Small bowel MR enterography: problem solving in Crohn’s disease

The patient is fasted for 4-6 h prior to the study. In adults, oral contrast consists of at least 1-1.5 l of a 2.5% mannitol solution mixed with 0.2% carob bean gum. This solution acts as a hyperosmolar agent to draw fluid into the bowel. In paediatric patients, the volume of oral contrast is adjusted (between 300-1,000 ml) according to the weight of the patient. Mannitol is a biphasic agent that appears as low signal intensity on T1-weighted images and high signal intensity on T2-weighted images. The patient drinks the oral contrast agent at regular intervals over a period of approximately 40 min prior to the study. The patient is imaged on a 1.5-T MRI scanner (Siemens, Erlangen, Germany), using a phased array surface coil, either in the supine or prone position (if no stoma is present). Coronal sequences are quicker to perform in the prone position, as there is a thinner volume of tissue to image. Although prone imaging has been shown to result in better small bowel distension, both positions are equivalent with respect to lesion detection and characterisation of changes in the bowel wall in CD [4].

With the exception of the cine and diffusion-weighted sequences, all scans are breath-hold and carried out in both the axial and coronal planes. The imaging parameters for our MRE protocol, and the order the sequences are performed in, are shown in Table 1.

The True FISP (fast imaging with steady state precession) sequence consists of a balanced gradient echo sequence where image contrast is dependent on T2*/T1 ratio. It gives high-contrast, predominantly T2*-weighted images. True FISP eliminates phase shifts caused by motion and thus both fluid and blood appear bright. It is a fast acquisition due to a short repetition time (TR) and echo time (TE) with each image acquired in a few hundred milliseconds. Susceptibility artefact occurs with the presence of intraluminal gas or ferromagnetic material, leading to image distortion. Off-resonance artefacts occur in the presence of a non-uniform magnetic field, resulting in banding artefact (alternating stripes) at the periphery of the image. Chemical-shift artefact results in a ‘black boundary’ effect around structures (Fig. 1). This makes mesenteric nodes and vessels more conspicuous but may impede assessment of bowel wall thickening. This sequence provides good delineation between the bowel and the mesentery.

The cine True FISP sequence involves repeatedly imaging the abdomen in the coronal plane sequentially from front to back over a period of 2 min. Twenty images are acquired in each coronal plane. Inflamed loops of bowel will demonstrate decreased peristalsis. An inflammatory small bowel stenosis should open up on cine imaging, compared with a fibrotic stricture where the stenosis will be constant and associated with more marked pre-stenotic dilatation.

Diffusion-weighted imaging (DWI) has recently been added to our MRE protocol with parameters as shown in Table 1. Three b values (b = 0, 100 and 800) are used with axial images through the upper and lower abdomen obtained. The purpose of this is to help identify actively inflamed loops of bowel by the presence of restricted diffusion within the affected bowel wall.

The post-contrast sequence involves a three-dimensional (3D) T1-weighted fat-saturated spoiled gradient echo sequence (Fig. 2) performed 70 s following hand injection of 0.2 ml/kg (0.1 mmol/kg) intravenous Gadoteric acid (Dotarem, Guerbet). Gadolinium is not given in patients with chronic renal impairment, due to the potential long-term risk of nephrogenic systemic fibrosis. A pre-contrast sequence is routinely performed. Some institutions use a dynamic post-contrast coronal acquisition; for example, a volume interpolated breath-hold examination (VIBE) can be performed in the arterial (30 s—optional) and portal venous (60-70 s) phases using bolus triggering once contrast reaches the descending aorta. With a 3D sequence, a radiofrequency pulse excites a thick volume of tissue rather than a thin 2D section, with increased spatial resolution. The 3D sequence is, however, sensitive to motion artefact. Bowel peristalsis is reduced by the prior intravenous administration of a spasmolytic. This usually consists of 20 mg intravenous hyoscine-N-butylbromide (buscopan). Buscopan is routinely given unless contra-indicated (e.g. history of cardiac arrhythmia, narrow angle glaucoma or prostatism). In instances when this cannot be administered, 1 mg intravenous glucagon is given as an alternative unless patients have a known hypersensitivity to glucagon or a history of phaeochromocytoma.. The purpose of this sequence is to assess bowel wall and mesenteric nodal enhancement and to evaluate for the presence of any rim-enhancing fluid collections.

