Sequence
Plane
Number of sections
Section thickness (mm)
Field of view (mm)
Advantages
Limitations
HASTE/SSFSE
Coronal
1
50
512 × 512
Minimal susceptibility artefact
Prone to flow artefacts
SSFP (True-FISP/FIESTA)
With and without fat suppression
Coronal and axial
19–25
5/0
160–512 × 160–400
Useful for extra enteric visualization including mesentery and nodes when fat saturation absent
In presence of fat suppression useful for enteric changes and subtle mural abnormality
Susceptibility artefact
HASTE with fat saturation
Coronal and axial
19–25
2–4
As above
Mesenteric evaluation impaired due to k-space filtering
2D and/or 3D fat-saturated dynamic T1-weighted GE (LAVA, VIBE, etc.)
Dynamic coronal with axial delayed
52–64
1.5–2.5
288–400 × 312–400
Mural assessment and evaluation of disease activity
3D better for spatial resolution and SNR but more prone to Misregistration artefact
The introduction of parallel imaging techniques , as well as improvements in coil technology, have contributed to the increased robustness of MRI as well as reduction in acquisition times. For instance, the recently introduced “CAIPIRINHA” (Controlled Aliasing In Parallel Imaging Results IN Higher Acceleration) sequence, which accelerates data acquisition in phase-encoding and slice-encoding directions with the additional advantage of using a non-standard sampling pattern, volumetric imaging can be acquired using higher acceleration factors, resulting in less image degradation, reduced acquisition times and superb spatial resolution. In our institution, we use 1.5 mm slice thickness CAIPIRINHA sequences routinely, which approaches the spatial resolution of CT (Fig. 18.1).
Fig. 18.1
Exquisite spatial resolution of “CAIPIRINHA ” images. These fat-saturated T1 weighted GE images allow higher acceleration factors and, consequently, can be obtained within a breath hold and simultaneously have exquisite spatial resolution. The arrows point to subtle ulcers in inflamed ileal segments
Diffusion-weighted imaging is also slowly being integrated in the protocols, and discussed below.
Preliminary data on magnetization transfer imaging has been published as useful for the assessment of fibrosis in strictures (Adler J et al., Radiology 229(1):275–81, 259(1), 127–135 2011), but more data is needed for full acceptance.
The ideal patient positioning is a theme of discussion. In many institutions these studies are performed prone to allow separation of pelvic small bowel loops. This position also allows maximum coverage on coronal images and decreases scanning volume. We prefer supine imaging for patient comfort in these patients, many of whom are slim and find prone imaging uncomfortable, in some cases due to prior surgical procedures.
Most institutions routinely administer an anti-peristaltic agent to minimize peristaltic artefact. This is of prime importance in maintaining image quality in sequences that are prone to flow artefacts, such as the HASTE or SSFSE (Half Fourier single shot turbo spin echo and Single shot fast spin echo sequences). We usually administer a divided dose of an anti-peristaltic with the second aliquot being given prior to the gadolinium enhanced sequences. Depending on local availability this can either be obtained with 10 mg of hyoscine butylbromide (Buscopan® ) or 0.2 mg of glucagon given intravenously. Buscopan is not licensed for use in the United States. To promote gastric emptying whilst ingesting oral contrast, either erythromycin or metaclopramide (20 mg) can be given once the first 500 mg of contrast has been drunk.
For MR enteroclysis X-ray fluoroscopic guidance is used to confirm catheter placement at or beyond the duodeno-jejunal flexure. Baseline imaging is then obtained prior to instillation of 1.5–2 L of fluid at a rate of 100–120 ml/min using an infusion pump. The progress of the contrast and the degree of distension can be monitored via thick slabs or dynamic MR fluoroscopic sequences. These are typically SSFP (Steady State Free Precession) 5 mm section images aligned parallel to the longitudinal axis of the segment of concern. The images are acquired at between 0.5–2 frames per second. When the contrast reaches the ileocecal junction, we administer antispasmodics (see below).
