with synchronous distant metastasis should undergo different treatment, such as neoadjuvant chemotherapy or metastasectomy. 25 July

8 Journal of Magnetic Resonance Imaging Recent studies indicated a role for induction chemotherapy in patients with locally advanced rectal carcinoma as an alternative to preoperative chemoradiation, because it can eradicate micrometastasis by the delivery of a full systemic dose. 10,26 Although the ability of high-resolution (HR) MRI to detect the poor prognostic factors in rectal cancer is well documented The information provided by HR MRI includes 1) the potential involvement of the circumferential resection margin (CMR), 2) depth of tumor spread beyond the muscularis propria, 3) nodal status, and 4) the presence of extramural vascular invasion. 30,31 The prediction of distant metastases remains a challenge. This study might help to provide new information beyond the anatomic description of the images. Based on conventional MRI, the assessment of extramural depth of tumor were associated with a more aggressive tumor profile in patients with rectal carcinoma. 29,32 However, these studies did not mention the value of extramural depth of tumor in predicting potential distant metastases. MRI-detected extramural vascular invasion (EMVI) is an independent risk factor for synchronous metastasis. 33 Another study proposed that MRI-detected EMVI is associated with an increased risk of developing metachronous metastases within 1 year of diagnosis. 34 It was consistent with the hypothesis that undiagnosed micrometastases may exist at the time of initial staging of EMVI-positive rectal tumors. 35,36 The comparison of the ability between ADC, D app, K app, and EMVI to predict distant metastasis was not discussed in this study. It is well known that lesions are not homogeneous, even within the same histological type. The quantitative metrics derived from standard DWI and DKI in this study demonstrated this phenomenon. The histogram indices 90th percentile ADC (ADC 90th ) was inversely higher in the lesions with distant metastasis. The histogram indices 10th percentile K app (K app-10th ) were inversely lower in the lesions with distant metastasis. A possible explanation is that rectal carcinoma processes display large heterogeneity. Intratumoural heterogeneity of proliferation has been assessed and diversity within tumors has been demonstrated in terms of morphology and differentiation. 37 In addition, the histogram indices of minimum and maximum may be more subject to measuring errors. The subtle variations in ROI size and ROI positioning may result in substantial variations. Our study had several limitations. First, the correlation of standard DWI and DKI with metachronous distant metastasis remains an uncertain area. Among the screened patients, there were only four patients with metachronous distant metastasis. The size of this subgroup was not enough for statistical analysis. However, early prediction of synchronous metastasis has great value for treatment decisionmaking. Second, the inclusion criteria may have applied a selection bias because the sample did not represent all patients who did not meet these criteria, either because they did not have an MRI for initial staging or because they were lost to CT follow-up. Third, not all of the distant metastases detected in our study were pathologically proven. Some hepatic or lung lesions were diagnosed on the basis of the imaging findings and follow-up results for the lesions in patients who were determined to be unsuitable for resection after their study enrollment. As the pathologic confirmation of all focal metastasis lesions for research purposes would not be practical or ethical, this limitation may have been unavoidable in our study. In conclusion, we observed that DKI can discriminate rectal carcinoma with distant metastasis from those without distant metastasis. In addition, compared with standard DWI, DKI was relatively better. The use of DKI in rectal carcinoma may provide a means of improving the ability to predict which patients are at risk of early distant metastasis. Therefore, this information is available preoperatively for multidisciplinary team discussion and could be used to guide alternative treatment strategies. Acknowledgments We thank Yu-Dong Zhang for technical support and Wei Shen for assistance in data statistical analysis. References 1. Samee A, Selvasekar CR. Current trends in staging rectal cancer. World J Gastroenterol 2011;17: Dewhurst C, Rosen MP, Blake MA, et al. ACR appropriateness criteria pretreatment staging of colorectal cancer. J Am Coll Radiol 2012;9: Heald RJ, Ryall RD. Recurrence and survival after total mesorectal excision for rectal cancer. Lancet 1986;1: Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med 2004;351: Bosset JF, Collette L, Calais G, et al. Chemotherapy with preoperative radiotherapy in rectal cancer. N Engl J Med 2006;355: Braendengen M, Tveit KM, Berglund A, et al. Randomized phase III study comparing preoperative radiotherapy with chemoradiotherapy in nonresectable rectal cancer. J Clin Oncol 2008;26: Gerard JP, Conroy T, Bonnetain F, et al. Preoperative radiotherapy with or without concurrent fluorouracil and leucovorin in T3-4 rectal cancers: results of FFCD J Clin Oncol 2006;24: Peeters KC, Marijnen CA, Nagtegaal ID, et al. The TME trial after a median follow-up of 6 years: increased local control but no survival benefit in irradiated patients with resectable rectal carcinoma. Ann Surg 2007;246: Engelen SM, Maas M, Lahaye MJ, et al. 