ª Springer Science+Business Media New York 2014

Abdominal Imaging

Abdom Imaging (2014) DOI: 10.1007/s00261-014-0103-3

Rectal cancer in inflammatory bowel diseases: MR imaging findings Matthias Barral,1 Christine Hoeffel,2 Mourad Boudiaf,1 Anthony Dohan,1,3 Philippe Marteau,3,4 Vale´rie Laurent,5 Philippe Soyer1,3 1

Department of Abdominal Imaging, Hoˆpital Lariboisie`re, Assistance Publique-Hoˆpitaux de Paris, 2 rue Ambroise Pare´, 75010 Paris, France 2 Department of Imaging, Hoˆpital Robert Debre´, 11 Boulevard Pasteur, 51092 Reims Cedex, France 3 Universite´ Paris-Diderot, Sorbonne Paris Cite´, 10 Avenue de Verdun, 75010 Paris, France 4 Department of Digestive Diseases, Hoˆpital Lariboisie`re, Assistance Publique-Hoˆpitaux de Paris, 2 rue Ambroise Pare´, 75010 Paris, France 5 Department of Radiology, CHU Nancy-Brabois, Alle´e du Morvan, 54511 Nancy Cedex, France

Abstract Purpose: To retrospectively analyze the MR imaging features of rectal cancer in patients with inflammatory bowel diseases (IBD). Materials and methods: The MR imaging examinations of 13 patients with IBD-related rectal cancer were retrospectively reviewed. MR imaging included T2weighted, diffusion-weighted (DW), and gadolinium chelate-enhanced MR imaging. MR imaging findings were analyzed and compared with endoscopic and histopathological findings. Results: Eight patients (8/13; 62%) had active IBD and five (5/13; 38%) had quiescent IBD on MR imaging. Two different tumor patterns were individualized including clearly visible soft-tissue mass (4/13; 31%) (Type 1 tumor) and marked circumferential rectal wall thickening (9/13; 69%) (Type 2 tumor). Twelve tumors (12/13; 92%) showed high signal intensity on T2-weighted MR images. All six tumors studied with DW-MR imaging (6/6; 100%) showed high signal on DW-MR imaging with restricted diffusion on apparent diffusion coefficient (ADC) map. On gadolinium chelate-enhanced MR imaging, heterogeneous enhancement was observed in one tumor (1/13; 8%), whereas 12 tumors (12/13; 92%) showed homogeneous enhancement. MR imaging showed pelvic fistula and intrapelvic abscess in association with four (4/13; 31%) and two tumors (2/13; 15%), respectively. Conclusion: Our limited retrospective study demonstrates that rectal cancer in IBD patients can present as a

Correspondence to: Philippe Soyer; email: [email protected]

circumferential wall thickening resembling inflammation and can occur in the absence of fistula or abscess. The use of T2-weighted and DW-MR imaging is recommended to improve rectal cancer detection in patients with long-standing IBD. Key words: Adenocarcinoma—Rectal neoplasm— Inflammatory bowel disease—Imaging—Magnetic resonance imaging

Inflammatory bowel diseases (IBD), including ulcerative colitis and Crohn disease, are associated with an increased incidence of colorectal cancer [1–4]. It is assumed that the increased risk of IBD-related rectal cancer results from chronic inflammation and depends on the duration of the disease [1, 2, 5]. Patients with IBD are subjected to inflammatory anal and pelvic complications of the disease that result in marked local changes [6]. Because treatment options markedly differ between inflammatory complications and rectal cancer, it is crucial to differentiate between these two conditions for an appropriate treatment. Magnetic resonance (MR) imaging has currently a pivotal role in the evaluation of patients with IBD, as well as it has a major role for the staging of rectal cancer [7–10]. The computed tomography (CT) features of IBD-related colorectal cancer have been well described [11]. By contrast, little attention has been given to the MR imaging features of IBD-related rectal cancer [12–15]. We are aware of several reports or case series that have

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

described the imaging appearance of anorectal adenocarcinomas associated with Crohn disease-related perineal fistulas [16–21]. However, these papers have predominantly focused on mucinous adenocarcinomas associated with perianal fistula and none of these have specifically addressed IBD-related rectal cancer. To our knowledge, no series have reported the MR imaging appearance of rectal cancer occurring on both ulcerative colitis and Crohn disease. The goal of this study was twofold. First, we wanted to illustrate the MR imaging features of rectal cancer that occur in IBD (either Crohn disease or ulcerative colitis). Second, we wanted to correlate the MR imaging findings with those observed at endoscopy and histopathological analysis.