For MR enterography, patients are given 1–2 L of one of the several possibilities of oral contrast (see below) about 45 min before the acquisition of images.
Oral Contrast
In most institutions, the majority of MR studies are performed as an enterography rather than enteroclysis, as discussed.
Luminal distension with oral contrast is vital for detailed assessment of the bowel wall. Additional benefits include the displacement of air from the lumen by oral contrast. This is necessary as air produces susceptibility artefact and degrades image quality.
Oral contrast utilization will be determined by several factors including local availability, patient tolerance, cost and the effectiveness of distension. In addition to the choice of agent there is departmental variation in the volumes administered and the timing of image acquisition following ingestion of the contrast material. In some instances there may be rapid transit of contrast to the right colon but in the majority of individuals a delay of 40–60 min from the start of contrast ingestion is adequate to obtain small bowel distension.
Significant variance exists between the agents available and it is important to be cognizant of the differences. Agents can be stratified into several categories:
Negative contrast agents are of low signal intensity on T1-weighted and T2-weighted imaging. These include super paramagnetic iron oxide agents such as ferumoxsil. It is rarely used.
Positive contrast agents are of high signal intensity on T1-weighted and T2-weighted imaging. They are currently very rarely used.
Biphasic agents are of variable signal intensity depending on the sequence that is applied (low signal intense on T1-weighted imaging and high signal intensity on T2-weighted imaging). In clinical practice, these are the most utilized and there is consequently a greater choice in this category. Table 18.2 provides more information regarding the characteristics of different contrast agents.
Table 18.2
Comparison of oral contrast agents
Agent category
Name
Benefits
Limitations
Practical issues
Positive
(high T1 and high T2)
• Gadolinium chelates
• Manganese
• Milk with high fat content
• Fruit juices (e.g. pineapple, blueberry)
Limit detection of subtle mucosal abnormality or wall enhancement
Cost, availability
Negative
• SPIO
• Feruomoxsil oral
Improve conspicuity of wall oedema
Unpleasant taste, Cost
Biphasic
(low T1 high T2)
• Water
• Methylcellulose
• Mannitol or mannitol with locust bean gum
• PEG (polyethylene glycol)
• VoLumen® (Sorbitol solution with low-density barium)
High intrinsic contrast between wall and lumen allows assessment of subtle fold thickening
Distension with agents such as water inconsistent
The hyperosmolar agents may promote diarrhoea. Isosmolar agents should be used
Absorption, taste, diarrhoea. These are the most frequently used in today’s practice
In our department we utilize a technique that is well reported in the literature and consists in a total volume of between 1–2 L of contrast being ingested in divided aliquots over a 45–60 min time period. Water is an undesirable biphasic contrast agent due to its rapid absorption and erratic distension of the distal small bowel. This can be problematic as the distal small bowel is most commonly involved in Crohn’s disease. There are many commercially available biphasic contrast agents. In our practice we have utilized both dilute barium 0.1 % wt/vol solution with sorbitol as well as a bulk fibre laxative, which helps luminal expansion by retaining water. High osmotic agents such as mannitol and sorbitol can have undesirable side effects depending on the sugar alcohol concentration. They can cause diarrhoea, excessive gas and cramping. This can be improved by keeping the concentration below 2.5 %.
An optional method for simultaneous large bowel assessment is administration of a rectal water enema. This allows the colonic wall to be examined for disease involvement (vide infra).
Intravenous Contrast Material
Gadolinium derivatives are typically administered intravenously at a dose of 0.2 mmol/kg body weight. Peak bowel enhancement is thought to occur between 70 and 75 s following contrast material administration but can vary between individuals [38]. It is therefore standard practice to perform multi-phasic MRI commencing in the arterial phase at 25 s and obtaining at least two further acquisitions. If patient is know to have strictures, the addition of a delayed (7 min) phase is a consideration, as it better allows the characterization of the presence/degree of wall fibrosis [39]. In circumstances where gadolinium usage is relatively or absolutely contra-indicated, unenhanced sequences usually suffice in demonstrated areas of mural abnormality as well as mesenteric hyperaemia in diseased segments.
