bs_bs_banner
Journal of Digestive Diseases 2014; 15; 188–194
doi: 10.1111/1751-2980.12124
Original article
T staging of rectal cancer: Accuracy of diffusion-weighted imaging compared with T2-weighted imaging on 3.0 tesla MRI Qi FENG, Yun Qi YAN, Jiong ZHU & Jian Rong XU Department of Radiology, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
OBJECTIVE: To evaluate the performance of diffusion-weighted imaging (DWI) in the T staging of primary rectal cancer compared with T2-weighted (T2W) fast spin-echo imaging using 3.0 tesla magnetic resonance imaging (MRI). METHODS: In total, 46 consecutive patients with rectal cancer who underwent MRI examination before surgery were included in the study. The diagnostic accuracy, sensitivity and specificity of DWI and T2W imaging (T2WI) for T staging of the tumors were evaluated, and interobserver agreement between the two radiologists was calculated. RESULTS: The diagnostic accuracies of DWI and T2WI for the T staging of rectal cancer were 73.9% and 71.7%, respectively. The sensitivity and specificity of KEY WORDS: diffusion-weighted imaging, neoplasm staging, sensitivity and specificity.
DWI were 90.0% and 88.9% for diagnosing T1 tumors, 64.3% and 87.5% for T2 tumors, 77.8% and 89.3% for T3 tumors and 50.0% and 97.6% for T4 tumors, respectively; while the sensitivity and specificity of T2WI were 80.0% and 91.7% for T1 tumors, 64.3% and 78.1% for T2 tumors, 77.8% and 89.3% for T3 tumors and 50.0% and 100% for T4 tumors, respectively. There were no significant differences in the diagnostic accuracy, sensitivity or specificity between DWI and T2WI no matter what kind of T stage was concerned (P > 0.05). The interobserver agreement was 0.74 for DWI and 0.63 for T2WI. CONCLUSIONS: DWI can be applied as a useful tool for evaluating the T staging of rectal cancer. The interobserver agreement obtained by using DWI is better than that obtained by using T2WI.
magnetic
resonance
imaging,
rectal
neoplasms,
INTRODUCTION Correspondence to: Jian Rong XU, Department of Radiology, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, 1630 Dongfang Road, Shanghai 200127, China. Email: [email protected] Conflict of interest: None. © 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
188
Over the past decades, magnetic resonance imaging (MRI) has proven to be one of the most accurate staging modalities for primary rectal cancer, especially with phased array coils for bulky T3 and T4 stage tumors.1,2 The T2-weighted imaging (T2WI), fast spin-echo (FSE) or turbo spin-echo sequence has been recommended, especially with a highresolution, small field of view (FOV) and thin slice,
Journal of Digestive Diseases 2014; 15; 188–194
T staging of rectal cancer using DWI
for the local T staging of rectal cancer. With the utility of MRI it is possible to precisely evaluate the tumor itself and its relationship with the mesorectal fascia and other pelvic organs.3 The accuracy of MRI on the T staging of rectal cancer ranges from 67% to 83%, mainly depending on the difficulty in differentiating between T1 and T2 tumors as well as the desmoplastic response of some tumors that might lead to a misdiagnosis of T2 tumors as T3 tumors.4 Nowadays, neoadjuvant chemotherapy and radiotherapy before surgery are crucial for the treatment of rectal cancer. Over-staging of rectal tumors may lead to the overtreatment of patients with T1 or T2 tumors, with an increased risk for therapy-related morbidity and mortality.5
PATIENTS AND METHODS
It has been concluded that gadolinium-enhanced MRI sequences would not improve the diagnostic accuracy for the assessment of tumor penetration through the rectal wall and tumor extension into mesorectal fascia.6 Diffusion-weighted imaging (DWI) explores the random motion of water molecules in the human body and provides qualitative and quantitative information that reflect tissue cellularity and cell membrane integrity.7 It has been increasingly applied for the oncological diagnosis attributed to its ability to detect and characterize tumors. The role of DWI lies mainly in monitoring the response to neoadjuvant radiochemotherapy in primary rectal cancer.8,9 This, however, does not help in treating patients individually.10
MRI
In this study, we aimed to evaluate the possibility of using DWI alone in the local T staging of primary rectal cancer, depending on its radiological features, compared with T2-weighted fast spin-echo imaging using 3.0 tesla (3.0T) MRI scanner.
Table 1.
189
Patients From November 2010 to September 2012, consecutive patients with rectal cancer were enrolled in this study. Exclusion criteria were: (i) patients who had undergone concurrent chemotherapy or radiotherapy before surgery; (ii) those with tumor metastasis including pelvis and/or liver metastasis; and (iii) those who had sigmorectal surgery with implantation of metal anastomat. The study was approved by the Institutional Review Board of Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University and written informed consent was obtained from each patient.
MRI examination of all the patients was performed with GE Signa EXCITE 3.0T MRI scanner (GE HealthCare, Milwaukee, WI, USA). All patients had bowel preparation before the MRI examination. Scopolamine 10 mg (Shanghai Xinyi Pharmaceuticals Co., Ltd., Shanghai, China) was administered intramuscularly 10 min before the scan and all patients were placed in the supine position. After acquiring standard three-plane scout images, the following sequences were obtained for the pelvis using an 8-channel body phased array coil (Table 1). No respiratory triggering technique was required. The acquisition time of the whole examination for each patient was approximately 25 min. Image analysis All images were evaluated by two radiologists (with 8-year and 3-year experiences, respectively) who were
Magnetic resonance imaging (MRI) sequences and parameters
Sequence Axial T2W FSE Coronal T2W FSE Sagital T2W FSE with fat suppression Axial T1W FSE DWI (EPI)
TR (ms)
TE (ms)
TI (ms)
Slice thickness (mm)
Gap (mm)
FOV
b value (s/mm2)
4940 4700 4320
130 113 105.4
– – –
4 4 6
1 1 1
28 × 28 30 × 30 28 × 28
– – –
580 5950
7.2 77.8
– –
4 4
1 1
28 × 28 28 × 28
– 1500
DWI, diffusion-weighted imaging; EPI, echo planar imaging; FOV, field of view; FSE, fast spin-echo; T1W, T1-weighted; T2W, T2-weighted; TE, echo time; TI, inversion time; TR, repetition time.