Materials and methods We considered consecutive patients with IBD-related rectal cancer who had pelvic MR imaging at 1.5-Tesla before surgery between January 2008 and December 2012. Only adult patients (age ‡18 years) were included. The study group is comprised of 13 patients (9 men, 4 women), with a median age of 46 years (q1 = 43; q3 = 54; range 25–65 years). Histopathological confirmation of rectal cancer was documented either after endoscopically guided biopsy or surgical resection of the primary rectal tumor. For all patients, MR imaging was performed prior to radiochemotherapy and surgery. The diagnosis of IBD was based on the results of clinical, biological, imaging, endoscopic, and histopathological examinations. Eight patients (5 men, 3 women) with a median age of 47 years (range 25–54 years) had Crohn disease, and five patients (3 men, 2 women) with a median age of 52.5 years (range 39–65 years) had ulcerative colitis. For each patient, clinical data including clinical symptoms, type of IBD, duration of IBD until the diagnosis of rectal cancer, age at the onset of IBD, associated ileocolic involvement by IBD, the presence of known fistula-in-ano and findings at optical colonoscopy were recorded. Original histopathological reports were reviewed with respect to tumor type and differentiation, local tumor staging (pT staging), lymph node involvement (pN staging), peritoneal carcinomatosis, hepatic metastases, and activity of underlying IBD (active vs. quiescent). This retrospective study was conducted following the guidelines of our institutional review board, and informed consent was waived.

MR imaging protocol MR examinations were obtained at 1.5 T with two different MR units (Magnetom Avanto, VB15 or VB 17software version, Siemens Healthcare, Erlangen, Germany) or Signa Excite HDX (General Electric Healthcare, Milwaukee, WI) equipped with high-performance

gradient system (gradient strength, 33–45 mT/m; slew rate, 120–200 mT/m/ms) and 9 receiver channels, using one anterior torso phased-array coil with six channels and a posterior spine cluster with three channels, with the patient in a supine position. No specific bowel preparation was used before MR examination, and no antispasmodic agents were administrated to the patients. Six patients (6/13; 46%) underwent MR imaging because of chronic fistula, 4 patients (4/13; 31%) because of colonic obstruction, and 3 patients (3/13; 23%) because of suspicious findings of malignancy at endoscopy. For all patients, MR imaging protocol included T2weighted turbo spin-echo (TSE) or fast spin-echo (FSE) MR imaging in the axial, coronal, and sagittal planes. The imaging parameters were as follows: TR, 3025– 5180 ms; TE, 85–114 ms; slice thickness, 3–5 mm; number of signal averages, 2–4; reconstruction matrix size, 192–172–320 9 288; intersection gap, 10–20%; field of view, 160–240 mm; echo train length, 10–21; echo spacing, 8–12 ms; receiver bandwidth, 130-190 Hz/pixel; 18– 25 sections acquired; turbo factor, 17–23; acquisition time, 3–6 min. In addition, when a rectal lesion was visible, highresolution oblique axial T2-weighted FSE or TSE MR images were obtained perpendicular to the rectal wall at the level of the rectal lesion. For patients with tumor in the lower rectum, an additional high-resolution coronal oblique MR sequence was performed parallel to the anal canal. In 6 patients (6/13; 46%), diffusion-weighted (DW) MR imaging was part of the imaging protocol. Images were obtained prior to gadolinium chelate administration using fat-attenuated spectral adiabatic inversion recovery technique (SPAIR) with a single-shot spin-echo echoplanar technique in the axial plane with three gradient factors (b values = 0, 400–500 and 800–1000 s/mm2). DW-MR imaging was performed in all patients in the axial plane. The imaging parameters were as follows: TR, 6200–8000 ms; TE, 85–92 ms; slice thickness, 5 mm; number of signal averages, 4–5; reconstruction matrix size, 160 9 160–192 9 182; intersection gap, 10%, field of view, 300–380 mm; voxel size, 2.1 9 2.0 9 5.0 mm; echo spacing, 0.83 ms; receiver bandwidth, 1302 Hz/ pixel; 26–40 sections acquired; EPI factor, 182; GRAPPA, 2; acquisition time, 2–3 min. Fat-suppressed three-dimensional T1-weighted fastspoiled gradient echo images (VIBE or LAVA) were obtained in the axial plane before and after intravenous administration of a gadolinium chelate (gadoterate meglumine, Dotarem, Laboratories Guerbet, RoissyCharles de Gaulle, France) at a dose of 0.1 mL per kg of body weight with the following parameters: TR, 5.8 ms; TE, 2.7 ms; flip angle, 15; slice thickness, 2.5 mm; number of signal averages, 1; reconstruction matrix size, 192 9 182; intersection gap, 10%, field of view, 320 mm; voxel size, 1.2 9 0.8 9 2.5 mm; receiver bandwidth,