MR Motility Imaging
MRE allows not only the static display of morphology but can be combined with ultrafast imaging techniques (“cine MRI” or “MR fluoroscopy”) for analysis of bowel motility. Traditional X-ray fluoroscopic imaging confirms that involvement with Crohn’s may result in motility disorders. Pathological changes in the bowel wall result in areas of aperistalsis or diminished motility. When used in conjunction with routine MRE it can improve lesion detection. In a study performed to assess if cine MRI improves additional lesion detection in patients with Crohn’s, 40 patients with CD underwent cine MR enterography in addition to a standard MR protocol. Blinded reads were performed with and without cine MRI. Overall cine MRI detected more Crohn’s specific findings than static MR enterography alone (p = 0.007) and more patients with CD relevant MR findings (p = 0.03) [40].
There is growing literature supporting the use of cine MR enterography. Froehlich et al. [40] showed that the addition of cine MR enterography identified more patients with MR findings of Crohn’s disease compared to static MR enterography alone because altered motility on cine imaging highlighted abnormal bowel segments and may lead to increased diagnostic confidence and because Cine MR enterography can facilitate diagnosis in otherwise equivocal cases, especially if other sequences are motion-degraded. Abnormal motility on cine MR enterography in Crohn’s disease has also been shown to correlate with inflammatory markers, biopsy results, and clinical disease activity scores [41, 42].
Multiphasic imaging can also be used to evaluate for adhesions or stenoses and helps distinguish true strictures from temporarily contracting or underdistended segments [43] (Fig. 18.2). Cine MR enterography has also been shown to increase visualization of the proximal small bowel compared to static MR enterography, simulating the benefits of enteroclysis [44].
Fig. 18.2
Utility of cine-imaging to distinguish true stenosis from peristalsis. In (a) the loop involved with Crohn’s disease seems to be strictured, but in (b), an image acquired just a few seconds later using a MR fluoroscopic technique (SSFP based), the loop is seen to distend, demonstrated that the first image was acquired during a peristaltic contraction
Although still not widely used in routine clinical practice in most institutions, there is growing interest in cine MR enterography as a valuable technique for motility evaluation. The joint European Crohn’s and Colitis Organisation (ECCO) /European Society of Gastrointestinal and Abdominal Radiology (ESGAR) guidelines in 2013 acknowledge that small bowel motility evaluation may increase lesion detection in Crohn’s disease compared to static MR enterography alone [45]. The consensus statement from the Society of Abdominal Radiology (SAR) Crohn’s disease-focused panel published in 2015 includes multiphasic imaging as an optional additional sequence in MR enterography evaluation [46].
Cine MRI can be performed by single slice techniques, usually SSFP sequences, which are repeated at intervals of 0.5–1 s in the same plane but in a stepwise location from anterior to posterior. After the images are acquired, the cine loop function of the workstations allows visualization of bowel motility. Anti-spasmodics should not be administered until the cine MRI sequence is obtained, otherwise they will artificially reduce peristaltism. Consequently, the SSFP sequences that allow cine MRI are the first sequence in our protocol. Since with MR radiation is not utilized, potential sites of disease can be repeatedly evaluated without incurring any risk. It must be emphasized, however, that cine MRI does not have sufficient spatial resolution to be used in isolation when performing diagnostic MRI.
Role of Diffusion Weighted Imaging
Diffusion weighted imaging (DWI) relies on differences in the motion of water molecules between tissues to provide image contrast. It is more and more becoming a standard application in routine imaging and it has already been incorporated in two MRI scores (the Clermont score, which is very similar to the MaRIA score but replaces contrast enhancement by restricted diffusion), and the Nancy score [47], but DWI’s low spatial resolution is a drawback compared with the anatomical details provided by the high-resolution post- gadolinium sequences. It remains to be determined whether DWI’s low specificity for detecting activity [47], can be overcome by including it in an overall index. However, in the presence of other imaging findings of inflammation, DWI is associated with more severe disease [48] (Fig. 18.3).