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
190 Table 2.
Q Feng et al.
Journal of Digestive Diseases 2014; 15; 188–194
T staging of rectal cancer in diffusion-weighted imaging (DWI) compared with histopathology DWI (reader 1)
DWI (reader 2)
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
8 3 1 0 80.0 88.9
2 9 2 0 64.3 87.5
0 2 14 2 77.8 85.7
0 0 1 2 50.0 97.6
9 3 2 0 90.0 86.1
1 9 2 1 64.3 87.5
0 2 13 1 72.2 89.3
0 0 1 2 50.0 97.6
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
blinded to the clinical and histopathological characteristics of the patients (obtained from the AW4.2 Workstation [GE HealthCare]). When comparing the T staging of rectal tumors between the two imaging protocols, DWI and T2WI, interobserver agreement of these two radiologists was calculated. In the DWI sequence the lesion was identified when its signal intensity (SI) was definitely higher than that in the normal-appearing loops on DWI but showed a low SI on the apparent diffusion coefficient (ADC) map; while in the other sequences the lesion was marked when the rectal wall was found to be thickened or a nodal protuberance was found to be inside the bowel cavity and SI was lower on the T1-weighted (T1W) images but higher on the T2-weighted (T2W) images with or without fat suppression. Rectal cancer was classified into four categories (T1 to T4) based on the TNM Classification of Malignant Tumours (conducted by Union for International Cancer Control [UICC]).11 The diagnostic criteria of T staging of rectal tumor using DWI were: (i) T1 or lower, lesions with a high SI and a low SI stalk or thickened component; (ii) T2, lesions with a high SI in the absence of a low SI stalk or thickened component but having a low SI margin; (iii) T3, lesions with a high SI invading the whole rectal wall or extending into the perirectal fat; and (iv) T4, tumor invasion into adjacent organs. The criteria of tumor T staging using T2WI were based on those established by Brown et al.12: (i) T1, low signal restricted in the submucosal layer, not extending into the muscle coat; (ii) T2, intermediate SI within the muscularis propria; (iii) T3, broad-based bulge or nodular projection or intermediate SI projecting beyond the outer muscle coat; and (iv) T4, an extension of abnormal signal into the adjacent organs.
Statistical analysis Statistical analyses were performed using SPSS 11.5 (SPSS Inc., Chicago, IL, USA). Categorical variables were expressed as frequencies or percentages. κ values were calculated to determine interobserver agreement (0–0.20, poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, good agreement; 0.81–1.00, excellent agreement). Differences in diagnostic accuracy, sensitivity and specificity for each image set were evaluated with the χ2 test. P ≤ 0.05 was considered to be statistically significant. RESULTS Altogether 46 patients (28 men and 18 women) who were diagnosed as stage I or II rectal cancer according to the TNM stage were evaluated, consisting of those with tubular-papillary adenocarcinoma (n = 19), tubular adenocarcinoma (n = 22) and papillary adenocarcinoma (n = 5). The T staging of the tumors evaluated by the two radiologists using DWI and T2WI are shown in Tables 2 and 3, respectively. With DWI, there were no significant differences in the diagnostic sensitivity (T1: χ2 = 0.697, P = 0.404; T2: χ2 = 0, P = 1.000; T3: χ2 = 0.148, P = 0.700; T4: χ2 = 0, P = 1.000) or specificity (T1: χ2 = 0.127, P = 0.722; T2: χ2 = 0, P = 1.000; T3: χ2 = 0.163, P = 0.686; T4: χ2 = 0, P = 1.000) between the two observers. With T2WI, there were also no significant differences in the diagnostic sensitivity (T1: χ2 = 0.952, P = 0.329; T2: χ2 = 0.583, P = 0.445; T3: χ2 = 0.148, P = 0.700; T4: χ2 = 0, P = 1.000) or specificity (T1: χ2 = 0, P = 1.000; T2: χ2 = 0.097, P = 0.756; T3: χ2 = 0.487, P = 0.485; T4: χ2 = 0, P = 1.000). The diagnostic accuracies of DWI and T2WI for T staging of rectal cancer were 73.9% and 71.7%,
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 188–194 Table 3.
T staging of rectal cancer using DWI
191
Tumor staging of rectal cancer in T2-weighted imaging (T2WI) imaging compared with histopathology T2WI (reader 1)
T2WI (reader 2)
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
8 3 0 0 80.0 91.7
2 7 4 0 50.0 81.3
0 4 13 2 72.2 78.6
0 0 1 2 50.0 97.6
6 2 1 0 60.0 91.7
4 9 2 1 64.3 78.1
0 3 14 1 77.8 85.7
0 0 1 2 50.0 97.6
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
Table 4.
Tumor staging of rectal cancer in T2-weighted imaging (T2WI) compared with diffusion-weighted imaging (DWI) DWI
T2WI
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
9 3 1 0 90.0 88.9
1 9 2 1 64.3 87.5
0 2 14 1 77.8 89.3
0 0 1 2 50.0 97.6
8 3 0 0 80.0 91.7
2 9 4 1 64.3 78.1
0 2 14 1 77.8 89.3
0 0 0 2 50.0 100
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
respectively, with no significant difference (χ2 = 0.055, P = 0.815) (Table 4). The sensitivity of DWI and T2WI was similar for T1 tumors (χ2 = 0.392, P = 0.0.531) and exactly the same for T2 to T4 tumors. There were also no significant differences in the specificities obtained using T2WI or DWI, no matter what kind of T-stage tumor was concerned (T1: χ2 = 0.158, P = 0.691; T2: χ2 = 0.988, P = 0.320; T3: χ2 = 0, P = 1.0000; T4: χ2 = 1.000, P = 0.317) (Figs 1 to 3).
nation of tumor aggressiveness.19 However, there are few reports of T staging of rectal cancer based on the radiological features on DWI.