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

280 Hz/pixel; 64 sections acquired; parallel imaging, acceleration factor of 2.

Image analysis Images were reviewed on a picture archiving and communication system (PACS) workstation (Directview, 11.3 sp1 version, Carestream HealthInc, Rochester, NY, USA) by two abdominal radiologists working in consensus blinded to all clinical information, the results of endoscopy, surgery, histopathological analysis, and location of the tumor. Quantitative analysis of MR images included the size of visible tumor, maximum rectal wall thickness and, when present, length of the stenosis. The distance to the circumferential resection margin was also recorded. The different MR sequences were analyzed in terms of tumor MR imaging features. According to Hristova et al. [11, 22], rectal tumors were classified as Type 1 (i.e., when a soft-tissue mass was visible) or Type 2 tumor (i.e., when the tumor presented as a stenosis with marked and layered circumferential thickening. T2-weighted TSE or FSE MR sequences were analyzed with a special attention given to the presence of perirectal fat infiltration, free-fluid effusion, the presence of fistula or abscess, wall thickening (i.e., wall thickness more than 3 mm) [23–25], and colonic dilatation proximal to luminal narrowing [26–30]. When a mass was present, its location (i.e., lower, mid, or upper rectum) was recorded and its signal intensity was compared to that of the muscularis layer and submucosa. MR images obtained after intravenous administration of gadoterate meglumine were analyzed for the presence of mural stratification and perirectal fat infiltration [25, 27, 30]. Mural stratification was defined as a target or double halo appearance of the rectal wall [23, 24]. DW-MR images and apparent diffusion coefficient (ADC) map were analyzed with respect to the presence of high signal intensity on DW-MR images and impeded diffusion on ADC map. The presence of perirectal lymph nodes was evaluated on T2-weighted and DW-MR images considered as suspicious of metastatic involvement when they presented with heterogeneous signal intensity, irregular edges, and shortest axial diameter >5 mm [23, 31, 32]. After the reading sessions, patient files were reviewed for the extent of the disease, presence of extra digestive abnormalities such as hepatic metastases, peritoneal nodules, and other findings that are usually associated with IBD such as primary sclerosing cholangitis, cholelithiasis, sacroiliitis, and nephrolithiasis [23].

Statistical analysis Descriptive statistics were calculated for all the clinical variables and those evaluated on MR Imaging. For

continuous data, (age, duration of IBD, age at onset of IBD, tumor size, rectal wall thickness, and length of stenosis) they included medians, first quartiles (q1), third quartiles (q3), and ranges. For the binary data, descriptive statistics included raw numbers, proportions, and 95% exact confidence intervals (CIs).