Fig. 18.3
Utility of DWI to discriminate segments with more severe disease. (a), (b) and (c) are from the same patient and with the same window and level parameters. Diffusion is significantly more restricted in the segment of image a, representing more severe disease
In the future, if DWI is proven to be of benefit in larger patient groups, it may circumvent the need for gadolinium and potentially avoid issues related to cost and patient safety with this intravenous contrast media.
MR Colonography (MRC)
Conventional colonoscopy remains the gold standard for mucosal evaluation of the colon and allows biopsy performance for histological confirmation of a suspected diagnosis of inflammatory bowel disease. Entire colonic visualization and stepwise biopsies are considered mandatory and IBD is typically correctly classified in 80–90 % of cases at the time of initial examination. In specific circumstances, however, imaging is a suitable alternative for the establishment of disease extent and severity. These include the presence of a fulminant colitis when the patient is at higher risk of colonic perforation. Similarly, for both patient and technical reasons, incomplete colonoscopy may preclude colonic assessment in between 5–20 % of cases. Additionally, submucosal and mesenteric involvement, which is common in Crohn’s disease, cannot be assessed with colonoscopy; consequently, the evaluation of the mucosa with colonoscopy alone may result in underestimation of the extent and activity of the disease, as when assessing small bowel involvement. Imaging is also invaluable for assessment of colonic anastomoses [49]. The assessment of an anastamosis can be challenging on endoscopy and is the most common site of disease recurrence.
MRC Technique
Routine bowel cleansing is performed as for optical colonoscopy. Replacing standard cleansing with faecal tagging is not advocated in this patient subgroup as compared with those undergoing screening examinations for colorectal cancer [50].
Adequate colonic distension is a requisite in order to minimize false positive or false negative studies. MR colonography can also be performed with positive, negative or biphasic agents. A warm tap water enema has the ideal characteristics of a biphasic agent being of low signal intensity on T1-weighted and high signal on T2-weighted sequences. A volume of between 1.5–2.5 L is administered via a rectal catheter once the patient is on the table.
Routine utilization of an anti-peristaltic agent (Hyoscine 20 mg, or Glucagon 1 mg) produces reflex atonia that helps in retention of the water enema. In addition it minimizes peristaltic artefacts as well as achieving more optimal colonic distension.
When MR Colonography is performed, it is usually as part of a MR entero-colonography study and the pulse sequences performed are the ones obtained for regular MR enterography (previously described). Of note, the MaRIA score , defined previously, was deducted with a MR entero-colonography protocol.
MR colonography may also be performed without the enterography component. The obtained pulse sequences are similar to the ones obtained for the regular MR enterography: a combination of SSFP, T2 weighted and fat-suppressed T1 weighted post-gadolinium 3D sequences (e.g. VIBE, LAVA or similar). A SSFP sequence allows initial evaluation to see if there is adequate colonic distension. A multiphasic post-contrast acquisition is performed, as for the regular MR enterography.
Imaging Findings
Ulcerative Colitis
Classic findings on imaging include involvement of the rectosigmoid colon which extends proximally to involve the entire colon. Less commonly there is a sub-total colitis (usually right sided) and in 15 % of cases there may be a backwash ileitis.
Uniform thickening of the wall is a hallmark feature. The degree of thickening is usually less marked in UC than in CD with mean values of 7–8 mm as compared with 13 mm respectively. In more active disease however mural thickness can exceed 10 mm. Mural stratification is observed in 60 % of patients with UC versus 8 % of patients with CD [51]. This is due to the presence of fat or oedema in the submucosal layer as described in the small bowel above.
The outer contour of the colonic wall is typically smooth and regular in patients with UC whereas serosal and outer mural irregularity is seen in 80 % of patients with CD (Gore RM et al., AJR Am J Roentgenol, 158(1):59–61.). However, not infrequently, the two diseases are not distinguishable by imaging alone (Fig. 18.4).