Interobserver agreement was good (κ = 0.74) and moderate (κ = 0.63) for DWI and T2WI, respectively.
It was believed that a desmoplastic fibrotic response was difficult to differentiate from perirectal tumor on T2W images. The microvessels or reactive tissues adjacent to the tumor could be enhanced to a level which is similar to that of the cancerous components and thus it is difficult to differentiate them even on contrast-enhanced images, but they could be distinguished on DWI where the SI of these vessels or tissues could be suppressed. Although the sensitivity of DWI and T2WI for diagnosing T2 tumors was exactly the same, the specificity of DWI might be higher than that of T2WI if more cases were included. It has been suggested that tumor contour could be evaluated more accurately using DWI, and DWI might be able to differentiate T2 from borderline T3 tumor more easily than T2WI.
DISCUSSION MRI has become one of the most accurate staging modalities for primary rectal cancer, with an reported diagnostic accuracy of no higher than 88%.13–16 The diagnostic performance for T staging of the tumor is not improved even using a 3.0T MRI scanner, with the sensitivity from 29% to 57% and specificity from 50% to 83%. Moreover, its diagnostic sensitivity and specificity have also been shown to be largely dependent on the experiences of the radiologists.3 It is also suggested that DWI, a functional MRI sequence, often plays an important role in monitoring the response to neoadjuvant radiochemotherapy or tumor recurrence.17,18 The ADC values are helpful for the determi-
In our study, the diagnostic accuracy of DWI was similar to that of T2WI in the absence of significant difference between their diagnostic specificity or sensitivity of the two sequences, suggesting that DWI could also be used in the T staging of rectal cancer.
In this study, some characteristic appearances of T1 tumor could be found on DWI such as C-shaped
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
192
Q Feng et al.
Journal of Digestive Diseases 2014; 15; 188–194
(a)
(a)
(b)
(b)
(c) (c)
Figure 1. T1 stage rectal adenocarcinoma in a 56-year-old woman. (a) Axial T2-weighted imaging (T2WI) showing protruding mass (arrow) on the left rectal wall. (b) Diffusion-weighted imaging (DWI) showing a C-shaped area of high signal intensity (SI) with a low SI stalk connecting to the left rectal wall. (c) Histopathology showing that the tumor invades the submucosal layer of the rectal wall consisting of fibrous tissue and inflammatory cell infiltration (HE stain, ×100).
Figure 2. T2 stage rectal adenocarcinoma in a 45-yearold woman. (a) Axial T2-weighted imaging (T2WI) showing localized thickening of posterior rectal wall (arrow). (b) Diffusion-weighted imaging (DWI) showing an area of high signal intensity (SI) with a low-SI intact rectal wall margin. (c) Histopathology showing that the tumor invades the muscular layer of the rectal wall (HE stain, ×100).
high signal intensity structure with low signal intensity stalk. According to the research on urinary bladder cancer by Takeuchi et al.,20 T1 stage and even lower bladder cancer had a similar finding on DWI. Saito et al.21 have suggested that the stalk extending
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 188–194 (a)
T staging of rectal cancer using DWI
193
Figure 3. T3 stage rectal adenocarcinoma in a 78-year-old man. (a) Axial T2-weighted imaging (T2WI) showing localized circular thickening of the rectal wall (arrows). (b) Diffusion-weighted imaging (DWI) showing that a high signal intensity (SI) tumor invades the whole rectal wall without low SI structure. The extraluminal extension of the left posterior wall is observed on T2WI while on DWI this phenomenon disappears, indicating a desmoplastic fibrotic response. (c) Histopathology showing that the tumor invades the serosa of the rectal wall (HE stain, ×100).
◀
(b)
(c)
from the urinary bladder wall to the center of T1 tumor consists of fibrous tissues, capillaries, inflammatory cells and edema. Takeuchi et al.20 also reported a similar mixture of edematous submucosa, fibrous tissues, capillaries and mild inflammatory cell infiltration. It is postulated that the reactive inflammation and edema lift the tumor and form the stalk. In our patients, obvious fibrous tissues and inflammatory cell infiltration could also be detected in pathological specimens. The wall structure of the rectum and bladder has four similar layer structures: mucosa, submucosa, muscularis and serosa, which might be the reason why a similar radiological appearance can also be found in T1 rectal cancer. Although most rectal cancers can be staged correctly using T2WI, even if a high-spatial resolution is applied with the new generation of phased array coils, it appears to be relatively poor to distinguishing T1 from T2 tumors.10,22 Thus, diagnosis mainly depends on the experiences of the radiologists. However, with DWI tumors can be staged mainly according to the characteristic MRI manifestations rather than the SI changes of different rectal wall structures, which might indicate that the accuracy of these results seldom depends on the experiences of the radiologists. Our study confirmed that two radiologists could achieve better interobserver agreements using DWI. In order to achieve the best overall assessment of rectal cancer, its extension along the nerves and extramural intravascular growth, for example, can be occasionally identified on T2WI instead of DWI because of the relatively poor image quality of DWI.22,23 DWI could not therefore replace T2WI for the evaluation of rectal cancer, especially those with high-spatial resolution, but it could be adopted as a useful supplementary tool for evaluating the T stage of the tumors, particularly for differentiating T1 or T2 tumors from those at T3 and T4 stages. Our study had several limitations. First of all, the tumors were divided into only four grades, whereas
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
194
Q Feng et al.