Results Clinical and histopathological findings Clinical and histopathological findings in the 13 patients are reported in Table 1. The median duration of IBD until the diagnosis of rectal cancer was 21 years (q1 = 15; q3 = 30; range 10–36 years). The median age at the onset of IBD was 24 years (q1 = 18; q3 = 33; range 7–50 years). All patients had rectal involvement by IBD (13/13; 100%; 95% CI 75%–100%). Four patients (4/13; 31%; 95% CI 9%–61%) had ileocolic involvement by IBD and four patients had a pancolitis (4/13; 31%; 95% CI 9%–61%). All patients (13/13; 100%; 95% CI 75%–100%) were under medical therapy when the diagnosis of rectal cancer was made.

Table 1. Clinical and histopathological findings in 13 patients with IBD-related rectal cancer Quantitative variables

Median

q1; q3

Range

Age (years) Duration of IBD (years) Age at onset of IBD (years)

46 21 24

43; 54 15; 30 18; 33

25–65 10–36 7–50

Categoric variables

Raw numbers

Proportions (%)

95% CI

Male gender Crohn disease Ulcerative colitis Active IBD Colonic obstruction Iron deficiency anemia Associated ileal involvement Pancolitis Abscess Fistula Visible tumor at endoscopy Tumor location Upper rectum Midrectum Low rectum Whole rectum Upper and midrectum Mid and lower rectum Tumor mass at gross examination Lieberkuhnian adenocarcinoma Presence of signet ring cells pT4* Peritoneal carcinomatosis Lymph node metastases Hepatic metastases

9 8 5 8 2 2 4 4 2 4 7

9/13 8/13 5/13 8/13 2/13 2/13 4/13 4/13 2/13 4/13 7/13

38–95 31–86 14–68 29–82 2–45 2–45 9–61 9–61 2–45 9–61 25–81

1 1 5 2 3 1 5 12 1 2 2 7 3

1/13 (8) 1/13 (8) 5/13 (38) 2/13 (15) 3/13 (23) 1/13 (8) 5/13 (38) 12/13 (86) 1/13 (8) 2/13 (15) 2/13 (15) 7/13 (54) 3/13 (23)

(69) (61) (38) (46) (15) (15) (31) (31) (15) (31) (54)

0–36 0–36 14–68 2–45 5–54 0–36 14–68 57–98 0–36 2–45 2–45 25–81 5–54

Note For quantitative data (continuous), data are medians; first quartiles (q1) and third quartiles (q3), and ranges. For categorical (binary) data, data are raw numbers; numbers in parenthesis are percentages; followed by 95% exact confidence intervals (CIs). *pT4 indicates a tumor infiltrating beyond the fascia recti at histopathological analysis

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

At the time rectal cancer was diagnosed, eight patients (8/13; 61%; 95% CI 31%–86%) presented with clinical symptoms suggesting active IBD; of these, four (4/13; 31%; 95% CI 9%–61%) had recurrent anal fistula in association with pelvic abscess in two of them (2/13; 15%; 95% CI 2%–45%). Four patients (4/13; 31%; 95% CI 9%–61%) complained of symptoms of colonic obstruction; of these, two patients did not respond favorably to medical treatment. Two patients (2/13; 15%; 95% CI 2%–45%) had chronic iron deficiency anemia. All patients underwent colorectal videoendoscopy. Histopathological analysis of biopsy specimens obtained during endoscopy showed tumor involvement in all patients. The diagnosis of rectal cancer was suspected during macroscopic endoscopic examination in seven patients (7/13; 54%; 95% CI 25%–81%); of these, endoscopy was part of the annually screening program in six patients. Endoscopy failed to visually detect the rectal cancer in the other six patients (6/13; 46%; 95% CI 19%– 75%) that was ultimately detected owing to systematic endoscopy-guided biopsies. Histopathological analysis revealed that 12 patients had rectal cancer ranging from poorly (n = 3), moderately (n = 3), to well-differentiated (n = 6) adenocarcinoma. One patient had an epidermoid carcinoma. In all but one patient, the tumor invaded or went beyond the muscularis layer: two rectal cancers (2/13; 15%; 95% CI 2%–45%) were categorized as pT4, nine (9/13; 69%; 95% CI 38%–91%) as pT3, one (1/ 13; 8%; 95% CI 1%–36%) as pT2, and one (1/13; 8%; 95% CI 1%–36%) as pT1. Signet ring cells were found in one patient (1/13; 8%; 95% CI 1%–36%). Three patients (3/13; 23%; 95% CI 5%–54%) had multiple focal liver lesions visible on extension assessment, consistent with hepatic metastases from primary rectal cancer; of these, two patients (2/13; 15%; 95% CI 2%–45%) had peritoneal nodules indicating peritoneal carcinomatosis. No patients had primary sclerosing cholangitis, cholelithiasis, or sacroiliitis.