Fig. 18.4
Pancolitis could represent both Crohn’s disease or UC. This particular patient had Crohn’s disease
As in Crohn’s disease, there is frequently engorgement of the vasa recta and mucosal hyperenhancement, as well as enlargement of regional pericolonic nodes. The presence of small traces of peri-colonic fluid is usually a marker of focal serosal involvement and typically indicates the presence of severe disease.
In long standing disease there will be wall thickening, an absence of haustra and associated luminal narrowing. This is thought to be due to hypertrophy of the muscularis mucosa. Mesenteric fatty proliferation in UC is typically confined to the perirectal space.
Ulcerative colitis is much less frequently an indication for MRE or MRC than Crohn’s disease. The most frequent indication for patients with UC is to rule out Crohn’s disease.
Crohn’s Disease
Involvement of the colon can be seen in more than 60 % of patients with CD and is exclusively limited to the colon in approximately 15–25 % of cases. The rectum may be involved in approximately 50 % of patients.
As in the small bowel, colonic wall thickening is present and post contrast enhancement is a good correlate of disease severity. The inner profile of the colonic wall may have an undulating configuration. This is thought to represent mucosal oedema and there may also be a relative absence of haustration for the same reason.
Other imaging findings that overlap with those in the small bowel include the presence of fistulae and sinus tracts.
Long standing quiescent disease may depict no abnormality on imaging. If however there is transmural fibrosis there is shortening of the bowel with ahaustration. This results in a relatively fixed and tubular configuration to the bowel. On post gadolinium sequences there is homogenous enhancement and absence of wall stratification.
Diagnostic Accuracy
A study by Ajaj et al. [49] assessed 23 patients with IBD on MR colonography. The imaging findings (MRC score) were correlated with histopathological specimens obtained on endoscopy. In this study group, MRC correctly identified 68 of 73 segments found to reveal IBD changes on pathology. The imaging score utilized four quantifiable criteria including colonic wall thickness, colonic wall enhancement, number of haustral folds and number of perienteric nodes. There were no false positive findings. MRC detected and characterized clinically relevant IBD of the large bowel with sensitivity and specificity values of 87 % and 100 %.
Rottgen et al. correlated bowel enhancement on MRC with inflammatory activity of Crohn’s disease at colonoscopy in 42 patients and found a significant correlation between colonoscopic inflammatory activity and changes in signal intensity within the bowel wall. These relatively modest patient numbers need to be replicated in larger cohorts however the data suggests that MRC is a credible alternate to conventional colonoscopy in both monitoring activity as well as evaluating therapeutic response [52].
Characteristic Imaging Findings
The earliest changes of Crohn’s disease such as erythema, superficial apthous ulcers and nodularity of the mucosa are difficult to appreciate on MR. An attempt to address this deficiency has been made by authors who have obtained high resolution thin section images (2–3 mm thick) aligned parallel to the bowel segment [53]. This allows a detailed depiction of the mucosa and provides in plane resolution of 1–2 mm.
However, there are several imaging findings that are characteristic of inflammatory bowel disease and they are discussed in some detail below.
Wall, Fold and Mucosal Abnormality
A normal bowel wall should be no more than 3 mm in thickness if it is optimally distended. In CD, wall thickness ranges between 5–10 mm. The degree of mural thickening correlates well with the Crohn’s disease activity index (CDAI) [54]. In the absence of mural oedema, the bowel wall is usually low to moderate in signal intensity on T2-weighted MR sequences. The black boundary artefact seen on SSFP sequences can confound assessment of wall thickness. HASTE sequences are relatively insensitive to this artefact and more accurate at estimating bowel thickness (Fig. 18.5).