some investigators have classified them into five or more groups. In addition, the distribution of tumors at different T stages was uneven. Nearly half of these patients had a T3 tumor and the other half had T1 and T2 tumors. Therefore, studies with large sample sizes on DWI alone in the T staging of rectal cancer are required in the future. We discussed only the utility of DWI in the T staging of rectal cancer, but its role in differentiating polypoid adenomas from T1 stage adenocarcinomas remains unknown. In addition, similar scanning FOV, slice thickness and gap were adopted in our study in order to make the DWI and T2WI more comparable, which might be the reason why the diagnosis of T staging using T2WI was less accurate than that mentioned in many published studies. In conclusion, DWI could be applied as a useful tool for the T staging of rectal cancer, the decision for treatment regimens as well as for the follow-up of the patients. The interobserver agreement using DWI was better than that obtained by using T2WI. ACKNOWLEDGMENT The authors thank Qing LU and He WANG for regulating the MRI sequences in this study. The study was supported by the National Basic Research Program of China (no. 2012CB932600) and Shanghai Leading Academic Discipline Project (no. S30203). REFERENCES 1 Valentini V, Aristei C, Glimelius B et al; Scientific Committee. Multidisciplinary rectal cancer management: 2nd European Rectal Cancer Consensus Conference (EURECA-CC2). Radiother Oncol 2009; 92: 148–63. 2 Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker J. Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging – a meta-analysis. Radiology 2004; 232: 773–83. 3 Klessen C, Rogalla P, Taupitz M. Local staging of rectal cancer: the current role of MRI. Eur Radiol 2007; 17: 379–89. 4 Sethi R, Lee SH. Imaging in colorectal cancer. In: Brown SR, Hartley JE, Hill J, Scott N, Williams G, eds. Contemporary Coloproctology. London: Springer, 2012; 123–38. 5 Maas M, Lambregts DM, Lahaye MJ et al. T-staging of rectal cancer: accuracy of 3.0 Tesla MRI compared with 1.5 Tesla. Abdom Imaging 2012; 37: 475–81. 6 Vliegen RF, Beets GL, von Meyenfeldt MF et al. Rectal cancer: MR imaging in local staging – is gadolinium-based contrast material helpful? Radiology 2005; 234: 179–88. 7 Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 2007; 188: 1622–35.
Journal of Digestive Diseases 2014; 15; 188–194 8 Dzik-Jurasz A, Domenig C, George M et al. Diffusion MRI for prediction of response of rectal cancer to chemoradiation. Lancet 2002; 360: 307–8. 9 Hein PA, Kremser C, Judmaier W et al. Diffusion-weighted magnetic resonance imaging for monitoring diffusion changes in rectal carcinoma during combined, preoperative chemoradiation: preliminary results of a prospective study. Eur J Radiol 2003; 45: 214–22. 10 Torkzad MR, Påhlman L, Glimelius B. Magnetic resonance imaging (MRI) in rectal cancer: a comprehensive review. Insights Imaging 2010; 1: 245–67. 11 International Union Against Cancer (UICC). TNM Classification of Malignant Tumours, 7th eds. Sobin LH, Gospodarowicz MK, Wittekind C, eds. New York: Wiley; 2010. 12 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: 355–64. 13 Rovera F, Dionigi G, Boni L, Cutaia S, Diurni M, Dionigi R. The role of EUS and MRI in rectal cancer staging. Surg Oncol 2007; 16 Suppl 1: S51–2. 14 Suzuki C, Torkzad MR, Tanaka S et al. The importance of rectal cancer MRI protocols on interpretation accuracy. World J Surg Oncol 2008; 6: 89. 15 Torkzad MR, Hansson KA, Lindholm J, Martling A, Blomqvist L. Significance of mesorectal volume in staging of rectal cancer with magnetic resonance imaging and the assessment of involvement of the mesorectal fascia. Eur Radiol 2007; 17: 1694–9. 16 Videhult P, Smedh K, Lundin P, Kraaz W. Magnetic resonance imaging for preoperative staging of rectal cancer in clinical practice: high accuracy in predicting circumferential margin with clinical benefit. Colorectal Dis 2007; 9: 412–9. 17 Jang KM, Kim SH, Choi D, Lee SJ, Park MJ, Min K. Pathological correlation with diffusion restriction on diffusion-weighted imaging in patients with pathological complete response after neoadjuvant chemoradiation therapy for locally advanced rectal cancer: preliminary results. Br J Radiol 2012; 85: e566–72. 18 Lambregts DM, Cappendijk VC, Maas M, Beets GL, Beets-Tan RG. Value of MRI and diffusion-weighted MRI for the diagnosis of locally recurrent rectal cancer. Eur Radiol 2011; 21: 1250–8. 19 Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG. Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging 2012; 35: 1365–71. 20 Takeuchi M, Sasaki S, Ito M et al. Urinary bladder cancer: diffusion-weighted MR imaging – accuracy for diagnosing T stage and estimating histologic grade. Radiology 2009; 251: 112–21. 21 Saito W, Amanuma M, Tanaka J, Heshiki A. Histopathological analysis of a bladder cancer stalk observed on MRI. Magn Reson Imaging 2000; 18: 411–5. 22 Gagliardi G, Bayar S, Smith R, Salem RR. Preoperative staging of rectal cancer using magnetic resonance imaging with external phase-arrayed coils. Arch Surg 2002; 137: 447–51. 23 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: 1517–22.