Fig. 1. A 44-year-old woman with Crohn disease diagnosed 12 years before and well-differentiated rectal adenocarcinoma. T2-weighted turbo spin-echo MR image in the axial plane (TR/TE = 3000/115 ms) shows a T3, posterior tissue mass of the lower rectum (arrow), just above the anorectal junction.

Imaging findings and pathological correlation Rectal tumors were visible on MR images in all patients (13/13; 100%; 95% CI 75%–100%). On the basis of MR imaging presentation, two distinct patterns were individualized. In four patients (4/13; 31%; 95% CI 9%–61%), the tumor presented as a rectal mass (Type 1 tumor) with a median axial diameter of 30 mm (q1 = 25; q3 = 36; range 9–43 mm) (Fig. 1). In nine patients (9/13; 69%; 95% CI 38%–95%), MR images showed an extended circumferential thickening of the rectal wall (Type 2 tumor) (Figs. 2, 3, 4, 5). The median maximal wall thickness was 12 mm (q1 = 11; q3 = 15; range 5–18 mm), and the median length of the circumferential thickening was 41.5 mm (q1 = 29; q3 = 60; range 20–77 mm). Locations of cancer with respect to the rectal segments are reported in Table 2. The median distance to

Fig. 2. A 47-year-old woman with Crohn disease diagnosed 30 years before and moderately differentiated adenocarcinoma. T2-weighted turbo spin-echo MR image in the sagittal plane (TR/TE = 3000/115 ms) shows T3 circumferential lesion (arrowheads) of the rectum.

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

Fig. 3. A 54-year-old woman with Crohn disease diagnosed 18 years before and well-differentiated adenocarcinoma of the midrectum. T2-weighted fat-suppressed half Fourier single-shot turbo spin-echo (HASTE) MR image in the sagittal plane (TR/TE = 1000/85 ms) shows a circumferential marked thickening of the lower rectum (arrow) responsible for an upstream dilatation of the sigmoid colon (arrowhead).

Fig. 5. A 43-year-old woman with ulcerative colitis diagnosed 33 years before and well-differentiated rectal adenocarcinoma discovered during annual screening. A T2weighted turbo spin-echo MR image in the axial plane (TR/ TE = 8780/114 ms) shows circumferential thickening of the upper rectum (arrow).B Diffusion-weighted MR image in the axial plane (TR/TE = 4000/81 ms; b = 1000 s/mm2) shows marked hyperintense thickening of the upper rectum wall (arrow) at high b value (b = 800 s/mm2). Fig. 4. A 43-year-old man with Crohn disease diagnosed 16 years before, presenting with painful anal stenosis. Endoscopic biopsy revealed poorly differentiated rectal adenocarcinoma. T2-weighted turbo spin-echo MR image in the axial plane (TR/TE = 4360/96.9 ms) shows T3 lesion (arrow) with circumferential and layered thickening of the rectal wall.

the circumferential resection margin was 2.5 mm (q1 = 1; q3 = 4; range 0–10 mm). An associated upstream colonic dilatation was present in two patients (2/13; 15%; 95% CI 2%–45%) (Fig. 3). Free-fluid effusion was present in one patient (1/13; 8%; 95% CI 1%–36%). Seven patients (7/13; 54%; 95% CI 25%–81%) had lymph node involvement on MR examination and were classified as pN1. Four patients (4/13; 31%; 95% CI 9%–61%) had a fistula tract originating from the rectum in association with an intrapelvic abscess in two of them (2/13; 15%; 95% CI 2%–45%). On gadolinium chelate-enhanced MR imaging, stratification was present in two patients (2/13; 15%; 95% CI 2%–45%) (Fig. 6), one patient had an heterogeneous enhancement of the submucosal portion of the rectal wall