The HASTE (half-Fourier acquired single-shot fast spin echo) sequence is a fast sequence consisting of heavily T2-weighted images. It is a pulse sequence with a very long echo train, where each echo is individually phase encoded. The partial Fourier technique assumes symmetry of raw data in K-space, to reduce data acquisition time. However, this results in a reduced signal-to-noise ratio. It is good at depicting fluid, but other tissues with short T2 values are associated with blurring artefact. It is sensitive to intraluminal flow voids (Fig. 3) and is thus performed after the intravenous administration of a spasmolytic. The HASTE sequence is used to assess for mural oedema. The optional use of fat saturation on one of the T2-weighted sequences (either the True FISP or HASTE sequence) allows differentiation between submucosal fat and oedema which both appear bright on T2-weighted images. Fat saturation also increases the conspicuousness of oedematous bowel loops.

Other radiology techniques used to image the small bowel include barium follow-through, CT enterography, ultrasound and nuclear medicine techniques (such as positron emission tomography [PET]-CT and white cell scintigraphy).

With regards to the use of PET or PET-CT in the evaluation of CD, the sensitivity in the detection of active inflammation ranges between 73% and 90% when compared with clinical, endoscopic or biological markers of disease activity [5, 6]. Using PET alone, there is poor disease localisation, and specificity can sometimes be low [7], as other pathological or physiological processes may lead to increased bowel fluorodeoxyglucose (FDG) uptake. The main disadvantage of PET-CT is the use of ionising radiation; this is clearly not ideal in young patients who may require repeated imaging. It is also more time consuming to perform than CT or MRI alone. Hence for these reasons, PET-CT is not routinely used in the assessment of patients with CD.

A recent meta-analysis of 33 studies using ultrasound, MRE, scintigraphy and CT in the diagnosis of CD, showed no significant difference in the mean sensitivity [8]. All these techniques showed a high sensitivity (> 84%) and specificity (90%) on a per patient basis [8]. Hence the preference is based on availability and consideration of radiation exposure.

Enteroclysis is a technique whereby oral contrast is directly infused into the small bowel via a nasojejunal catheter at a high flow rate (e.g. 80 ml/min) in order to obtain optimal small bowel distension. Depending on the oral contrast agent used and preference of the radiologist, the small bowel can then be imaged using either fluoroscopy, CT or MRI. MR enteroclysis gives better mucosal detail than MRE [9] and is thus more likely to detect subtle aphthous or other types of mucosal ulceration. However, in the assessment of ileal CD, MRE has shown an equivalent accuracy and reproducibility to MR enteroclysis [10].

In addition to ileocolonoscopy, the gastroenterologist can use other techniques to evaluate the small bowel. Double balloon enteroscopy can examine the whole of the small bowel, either under conscious sedation or general anaesthesia. Video (or wireless) capsule endoscopy (VCE) involves the ingestion of a capsule that contains a camera and transmitter, which is propelled along the bowel by peristalsis. A video recorder carried on the patient records the signals and a computer later processes the data. A recent meta-analysis [11] looking at nine studies comparing VCE to other techniques in the diagnosis of CD (i.e. ileocolonoscopy, CT enterography/enteroclysis, push enteroscopy and MRI) showed VCE gave a greater diagnostic yield due to its ability to detect mucosal abnormalities. However VCE is not possible in stricturing disease, hence radiological imaging is usually required first to exclude this (unless a patency capsule is used).

Table 2 shows the advantages and disadvantages of each technique when compared with MRE.

The multidisciplinary team meeting (consisting of the radiologist, gastroenterologist, histopathologist and surgeon) is an important forum where imaging, histopathology and clinical status of the patient can all be reviewed, in order to determine the most appropriate management. The following important questions can be addressed on MRE: (1) extent of small and large bowel involvement at first presentation; (2) distinction between active inflammatory and fibrotic stricturing disease; (3) recognition of penetrating disease with the development of extramural complications; (4) evaluation of response to medical therapy; (5) detection of recurrent disease following surgery. Each of these questions will be addressed in turn.