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 188–194
doi: 10.1111/1751-2980.12124
Original article
T staging of rectal cancer: Accuracy of diffusion-weighted imaging compared with T2-weighted imaging on 3.0 tesla MRI Qi FENG, Yun Qi YAN, Jiong ZHU & Jian Rong XU Department of Radiology, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China
OBJECTIVE: To evaluate the performance of diffusion-weighted imaging (DWI) in the T staging of primary rectal cancer compared with T2-weighted (T2W) fast spin-echo imaging using 3.0 tesla magnetic resonance imaging (MRI). METHODS: In total, 46 consecutive patients with rectal cancer who underwent MRI examination before surgery were included in the study. The diagnostic accuracy, sensitivity and specificity of DWI and T2W imaging (T2WI) for T staging of the tumors were evaluated, and interobserver agreement between the two radiologists was calculated. RESULTS: The diagnostic accuracies of DWI and T2WI for the T staging of rectal cancer were 73.9% and 71.7%, respectively. The sensitivity and specificity of KEY WORDS: diffusion-weighted imaging, neoplasm staging, sensitivity and specificity.
DWI were 90.0% and 88.9% for diagnosing T1 tumors, 64.3% and 87.5% for T2 tumors, 77.8% and 89.3% for T3 tumors and 50.0% and 97.6% for T4 tumors, respectively; while the sensitivity and specificity of T2WI were 80.0% and 91.7% for T1 tumors, 64.3% and 78.1% for T2 tumors, 77.8% and 89.3% for T3 tumors and 50.0% and 100% for T4 tumors, respectively. There were no significant differences in the diagnostic accuracy, sensitivity or specificity between DWI and T2WI no matter what kind of T stage was concerned (P > 0.05). The interobserver agreement was 0.74 for DWI and 0.63 for T2WI. CONCLUSIONS: DWI can be applied as a useful tool for evaluating the T staging of rectal cancer. The interobserver agreement obtained by using DWI is better than that obtained by using T2WI.
magnetic
resonance
imaging,
rectal
neoplasms,
INTRODUCTION Correspondence to: Jian Rong XU, Department of Radiology, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, 1630 Dongfang Road, Shanghai 200127, China. Email: [email protected] Conflict of interest: None. © 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
188
Over the past decades, magnetic resonance imaging (MRI) has proven to be one of the most accurate staging modalities for primary rectal cancer, especially with phased array coils for bulky T3 and T4 stage tumors.1,2 The T2-weighted imaging (T2WI), fast spin-echo (FSE) or turbo spin-echo sequence has been recommended, especially with a highresolution, small field of view (FOV) and thin slice,
Journal of Digestive Diseases 2014; 15; 188–194
T staging of rectal cancer using DWI
for the local T staging of rectal cancer. With the utility of MRI it is possible to precisely evaluate the tumor itself and its relationship with the mesorectal fascia and other pelvic organs.3 The accuracy of MRI on the T staging of rectal cancer ranges from 67% to 83%, mainly depending on the difficulty in differentiating between T1 and T2 tumors as well as the desmoplastic response of some tumors that might lead to a misdiagnosis of T2 tumors as T3 tumors.4 Nowadays, neoadjuvant chemotherapy and radiotherapy before surgery are crucial for the treatment of rectal cancer. Over-staging of rectal tumors may lead to the overtreatment of patients with T1 or T2 tumors, with an increased risk for therapy-related morbidity and mortality.5
PATIENTS AND METHODS
It has been concluded that gadolinium-enhanced MRI sequences would not improve the diagnostic accuracy for the assessment of tumor penetration through the rectal wall and tumor extension into mesorectal fascia.6 Diffusion-weighted imaging (DWI) explores the random motion of water molecules in the human body and provides qualitative and quantitative information that reflect tissue cellularity and cell membrane integrity.7 It has been increasingly applied for the oncological diagnosis attributed to its ability to detect and characterize tumors. The role of DWI lies mainly in monitoring the response to neoadjuvant radiochemotherapy in primary rectal cancer.8,9 This, however, does not help in treating patients individually.10
MRI
In this study, we aimed to evaluate the possibility of using DWI alone in the local T staging of primary rectal cancer, depending on its radiological features, compared with T2-weighted fast spin-echo imaging using 3.0 tesla (3.0T) MRI scanner.
Table 1.
189
Patients From November 2010 to September 2012, consecutive patients with rectal cancer were enrolled in this study. Exclusion criteria were: (i) patients who had undergone concurrent chemotherapy or radiotherapy before surgery; (ii) those with tumor metastasis including pelvis and/or liver metastasis; and (iii) those who had sigmorectal surgery with implantation of metal anastomat. The study was approved by the Institutional Review Board of Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University and written informed consent was obtained from each patient.
MRI examination of all the patients was performed with GE Signa EXCITE 3.0T MRI scanner (GE HealthCare, Milwaukee, WI, USA). All patients had bowel preparation before the MRI examination. Scopolamine 10 mg (Shanghai Xinyi Pharmaceuticals Co., Ltd., Shanghai, China) was administered intramuscularly 10 min before the scan and all patients were placed in the supine position. After acquiring standard three-plane scout images, the following sequences were obtained for the pelvis using an 8-channel body phased array coil (Table 1). No respiratory triggering technique was required. The acquisition time of the whole examination for each patient was approximately 25 min. Image analysis All images were evaluated by two radiologists (with 8-year and 3-year experiences, respectively) who were
Magnetic resonance imaging (MRI) sequences and parameters
Sequence Axial T2W FSE Coronal T2W FSE Sagital T2W FSE with fat suppression Axial T1W FSE DWI (EPI)
TR (ms)
TE (ms)
TI (ms)
Slice thickness (mm)
Gap (mm)
FOV
b value (s/mm2)
4940 4700 4320
130 113 105.4
– – –
4 4 6
1 1 1
28 × 28 30 × 30 28 × 28
– – –
580 5950
7.2 77.8
– –
4 4
1 1
28 × 28 28 × 28
– 1500
DWI, diffusion-weighted imaging; EPI, echo planar imaging; FOV, field of view; FSE, fast spin-echo; T1W, T1-weighted; T2W, T2-weighted; TE, echo time; TI, inversion time; TR, repetition time.