(1/13; 8%; 95% CI 1%–36%) and four patients had perirectal fat infiltration (4/13; 31%; 95% CI 9%–61%) (Fig. 6). Ten tumors (10/13; 77%; 95% CI 46%–95%) presented with a circumferential rectal wall thickening of more than 11 mm and no stratification. Twelve tumors (12/13; 92%; 95% CI 64%–99%) showed high signal intensity on T2-weighted MR images compared to that of the muscularis mucosae. Of these, eleven (11/12; 92%; 95% CI 61%–99%) showed low signal intensity compared to that of the submucosa and one (1/12; 8%; 95% CI 1%–38%) showed high signal intensity. All six tumors for which DW-MR imaging was part of the MR imaging protocol (6/6; 100%; 95% CI 54%– 100%) showed high signal intensity on DW-MR images (Fig. 5) and restricted diffusion on apparent diffusion coefficient (ADC) map.

Discussion We found in our retrospective analysis that IBD-related rectal cancer displays two different patterns on MR

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

Table 2. Magnetic resonance imaging findings in 13 patients with IBDrelated rectal cancer Quantitative variables

Median

q1; q3

Range

Tumor size at MR imaging (mm) Maximal wall thickness (mm) Length of the stenosis (mm) Circumferential margin of resection (mm)

30 12 41.5 2.5

25; 26 11; 15 29; 60 1; 4

9–43 5–18 20–77 0–10

Categorical variables

Raw number

Proportions (%)

95% CI

Visible tumor at MR imaging Type 1 tumor at MR imaging Type 2 tumor at MR imaging High signal on T2W MR imaging* High signal on DW-MR imaging  Stratification Submucosal fat deposition Heterogeneous submucosal enhancement Adjacent fat infiltration Pelvic fistula Intrapelvic abscess Upstream colonic dilatation Lymph node involvement pattern Free-fluid effusion

13 4 9 12 6 2 2 1

13/13 (100) 4/13 (31) 9/13 (69) 12/13 (79) 6/6 (100) 2/13 (15) 2/13 (15) 1/13 (8)

75–100 9–61 38–95 64–99 54–100 2–45 2–45 0–36

4 4 2 2 7 1

4/13 4/13 2/13 2/13 7/13 1/13

9–61 9–61 2–45 2–45 25–81 0–36

(31) (31) (15) (15) (54) (8)

Note For quantitative data (continuous), data are medians, first quartiles (q1) and third quartiles (q3) and ranges. For categorical (binary) data, data are raw numbers; numbers in parenthesis are percentages; followed by 95% exact confidence intervals (CIs) a T2W MR imaging indicates T2-weighted MR imaging b DW-MR imaging indicates diffusion-weighted MR imaging

imaging. One is a classical soft-tissue mass similar to that observed in the more common rectal adenocarcinoma that develops in the absence of underlying IBD, while the other corresponds to a circumferential thickening that may be responsible of a stenosis and may be difficult to differentiate from benign morphological changes caused by IBD. In six patients (6/13; 46%) of our study, endoscopy failed to visually detect the tumor that was ultimately detected owing to systematic endoscopy-guided biopsies. This is the reason why systematic biopsies or curettage should be performed to improve diagnostic performances and avoid delayed management of rectal malignancies [33]. The detection of IBD-associated rectal cancer remains difficult because IBD patients sometimes have stricturing lesions that prevent the progression of the endoscope. In additional, digital rectal examination is limited by pain and local fibrotic changes [12]. Even under general anesthesia, experienced colorectal surgeons may miss an early malignant lesion. Consequently, MR imaging may help guide surgeons and endoscopists for performing biopsies in suspicious areas and may represent an option in the detection of rectal cancer in patients with incomplete rectosigmoidoscopy. Charles et al. [3] have demonstrated in a large cohort study that there was an increased incidence of rectal cancer only for patients with ulcerative colitis and not for