Fig. 18.5
Mural thickening . Distal ileal segment demonstrates wall thickening. Part (a) is a SSFP image and an India ink artefact at the interface with the mesenteric fat can be seen. Part (b) is a T2 fat-saturated image. The bright signal in the submucosa represents oedema and is in keeping with active disease (significant inflammatory component). The same segment is demonstrated in (c), a T1 weighted fat-saturated image post contrast administration
Fold abnormalities are more evident along the mesenteric border. They can manifest in several ways including diffuse fold thickening, ulceration or in more severe disease as areas of cobblestoning. Early areas of apthous ulceration are seen as small focus of high T2 signal intensity surrounded by a rim of oedema (seen as an area of moderate signal intensity), but these are usually difficult to see with MR. Deeper areas of penetrating ulcers are easier to appreciate than superficial ulcers. They are seen as areas of high T2 signal intensity within areas of segmental wall thickening (Fig. 18.6).
Fig. 18.6
Ulcers . Multiple ulcers can be seen in (a) (SSFP image). In (b), a T2 fat-saturated image, both superficial (arrowheads) and deep (arrows) can be identified. Subtle ulcers can also be seen in (c) (arrow), a CAIPIRINHA image
Strictures
These are seen as fixed, consistent areas of luminal narrowing. If there is upstream dilatation of bowel loops by greater than 3 cm, the stricture is considered to be functionally significant. If however there is no dilatation and a more than 10 % narrowing in the lumen as compared with subjacent bowel, the stricture is most likely functionally insignificant.
As recently proven by many studies, most stenotic lesions in CD have a mixed component: fibrosis plus inflammation [55, 56]. Differentiating the presence of significant inflammation, significant fibrosis and/or which component predominantes has important prognostic and management implications, and MRI can contribute significantly here.
The presence of ulcerations, acute mural oedema (areas of high T2-weighted signal intensity within thickened loops of small bowel on fat-saturated T2 weighted sequences) and mural thickening is associated with presence of inflammation. High submucosal T2 signal is also an independent correlate of disease activity [57, 58] (Fig. 18.7).
Fig. 18.7
Submucosal oedema , sign of active disease. A wall thickened and hyperenhancing ileal segment is demonstrated. In (a) several areas of high T2 signal in the submucosa are demonstrated, represent oedema. Findings are in keeping with active disease
Fibrotic strictures tend to be hypointense on T1- and T2-weighted sequences and enhance inhomogenously following contrast. There is an absence of accompanying mesenteric hyperaemia or inflammatory change. They may cause bowel obstruction and MR fluoroscopic sequences can be helpful in locating the level and degree of obstruction. A recent publication from Rimola et al. demonstrated prospectively and with pathological correlation that the assessment of gadolinium enhancement over time allows the identification of segments with a high component of fibrosis, regardless of the degree of coexisting inflammation. In their publication, >24 % of enhancement from the 70 s acquisition to a 7 min delay acquisition was strongly associated with severe fibrosis [39] (Fig. 18.8).
Fig. 18.8
Delayed enhancement, sign of significant fibrosis . Multiple stenotic segments with pseudosacculation are identified. Of note, there is progressive enhancement from image (a) (enteric phase) to image (b) (5 min delay), in keeping with presence of significant fibrosis
Multiple other investigators have analyzed numerous pulse sequences and imaging methods to estimate the degree of fibrosis in an effort to estimate the potential for medical response to therapy. Magnetization transfer MR imaging has been shown in animal studies to depict intestinal fibrosis [59], and initial experience in patients has shown that magnetization transfer ratios are elevated in patients with predominantly fibrotic strictures [60]. Zappa et al. examined inflammation and fibrosis at MRI by comparison with histopathologic scoring systems and found a high correlation between advanced inflammation and advanced fibrosis [55], so reliance on enhancement, so separation of these two processes was difficult when relying upon imaging findings such as wall thickness and hyperenhancement. Further investigation into reliable imaging markers for intestinal fibrosis such as magnetization transfer, diffusion-weighted imaging, and delayed enhancement is ongoing.
Fatty replacement of the sub-mucosa is also seen in long standing IBD and is seen as an area of high signal intensity on non-fat-saturated T1 and T2 sequences , which suppresses on fat-saturated sequences.