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
190 Table 2.
Q Feng et al.
Journal of Digestive Diseases 2014; 15; 188–194
T staging of rectal cancer in diffusion-weighted imaging (DWI) compared with histopathology DWI (reader 1)
DWI (reader 2)
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
8 3 1 0 80.0 88.9
2 9 2 0 64.3 87.5
0 2 14 2 77.8 85.7
0 0 1 2 50.0 97.6
9 3 2 0 90.0 86.1
1 9 2 1 64.3 87.5
0 2 13 1 72.2 89.3
0 0 1 2 50.0 97.6
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
blinded to the clinical and histopathological characteristics of the patients (obtained from the AW4.2 Workstation [GE HealthCare]). When comparing the T staging of rectal tumors between the two imaging protocols, DWI and T2WI, interobserver agreement of these two radiologists was calculated. In the DWI sequence the lesion was identified when its signal intensity (SI) was definitely higher than that in the normal-appearing loops on DWI but showed a low SI on the apparent diffusion coefficient (ADC) map; while in the other sequences the lesion was marked when the rectal wall was found to be thickened or a nodal protuberance was found to be inside the bowel cavity and SI was lower on the T1-weighted (T1W) images but higher on the T2-weighted (T2W) images with or without fat suppression. Rectal cancer was classified into four categories (T1 to T4) based on the TNM Classification of Malignant Tumours (conducted by Union for International Cancer Control [UICC]).11 The diagnostic criteria of T staging of rectal tumor using DWI were: (i) T1 or lower, lesions with a high SI and a low SI stalk or thickened component; (ii) T2, lesions with a high SI in the absence of a low SI stalk or thickened component but having a low SI margin; (iii) T3, lesions with a high SI invading the whole rectal wall or extending into the perirectal fat; and (iv) T4, tumor invasion into adjacent organs. The criteria of tumor T staging using T2WI were based on those established by Brown et al.12: (i) T1, low signal restricted in the submucosal layer, not extending into the muscle coat; (ii) T2, intermediate SI within the muscularis propria; (iii) T3, broad-based bulge or nodular projection or intermediate SI projecting beyond the outer muscle coat; and (iv) T4, an extension of abnormal signal into the adjacent organs.
Statistical analysis Statistical analyses were performed using SPSS 11.5 (SPSS Inc., Chicago, IL, USA). Categorical variables were expressed as frequencies or percentages. κ values were calculated to determine interobserver agreement (0–0.20, poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, good agreement; 0.81–1.00, excellent agreement). Differences in diagnostic accuracy, sensitivity and specificity for each image set were evaluated with the χ2 test. P ≤ 0.05 was considered to be statistically significant. RESULTS Altogether 46 patients (28 men and 18 women) who were diagnosed as stage I or II rectal cancer according to the TNM stage were evaluated, consisting of those with tubular-papillary adenocarcinoma (n = 19), tubular adenocarcinoma (n = 22) and papillary adenocarcinoma (n = 5). The T staging of the tumors evaluated by the two radiologists using DWI and T2WI are shown in Tables 2 and 3, respectively. With DWI, there were no significant differences in the diagnostic sensitivity (T1: χ2 = 0.697, P = 0.404; T2: χ2 = 0, P = 1.000; T3: χ2 = 0.148, P = 0.700; T4: χ2 = 0, P = 1.000) or specificity (T1: χ2 = 0.127, P = 0.722; T2: χ2 = 0, P = 1.000; T3: χ2 = 0.163, P = 0.686; T4: χ2 = 0, P = 1.000) between the two observers. With T2WI, there were also no significant differences in the diagnostic sensitivity (T1: χ2 = 0.952, P = 0.329; T2: χ2 = 0.583, P = 0.445; T3: χ2 = 0.148, P = 0.700; T4: χ2 = 0, P = 1.000) or specificity (T1: χ2 = 0, P = 1.000; T2: χ2 = 0.097, P = 0.756; T3: χ2 = 0.487, P = 0.485; T4: χ2 = 0, P = 1.000). The diagnostic accuracies of DWI and T2WI for T staging of rectal cancer were 73.9% and 71.7%,
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 188–194 Table 3.
T staging of rectal cancer using DWI
191
Tumor staging of rectal cancer in T2-weighted imaging (T2WI) imaging compared with histopathology T2WI (reader 1)
T2WI (reader 2)
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
8 3 0 0 80.0 91.7
2 7 4 0 50.0 81.3
0 4 13 2 72.2 78.6
0 0 1 2 50.0 97.6
6 2 1 0 60.0 91.7
4 9 2 1 64.3 78.1
0 3 14 1 77.8 85.7
0 0 1 2 50.0 97.6
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
Table 4.
Tumor staging of rectal cancer in T2-weighted imaging (T2WI) compared with diffusion-weighted imaging (DWI) DWI
T2WI
Histopathology
T1
T2
T3
T4
T1
T2
T3
T4
T1 T2 T3 T4 Sensitivity (%) Specificity (%)
9 3 1 0 90.0 88.9
1 9 2 1 64.3 87.5
0 2 14 1 77.8 89.3
0 0 1 2 50.0 97.6
8 3 0 0 80.0 91.7
2 9 4 1 64.3 78.1
0 2 14 1 77.8 89.3
0 0 0 2 50.0 100
T1 to T4, the T staging of the tumors according to the TNM system of the Union for International Cancer Control.11
respectively, with no significant difference (χ2 = 0.055, P = 0.815) (Table 4). The sensitivity of DWI and T2WI was similar for T1 tumors (χ2 = 0.392, P = 0.0.531) and exactly the same for T2 to T4 tumors. There were also no significant differences in the specificities obtained using T2WI or DWI, no matter what kind of T-stage tumor was concerned (T1: χ2 = 0.158, P = 0.691; T2: χ2 = 0.988, P = 0.320; T3: χ2 = 0, P = 1.0000; T4: χ2 = 1.000, P = 0.317) (Figs 1 to 3).
nation of tumor aggressiveness.19 However, there are few reports of T staging of rectal cancer based on the radiological features on DWI.