Fig. 6. A 62-year-old man with ulcerative colitis diagnosed 42 years before and well-differentiated rectal adenocarcinoma discovered during annual screening. A T2-weighted turbo spin-echo MR image in the axial plane (TR/TE = 6430/ 122 ms) shows circumferential and layered wall thickening of the midrectum (arrow), irregular and enlarged lymph node (white arrowhead), of which one is extrafascial (black arrowhead). B T1-weighted spin-echo MR image in the axial plane before intravenous administration of gadolinium chelate (TR/ TE = 636/13 ms) shows circumferential and layered wall thickening (arrow) and infiltration of the perirectal fat (arrowhead). C, T1-weighted fat-suppressed spin-echo MR image in the axial plane after intravenous administration of gadolinium chelate (TR/TE = 553/11 ms) shows circumferential thickening with enhancement of the muscularis layer and submucosa resulting in stratified pattern (arrow), and mesorectal infiltration (arrowhead).

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

those with Crohn disease. However, our population of patients with IBD-related rectal cancer included patients with ulcerative colitis (35%) and patients with Crohn disease (65%). This suggests that Crohn disease patients may have an increased risk for rectal cancer although our study design does not allow calculation of such risk. The imaging presentation of IBD-related colorectal cancer has been largely reported on computed tomography (CT) and barium enema [11, 23, 27, 34–36]. Similarly, the CT and MR imaging findings of IBD-related small-bowel tumors have also been described [37–39]. Conversely, a few studies have reported the imaging presentation of IBDrelated rectal cancer [12–15] and no studies have described specifically the MR appearance of IBD-related rectal cancer. As a matter of fact, the diagnosis of rectal cancer in IBD remains challenging. Indeed, there is an overlap between the clinical presentation of benign complications of IBD and that of rectal cancer. Intestinal obstruction, iron deficiency related to chronic bleeding, weight loss, diarrhea, and fistulas may classically reveal rectal cancer in patients free of IBD [40]. The same symptoms are frequently observed in patients with IBD in the absence of rectal cancer. In our study, four patients (4/13; 31%) presented with abdominal symptoms of colonic obstruction, and two patients (2/13; 15%) had chronic anemia. This may explain why the diagnosis of rectal cancer is often difficult and delayed in IBD patients [40, 41]. In addition, chronic complications as well as active disease may obscure classical imaging findings that usually warn the radiologist of the potential presence of malignancy. Moreover, endoscopy and negative histological findings of biopsy samples obtained through endoscopy may ignore the diagnosis that will ultimately be revealed after surgery [11]. The main result of our study is that the majority of IBD-related cancers present as a circumferential and layered wall thickening (8/13; 67%) with a median length of segmental involvement of 41.5 mm and not as a tumor mass as observed in the more common, sporadic rectal cancer. This less frequent pattern has been reported in secondary rectal tumors such as metastasis and linitis plastica [22, 42–46]. Indeed, these two patterns consist in a circumferential, segmental, parietal infiltration with moderate wall thickening with stratification, and are accompanied by a peritumoral fibrosis with infiltration of the perirectal fat [22, 42–46]. Regarding rectal wall chronic changes due to IBD, the loss of mural stratification is thought to correspond to fibrotic tissue scars, but when present in association with a marked parietal thickening, it should be considered as an alarming finding for the presence of an underlying malignancy as suggested by our results [11, 23, 27]. In our study, loss of stratification associated with a marked circumferential thickening of the rectal wall was visible in ten patients on MR imaging. It is commonly assumed that in patients with active IBD, stratification, adjacent fat infiltration, and free-fluid

effusion are usually due to a combination of hyperhemia and edema, as a result of an IBD-related inflammatory process [47]. Consequently, inflammation, when present may obscure findings suggestive for the presence of rectal cancer, thus potentially hampering cancer detection. Another result of our study is that the majority of IBD-related rectal cancers occur in the absence of fistula or abscess. Researchers have demonstrated that anorectal carcinoma may occur in Crohn disease patients with longstanding IBD and unhealed chronic fistula [17, 18]. However, these cancers were mucinous or perianal adenocarcinomas [18, 19] and may also occur in patients with chronic fistulas in the absence of IBD [16, 19, 48]. In our study, we found a median age of 46 years at the time of diagnosis of IBD-related rectal cancer, which is consistent with the results of other researchers and less than the age of onset of sporadic rectal cancer [49, 50]. We also found a median duration of IBD of 21 years before the occurrence of rectal cancer, which is longer than those previously reported [11]. In one patient of our series, adenocarcinoma was found 36 years after the onset of the disease and may be not related to IBD. However, IBD-related rectal cancer should be actively searched for in patients presenting with well-identified risk factors or alarming findings such as an age over 45 years, a long-standing IBD, recent changes in clinical symptoms, a structuring disease, a pancolitis, a young age at the time of the diagnosis of IBD, or a family history of rectal cancer [3, 50–53]. In addition, as reported by Gore et al. [23], several features such as asymmetric mural thickening, focal loss of stratification, the presence of free-fluid effusion, colonic dilation proximal to marked stenosis, and mural thickening of more than 15 mm should be considered as alarming findings. In our study, we found a median maximal rectal wall thickness of 12 mm that was less than the generally admitted cut-off value. By contrast with the results of Hristova et al., who found a heterogeneous enhancement in the majority of IBD patients with diffuse rectal cancer at CT, we found only one patient (1/13; 8%) who had such specific pattern of enhancement on gadolinium chelate-enhanced MR images [11]. Consequently, our results suggest that the use of gadolinium chelate does not help to improve detection of IBD-related rectal cancer and its use may be not helpful. In six patients (6/13; 46%) in whom DW-MR imaging was part of the protocol, the tumor showed high signal intensity suggesting restricted diffusion. Of interest, Soyer et al. [54] have reported high degrees of sensitivity for DW-MR imaging for the detection of rectal cancer, but their population of patients did not include IBD patients. Our results suggest that DW-MR imaging may improve rectal cancer detection in IBD patients and should therefore be included in the basic protocol for the follow up of IBD patients with longstanding disease.

M. Barral et al.: Rectal cancer in inflammatory bowel diseases

Our study has several limitations. The first relates to the relatively small sample size of our patients population. However, this is to date the largest study that has reported the MR imaging findings of IBD-related rectal cancer. The second limitation is due to the fact that the MR imaging protocol was not specifically designed for the evaluation of rectal cancer but made for the evaluation of pelvic IBD. This is the reason why our protocol included a gadolinium chelate-enhanced MR sequence and a T2-weighted fat-suppressed acquisition, which both are not recommended for the assessment of rectal cancer [55]. The third limitation was that only six patients (6/13; 46%) of our study population had DW-MR imaging so that the potential role of this sequence for the detection of IBD-related rectal cancer cannot be fully evaluated. Another limitation was that there were not any negative MR examinations in our study so that the specificity of MR imaging could not be assessed. In conclusion, because of the difficulty in making the diagnosis of rectal cancer in the setting of IBD, radiologists should be aware of alarming MR imaging findings that may suggest rectal cancer. Our analysis shows that rectal cancer in IBD patients displays two main patterns on MR imaging, but predominantly presents as a circumferential wall thickening resembling inflammation. In addition, we found that the majority of IBD-related rectal cancers occur in the absence of an associated fistula or abscess. It is assumed that knowledge of these findings should help to suggest the diagnosis of this rare complication. Our results suggest that the combination of T2-weighted and DW-MR imaging is recommended to improve rectal cancer detection in patients with longstanding IBD although our limited sample size does not allow us to draw definite conclusion. Acknowledgements. All authors have made substantial contributions to all of the following: (1) the conception and design of the study, or acquisition of data, or analysis and interpretation of data, (2) drafting the article or revising it critically for important intellectual content, (3) final approval of the version to be submitted.

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Rectal cancer in inflammatory bowel diseases: MR imaging findings.

To retrospectively analyze the MR imaging features of rectal cancer in patients with inflammatory bowel diseases (IBD)...
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