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9 Yu et al.: Metastases Prediction by Standard DWI and DKI 11. Nogueira L, Brandao S, Matos E, et al. Application of the diffusion kurtosis model for the study of breast lesions. Eur Radiol 2014;24: Shen G, Hu S, Deng H, Kuang A. Performance of DWI in the nodal characterization and assessment of lung cancer: a meta-analysis. AJR Am J Roentgenol 2015: Mizukami Y, Ueda S, Mizumoto A, et al. Diffusion-weighted magnetic resonance imaging for detecting lymph node metastasis of rectal cancer. World J Surg 2011;35: Cho EY, Kim SH, Yoon JH, et al. Apparent diffusion coefficient for discriminating metastatic from non-metastatic lymph nodes in primary rectal cancer. Eur J Radiol 2013;82:e662 e Heijnen LA, Lambregts DM, Mondal D, et al. Diffusion-weighted MR imaging in primary rectal cancer staging demonstrates but does not characterise lymph nodes. Eur Radiol 2013;23: Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K. Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 2005;53: Lu H, Jensen JH, Ramani A, Helpern JA. Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed 2006;19: Quentin M, Pentang G, Schimmoller L, et al. Feasibility of diffusional kurtosis tensor imaging in prostate MRI for the assessment of prostate cancer: preliminary results. Magn Reson Imaging 2014;32: Rosenkrantz AB, Sigmund EE, Johnson G, et al. Prostate cancer: feasibility and preliminary experience of a diffusional kurtosis model for detection and assessment of aggressiveness of peripheral zone cancer. Radiology 2012;264: Tamura C, Shinmoto H, Soga S, et al. Diffusion kurtosis imaging study of prostate cancer: preliminary findings. J Magn Reson Imaging 2014; 40: Raab P, Hattingen E, Franz K, Zanella FE, Lanfermann H. Cerebral gliomas: diffusional kurtosis imaging analysis of microstructural differences. Radiology 2010;254: Van Cauter S, Veraart J, Sijbers J, et al. Gliomas: diffusion kurtosis MR imaging in grading. Radiology 2012;263: Banyard J, Bielenberg DR. The role of EMT and MET in cancer dissemination. Connect Tissue Res 2015;56: Sun K, Chen X, Chai W, et al. Breast cancer: diffusion kurtosis MR imaging-diagnostic accuracy and correlation with clinical-pathologic factors. Radiology 2015;277: Sauer R, Liersch T, Merkel S, 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. J Clin Oncol 2012;30: Glynne-Jones R, Anyamene N, Moran B, Harrison M. Neoadjuvant chemotherapy in MRI-staged high-risk rectal cancer in addition to or as an alternative to preoperative chemoradiation? Ann Oncol 2012; 23: Brown G, Radcliffe AG, Newcombe RG, Dallimore NS, Bourne MW, Williams GT. Preoperative assessment of prognostic factors in rectal cancer using high-resolution magnetic resonance imaging. Br J Surg 2003;90: Smith NJ, Shihab O, Arnaout A, Swift RI, Brown G. MRI for detection of extramural vascular invasion in rectal cancer. AJR Am J Roentgenol 2008;191: Extramural depth of tumor invasion at thin-section MR in patients with rectal cancer: results of the MERCURY study. Radiology 2007;243: Smith N, Brown G. Preoperative staging of rectal cancer. Acta Oncol 2008;47: Cervantes A, Rosello S, Rodriguez-Braun E, et al. Progress in the multidisciplinary treatment of gastrointestinal cancer and the impact on clinical practice: perioperative management of rectal cancer. Ann Oncol 2008;19(Suppl 7):i266 i Tong T, Yao Z, Xu L, et al. Extramural depth of tumor invasion at thinsection MR in rectal cancer: associating with prognostic factors and ADC value. J Magn Reson Imaging 2014;40: Sohn B, Lim JS, Kim H, et al. MRI-detected extramural vascular invasion is an independent prognostic factor for synchronous metastasis in patients with rectal cancer. Eur Radiol 2015;25: Bugg WG, Andreou AK, Biswas D, Toms AP, Williams SM. The prognostic significance of MRI-detected extramural venous invasion in rectal carcinoma. Clin Radiol 2014;69: Ouchi K, Sugawara T, Ono H, et al. Histologic features and clinical significance of venous invasion in colorectal carcinoma with hepatic metastasis. Cancer Am Cancer Soc 1996;78: Brown G. Thin section MRI in multidisciplinary pre-operative decision making for patients with rectal cancer. Br J Radiol 2005;78(Spec No 2):S117 S Leibovitz A, Stinson JC, McCombs WR, McCoy CE, Mazur KC, Mabry ND. Classification of human colorectal adenocarcinoma cell lines. Cancer Res 1976;36: July

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