Interobserver agreement was good (κ = 0.74) and moderate (κ = 0.63) for DWI and T2WI, respectively.
It was believed that a desmoplastic fibrotic response was difficult to differentiate from perirectal tumor on T2W images. The microvessels or reactive tissues adjacent to the tumor could be enhanced to a level which is similar to that of the cancerous components and thus it is difficult to differentiate them even on contrast-enhanced images, but they could be distinguished on DWI where the SI of these vessels or tissues could be suppressed. Although the sensitivity of DWI and T2WI for diagnosing T2 tumors was exactly the same, the specificity of DWI might be higher than that of T2WI if more cases were included. It has been suggested that tumor contour could be evaluated more accurately using DWI, and DWI might be able to differentiate T2 from borderline T3 tumor more easily than T2WI.
DISCUSSION MRI has become one of the most accurate staging modalities for primary rectal cancer, with an reported diagnostic accuracy of no higher than 88%.13–16 The diagnostic performance for T staging of the tumor is not improved even using a 3.0T MRI scanner, with the sensitivity from 29% to 57% and specificity from 50% to 83%. Moreover, its diagnostic sensitivity and specificity have also been shown to be largely dependent on the experiences of the radiologists.3 It is also suggested that DWI, a functional MRI sequence, often plays an important role in monitoring the response to neoadjuvant radiochemotherapy or tumor recurrence.17,18 The ADC values are helpful for the determi-
In our study, the diagnostic accuracy of DWI was similar to that of T2WI in the absence of significant difference between their diagnostic specificity or sensitivity of the two sequences, suggesting that DWI could also be used in the T staging of rectal cancer.
In this study, some characteristic appearances of T1 tumor could be found on DWI such as C-shaped
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
192
Q Feng et al.
Journal of Digestive Diseases 2014; 15; 188–194
(a)
(a)
(b)
(b)
(c) (c)
Figure 1. T1 stage rectal adenocarcinoma in a 56-year-old woman. (a) Axial T2-weighted imaging (T2WI) showing protruding mass (arrow) on the left rectal wall. (b) Diffusion-weighted imaging (DWI) showing a C-shaped area of high signal intensity (SI) with a low SI stalk connecting to the left rectal wall. (c) Histopathology showing that the tumor invades the submucosal layer of the rectal wall consisting of fibrous tissue and inflammatory cell infiltration (HE stain, ×100).
Figure 2. T2 stage rectal adenocarcinoma in a 45-yearold woman. (a) Axial T2-weighted imaging (T2WI) showing localized thickening of posterior rectal wall (arrow). (b) Diffusion-weighted imaging (DWI) showing an area of high signal intensity (SI) with a low-SI intact rectal wall margin. (c) Histopathology showing that the tumor invades the muscular layer of the rectal wall (HE stain, ×100).
high signal intensity structure with low signal intensity stalk. According to the research on urinary bladder cancer by Takeuchi et al.,20 T1 stage and even lower bladder cancer had a similar finding on DWI. Saito et al.21 have suggested that the stalk extending
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
Journal of Digestive Diseases 2014; 15; 188–194 (a)
T staging of rectal cancer using DWI
193
Figure 3. T3 stage rectal adenocarcinoma in a 78-year-old man. (a) Axial T2-weighted imaging (T2WI) showing localized circular thickening of the rectal wall (arrows). (b) Diffusion-weighted imaging (DWI) showing that a high signal intensity (SI) tumor invades the whole rectal wall without low SI structure. The extraluminal extension of the left posterior wall is observed on T2WI while on DWI this phenomenon disappears, indicating a desmoplastic fibrotic response. (c) Histopathology showing that the tumor invades the serosa of the rectal wall (HE stain, ×100).
◀
(b)
(c)
from the urinary bladder wall to the center of T1 tumor consists of fibrous tissues, capillaries, inflammatory cells and edema. Takeuchi et al.20 also reported a similar mixture of edematous submucosa, fibrous tissues, capillaries and mild inflammatory cell infiltration. It is postulated that the reactive inflammation and edema lift the tumor and form the stalk. In our patients, obvious fibrous tissues and inflammatory cell infiltration could also be detected in pathological specimens. The wall structure of the rectum and bladder has four similar layer structures: mucosa, submucosa, muscularis and serosa, which might be the reason why a similar radiological appearance can also be found in T1 rectal cancer. Although most rectal cancers can be staged correctly using T2WI, even if a high-spatial resolution is applied with the new generation of phased array coils, it appears to be relatively poor to distinguishing T1 from T2 tumors.10,22 Thus, diagnosis mainly depends on the experiences of the radiologists. However, with DWI tumors can be staged mainly according to the characteristic MRI manifestations rather than the SI changes of different rectal wall structures, which might indicate that the accuracy of these results seldom depends on the experiences of the radiologists. Our study confirmed that two radiologists could achieve better interobserver agreements using DWI. In order to achieve the best overall assessment of rectal cancer, its extension along the nerves and extramural intravascular growth, for example, can be occasionally identified on T2WI instead of DWI because of the relatively poor image quality of DWI.22,23 DWI could not therefore replace T2WI for the evaluation of rectal cancer, especially those with high-spatial resolution, but it could be adopted as a useful supplementary tool for evaluating the T stage of the tumors, particularly for differentiating T1 or T2 tumors from those at T3 and T4 stages. Our study had several limitations. First of all, the tumors were divided into only four grades, whereas
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
194
Q Feng et al.
some investigators have classified them into five or more groups. In addition, the distribution of tumors at different T stages was uneven. Nearly half of these patients had a T3 tumor and the other half had T1 and T2 tumors. Therefore, studies with large sample sizes on DWI alone in the T staging of rectal cancer are required in the future. We discussed only the utility of DWI in the T staging of rectal cancer, but its role in differentiating polypoid adenomas from T1 stage adenocarcinomas remains unknown. In addition, similar scanning FOV, slice thickness and gap were adopted in our study in order to make the DWI and T2WI more comparable, which might be the reason why the diagnosis of T staging using T2WI was less accurate than that mentioned in many published studies. In conclusion, DWI could be applied as a useful tool for the T staging of rectal cancer, the decision for treatment regimens as well as for the follow-up of the patients. The interobserver agreement using DWI was better than that obtained by using T2WI. ACKNOWLEDGMENT The authors thank Qing LU and He WANG for regulating the MRI sequences in this study. The study was supported by the National Basic Research Program of China (no. 2012CB932600) and Shanghai Leading Academic Discipline Project (no. S30203). REFERENCES 1 Valentini V, Aristei C, Glimelius B et al; Scientific Committee. Multidisciplinary rectal cancer management: 2nd European Rectal Cancer Consensus Conference (EURECA-CC2). Radiother Oncol 2009; 92: 148–63. 2 Bipat S, Glas AS, Slors FJ, Zwinderman AH, Bossuyt PM, Stoker J. Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging – a meta-analysis. Radiology 2004; 232: 773–83. 3 Klessen C, Rogalla P, Taupitz M. Local staging of rectal cancer: the current role of MRI. Eur Radiol 2007; 17: 379–89. 4 Sethi R, Lee SH. Imaging in colorectal cancer. In: Brown SR, Hartley JE, Hill J, Scott N, Williams G, eds. Contemporary Coloproctology. London: Springer, 2012; 123–38. 5 Maas M, Lambregts DM, Lahaye MJ et al. T-staging of rectal cancer: accuracy of 3.0 Tesla MRI compared with 1.5 Tesla. Abdom Imaging 2012; 37: 475–81. 6 Vliegen RF, Beets GL, von Meyenfeldt MF et al. Rectal cancer: MR imaging in local staging – is gadolinium-based contrast material helpful? Radiology 2005; 234: 179–88. 7 Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 2007; 188: 1622–35.
Journal of Digestive Diseases 2014; 15; 188–194 8 Dzik-Jurasz A, Domenig C, George M et al. Diffusion MRI for prediction of response of rectal cancer to chemoradiation. Lancet 2002; 360: 307–8. 9 Hein PA, Kremser C, Judmaier W et al. Diffusion-weighted magnetic resonance imaging for monitoring diffusion changes in rectal carcinoma during combined, preoperative chemoradiation: preliminary results of a prospective study. Eur J Radiol 2003; 45: 214–22. 10 Torkzad MR, Påhlman L, Glimelius B. Magnetic resonance imaging (MRI) in rectal cancer: a comprehensive review. Insights Imaging 2010; 1: 245–67. 11 International Union Against Cancer (UICC). TNM Classification of Malignant Tumours, 7th eds. Sobin LH, Gospodarowicz MK, Wittekind C, eds. New York: Wiley; 2010. 12 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: 355–64. 13 Rovera F, Dionigi G, Boni L, Cutaia S, Diurni M, Dionigi R. The role of EUS and MRI in rectal cancer staging. Surg Oncol 2007; 16 Suppl 1: S51–2. 14 Suzuki C, Torkzad MR, Tanaka S et al. The importance of rectal cancer MRI protocols on interpretation accuracy. World J Surg Oncol 2008; 6: 89. 15 Torkzad MR, Hansson KA, Lindholm J, Martling A, Blomqvist L. Significance of mesorectal volume in staging of rectal cancer with magnetic resonance imaging and the assessment of involvement of the mesorectal fascia. Eur Radiol 2007; 17: 1694–9. 16 Videhult P, Smedh K, Lundin P, Kraaz W. Magnetic resonance imaging for preoperative staging of rectal cancer in clinical practice: high accuracy in predicting circumferential margin with clinical benefit. Colorectal Dis 2007; 9: 412–9. 17 Jang KM, Kim SH, Choi D, Lee SJ, Park MJ, Min K. Pathological correlation with diffusion restriction on diffusion-weighted imaging in patients with pathological complete response after neoadjuvant chemoradiation therapy for locally advanced rectal cancer: preliminary results. Br J Radiol 2012; 85: e566–72. 18 Lambregts DM, Cappendijk VC, Maas M, Beets GL, Beets-Tan RG. Value of MRI and diffusion-weighted MRI for the diagnosis of locally recurrent rectal cancer. Eur Radiol 2011; 21: 1250–8. 19 Curvo-Semedo L, Lambregts DM, Maas M, Beets GL, Caseiro-Alves F, Beets-Tan RG. Diffusion-weighted MRI in rectal cancer: apparent diffusion coefficient as a potential noninvasive marker of tumor aggressiveness. J Magn Reson Imaging 2012; 35: 1365–71. 20 Takeuchi M, Sasaki S, Ito M et al. Urinary bladder cancer: diffusion-weighted MR imaging – accuracy for diagnosing T stage and estimating histologic grade. Radiology 2009; 251: 112–21. 21 Saito W, Amanuma M, Tanaka J, Heshiki A. Histopathological analysis of a bladder cancer stalk observed on MRI. Magn Reson Imaging 2000; 18: 411–5. 22 Gagliardi G, Bayar S, Smith R, Salem RR. Preoperative staging of rectal cancer using magnetic resonance imaging with external phase-arrayed coils. Arch Surg 2002; 137: 447–51. 23 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: 1517–22.
© 2013 Chinese Medical Association Shanghai Branch, Chinese Society of Gastroenterology, Renji Hospital Affiliated to Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd
