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Over the years, radiological examinations for small and large bowel are radically changed: milestones were the introduction of barium meals in the 1950s, of enteroclysis in the 1980s, and of cross-sectional techniques in the 1990s.

Until the 1980s, gold standard examinations were the small bowel follow-through (SBFT) [1] and the single-contrast colon enema [2]. In the 1980s, Sellink JL [3], Herlinger H [4], and Maglinte DD [5] developed single- and double-contrast small bowel enteroclysis, while Welin S [6], Altaras J [7], and Cittadini G [8] encoded the method of the double-contrast barium enema of the colon. These examinations provide an extraordinary evaluation of the mucosal layer with a reported sensitivity and a specificity respectively of 85–95 % and 89–94 % in the detection of the typical Crohn’s disease lesions, when performed by expert radiologists [9]. Unfortunately, they give only indirect information on transmural and extraintestinal involvement, with difficulties in the assessment of single bowel loops, even if displayed in transparency [10].

Since the second half of the 1990s, already known cross-sectional techniques, mainly CT and MRI, have been specifically developed for the assessment of gastrointestinal pathology [11], with excellent results. These examinations allow a simultaneous evaluation of mucosal, mural, and extraintestinal pathologies without any possible superposition of bowel loops.

Conventional techniques have so largely lost their role in the everyday clinical practice, being less and less used in the last years. Only plain abdominal film still plays a role as the first-line examination in the acute abdomen, being able to identify signs of obstruction and perforation (Fig. 8.1).

Fig. 8.1
figure 1

Acute ileal obstruction. Plain abdominal film (a) shows signs of acute obstruction (small bowel loop distension with multiple air-fluid levels). Contrast-enhanced CT (b) detects a Crohn’s stenotic lesion of the last ileal loop (arrow in b)

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Each cross-sectional imaging technique is characterized by peculiar advantages and limitations (diagnostic accuracy, availability, cost, X-ray dose, spatial and contrast resolution). In some circumstances, different modalities can be used to complement each other [12].

8.1 Technical Principles of Cross-Sectional Techniques

The most used cross-sectional techniques for the evaluation of small and large bowel are ultrasound, CT, and MRI. They share some essential technical common points that must be satisfied:

  • Intestinal cleansing

  • Bowel distension

  • Bowel wall enhancement

8.1.1 Intestinal Cleansing

The aim of a complete cleansing is to remove residual stool, which obviously may mimic pathologic findings; it also allows an easier anterograde and retrograde bowel filling.

8.1.2 Bowel Distension

An optimal distention allows a correct and complete evaluation of the bowel, since collapsed intestinal loops can hide small lesions or mimic diseases, so leading to false-positive or false-negative results.

In the past, it was widely debated about the most performing route of administration of enteral contrast media, and if positive contrast agents (baritated or iodinated), neutral (water solutions), or negative ones (air or carbon dioxide) were to be preferred. Enteral contrast agent can be orally administrated, infused through a nasojejunal tube or retrograde introducted by an enema [13].

8.1.3 Bowel Wall Enhancement

The injection of intravenous contrast media ensures bowel wall enhancement, improving contrast resolution and allowing to distinguish between different mural layers. In this way, it is possible to combine anatomical and functional information. In fact a functional analysis of bowel wall microcirculation allows to get the right differential diagnosis between different inflammatory diseases or between inflammations and tumors. Intravenous contrast media injection also provides an overall enhancement of the entire abdomen, improving the detection of extraintestinal findings, related to Crohn’s disease or unexpected.

8.2 Small Bowel

Due to its anatomical location, the small bowel remains beyond the reach of conventional upper and lower endoscopy techniques, and a radiological evaluation of luminal and extraluminal findings is still quite a challenge.

8.2.1 Ultrasound

In the last decade, interesting results were reported about the use of ultrasound (US) in many common intestinal diseases, such as appendicitis, diverticulitis, bowel obstructions, and Crohn’s disease [14]. Right iliac fossa and its structures, as cecum and last ileal loop, could be properly evaluated by ultrasound. So Crohn’s lesions of the last ileal loop can be detected, while early ileal lesions localized elsewhere are still challenging findings, due to the lack of sure anatomical landmarks. For these reasons, a fully comprehensive examination of all ileal loops is rarely achievable, leading to a possible false-negative examination. Ultrasound can also detect and characterize bowel mural thickening and strictures that are Crohn’s typical pathologic findings. It has been reported that the cause of small bowel obstructions can be sonographically detected up to 76 % of the patients [14]. Also the presence of mesenteric nodes, phlegmon, and abscesses can be quite easily identified, even if with less accuracy than CT.

An improvement in small bowel evaluation with ultrasound is the use of SICUS (small intestine contrast ultrasonography with oral administration of enteral contrast medium) or CEUS (contrast-enhanced ultrasonography) [9]. However, the timing and costs of these US techniques are similar to CT ones but with less accuracy and less panoramic view.

Ultrasound strengths remain its wide availability and relatively low cost (except for CEUS).

Furthermore, ultrasound allows a continuous and direct contact with the patient during the examinations, with the possibility to use the probe as “a hand” to visit the patient.

Since Crohn’s disease is a chronic pathology needing multiple follow-ups and affecting also pediatric or very young patients, US can be safely implied, thanks to the lack of radiation exposure.

Ultrasound should be so considered as a valid first-line examination in symptomatic patients with suspected Crohn’s disease and a useful tool for the follow-up of already known lesions, especially when located in the last ileal loop. US however is unsuitable for lesion’s staging because it lacks of panoramic view.

The use of ultrasound in Crohn’s disease has however several limitations, and high dependence on the skillness of the operator remains the main one. The experience in the use of US for bowel disease evaluation is in fact still quite limited [11, 15].

8.2.2 CT

CT is an accurate and panoramic imaging technique ensuring the visualization of both the bowel and the surrounding structures.

In the past it was widely debated if positive contrast agents (baritated or iodinated) or neutral ones (water solutions) were to be preferred for bowel distension in CT examinations. Nowadays, neutral enteral agents are usually preferred. In fact they have attenuation values and signal intensity similar to water, allowing a better depiction of mesenteric wall. Positive contrast agent could be sometimes used in TC examinations in peculiar conditions, such as to better detect fistulous tracts.

Another controversial issue regards the route of administration of enteral contrast. Two main techniques have been proposed:

  • Enteroclysis, with infusion of neutral contrast material through a nasojejunal tube

  • Enterography, with oral administration of a nonabsorbable isotonic solution

With enteroclysis, a better luminal distension in both jejunal and ileal tracts in comparison to the one achieved with enterography, especially for jejunal loops, is achievable [16].

However, in Crohn’s disease, some studies demonstrated no significant difference in the overall detection of clinically significant findings [11] (Fig. 8.2). The question is still debated, and a consensus conference has been issued by The European Society of Gastrointestinal and Abdominal Radiology (ESGAR).

Fig. 8.2
figure 2

CT enteroclysis (CTE) vs. CT enterography (CTe). Both CTE (a) and CTe (b) show adequate luminal distension of small bowel loops and a Crohn’s lesion of the last ileal loop (arrow in a and b). Nasojejunal catheter in CTE (arrowhead in a)

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Usually, enterographic studies are preferred to the enteroclysis-based ones because they are easier to perform and better tolerated by the patient [10]. Patient’s discomfort due to nasojejunal catheter, along with the radiation exposure during its placing (about 0.5–1 mSv), is an important disadvantage of enteroclysis [11, 17].

According to our experience, the most performing examination is obtained with the association of a small bowel enterography to a colon water enema [18]. CT enterography of small bowel associated with colon water enema (CTe-WE) allows a simultaneous, combined, and constant distension of both small and large bowels, with some limitations only in the depiction of jejunum loops. With this technique, it is so possible to obtain a whole digestive tube examination with high diagnostic accuracy, allowing to simultaneously detect pathologic findings in different gastrointestinal tracts [13] (Fig. 8.3).

Fig. 8.3
figure 3

CTe-WE. Typical trilaminar mural stratification of Crohn’s disease (arrowheads in a and b) seen on axial (a) and coronal (b) planes. Curved reformatted image (c) shows multiple inflammatory skip lesions involving the terminal ileum (arrowheads in c)

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Regardless of the bowel filling technique, the injection of intravenous iodinated contrast media ensures mural and mucosal enhancement, improving contrast resolution, so allowing to detect the typical trilaminar mural stratification of Crohn’s disease.

Nowadays, CT is the most comprehensive, accurate, and repeatable radiological examination for Crohn’s disease evaluation. CT limitations remain the use of ionizing radiations and the need of intravenous injection of iodinated contrast media, possibly leading to acute adverse reactions and to renal failure. New reduction dose techniques have overcome the problem of ionizing radiation, and this result probably will improve in the future. Cost to replace older equipment is the only present limitation to the spread of these new reduction dose techniques [11]. The other limitation due to the need of contrast media could be overcome by using new drugs, but unfortunately, iodinated ones are the only choice on the market, probably because of their low production costs. Anyway a substantial contrast media dose reduction can be achieved with new dual-energy CT scanners [19].

Nowadays, CT allows an almost infinite number of planar or curved reconstructions, thanks to volume acquisitions with isotropic and submillimeter voxel, with advanced workstation’s post-processing. A multiplanar assessment is particularly useful for bowel’s evaluation: according to the anatomical orientation of ileal loops, the best plane for bowel examination is in fact the coronal one.

8.2.3 MRI

Magnetic resonance imaging of small bowel is mainly based on T1-weighted images with and without paramagnetic contrast media injection, T2-weighted images with and without fat suppression technique, and diffusion-weighted images (DWI), in multiplanar scansions (Fig. 8.4).

Fig. 8.4
figure 4

MR enterography. (a) Axial T2-weighted acquisition with fat suppression. (b, c) Coronal GET1 acquisition with fat suppression. Crohn’s lesion of the last ileal loop (arrowheads) with enlarged local nodes (arrow in c), better shown on coronal planes after paramagnetic contrast media injection (c)

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MR enteroclysis (MREc) and MR enterography (MRE) share common technical points with CT-based enteroclysis and enterography techniques. Like CT examinations, the bowel must be adequately cleansed, distended, and enhanced. The most performing route of administration of the endoluminal contrast media is still debated [9, 20].

The spatial resolution achievable with MRI is lower than with CT [17], but MRI demonstrated higher contrast resolution. The use of intravenous contrast media, as for CT and US, could improve the detection of bowel hyperemia and edema and of inflammatory mucosal erosions and ulcers. These typical Crohn’s disease signs are useful to assess the activity grade of the pathology. MRI seems to be superior also in the detection of fistulous tracts [16], a common Crohn’s complication.

Another advantage of MRI is the possibility to evaluate bowel motility, with the use of fast T2-weighted SSFP or echo planar imaging sequences comprehensively called “MRI-fluoroscopy sequences” that can be visualized in a cine-like mode [17]. A chronic Crohn’s fibrotic stricture is shown as aperistaltic [16], while an acute inflammatory one may present wall spasms and hyperenhancement. New studies have to be done in order to develop MR motility imaging, but interesting results about the improvement of Crohn’s disease lesions detection are encouraging [21, 22]. The possibility to check bowel motility and its grade of filling is also very useful during the technical execution of MRI with the possibility to achieve better bowel distension.

Other recent MRI innovation is the analysis of Brownian motion of water among cellular structures using diffusion-weighted imaging (DWI) [23, 24]. Although it is already known that DWI signal and ADC values directly reflect tissue structure, recent studies have reported a higher sensibility of these sequences in the detection of bowel inflammatory lesions compared with contrast-enhanced MR imaging [25].

The longer time of acquisition, the lower spatial resolution, the low availability, and the higher cost of the examination suggest the use of magnetic resonance imaging only in selected patients. MRI should be preferred in pediatric or very young patients who need multiple follow-ups over a lifetime [10, 16], in patients with known chronic renal failure, or in patients allergic to iodinated contrast media.

8.2.4 Endoscopy

Small bowel loops cannot be reached easily by conventional upper and lower endoscopy. In order to overcome this limitation, new endoscopic techniques have been used, such as single-balloon endoscopy (SBE) [26] and double-balloon endoscopy (DBE) [27, 28]. The main advantages of endoscopic examinations are the availability of biopsies and the possibility to perform therapeutic procedures such as balloon dilatation of stenosis [29]. However, these endoscopic techniques have great limitations: they are not universally available and it takes quite long time to be performed. Furthermore, they highly depend on the operator experience, on the patient’s conditions, and on the number and the entity of ileal stenosis.

8.2.5 Capsule

Video capsule endoscopy (VCE) [10, 29] is an alternative technique used for small and large bowel investigation. The patient swallows a capsule of less than 2 cm of length lighting the lumen and acquiring about 2 images per second during its way. All data are radiotransmitted wireless to an external recorder [11]. Capsule endoscopy should be performed mainly in case of suspected gastrointestinal bleeding with previous negative upper and lower endoscopy [30, 31]. The main limitation of capsule endoscopy is its possible retention in case of bowel strictures, quite common in Crohn’s disease. To overcome this limitation, the proper VCE capsule should be administrated only after capsule patency test, implying the previous use of a dissolvable capsule.

Furthermore, capsule is able to demonstrate nonspecific mucosal ulcers only, so resulting poor in the assessment of typical Crohn’s mural involvement. High costs and long time for interpretation are other limitations of this technique. The European consensus group [32] recommends the use of capsule endoscopy when standard imaging techniques and endoscopy cannot detect the pathology [11], mainly in the suspect of angiodysplastic lesions.

8.2.6 Nuclear Medicine

Nowadays, nuclear medicine has no more a main role in the diagnosis of Crohn’s disease, except for differential diagnosis between Crohn’s lesion and Meckel’s diverticulum by means of scintigraphy and in case of suspected neoplastic degeneration of chronic Crohn’s lesions with the use of fluorodeoxyglucose positron emission tomography CT (18F-FDG PET-CT).

Generally, nuclear medicine examinations could be performed when other imaging modalities have been negative [11].

8.3 Large Bowel

8.3.1 Ultrasound

Ultrasound examinations in Crohn’s disease have a role in the detection and evaluation of lesions localized in the cecum and in the differential diagnosis between inflammatory bowel diseases and acute appendicitis in acute scenarios. It can be also performed to evaluate Crohn’s perianal complications, such as fistula and abscesses [33].

8.3.2 CT

Two main CT techniques have been developed to adequately analyze the large bowel:

  • CT with water enema (CT-WE), with introduction of tap water through a rectal enema in a previously cleansed colon, with the patient placed on the CT table. The neutral contrast agent may sometimes reflux through the ileocecal valve from the cecum into the ileum, revealing pathologic findings of the last ileal loop. An intravenous iodinated contrast media injection ensures mural and mucosal enhancement, improving contrast resolution.

  • Computed tomographic colonography (CTC) or virtual colonoscopy (VC), with inflation of air or carbon dioxide through a rectal catheter. The morphology of colonic surface is emphasized by reflections arising from a virtual external light source, obtaining images similar to conventional endoscopic vision.

Main advantages of CTC over CT-WE are the lower X-ray dose and the absence of iodinated contrast media injection. Nowadays, CTC is included as a colorectal cancer (CRC) screening option for asymptomatic average-risk adults aged 50 years and older [34].

However, polyps are not pathognomonic findings of Crohn’s disease. Main Crohn’s pathological signs are hyperemic thickening of bowel wall and perienteric fat stranding with engorged vasa recta, better depicted by CT-WE.

In the case of CTC, air or carbon dioxide is used to achieve lumen distension. The gas provides an extreme HU difference between bowel wall and the lumen. This extreme HU difference affects the bowel enhancement evaluation. In CT-WE, water is used to distend the lumen, and a better wall-lumen interface is achieved, allowing to distinguish the three-layered structure of the bowel walls and to easily detect Crohn’s lesions [35]. For these reasons, CT-WE in Crohn’s disease seems to be superior to CTC.

8.3.3 MRI

MR colonography (MRC) is a recent colonic imaging technique offering an alternative to CTC without the use of ionizing radiations [36]. Similar to CTC, colon distension is commonly achieved by inflaction of air or carbon dioxide. Data on the accuracy of MRI colonography for the detection of inflammatory colonic lesions in IBD are still limited.

MR imaging, due to its high contrast resolution, is instead the most accurate tool to evaluate Crohn’s perianal complications: fistulous tracts, abscesses, and their anatomical relationship with pelvic floor muscles are very well depicted.

8.3.4 Colonoscopy

Conventional colonoscopy is currently considered the reference standard for the evaluation of inflammatory bowel diseases. However, technical failure of colonoscopy is not uncommon. Causes of incomplete colonoscopy are anatomic variants, patient intolerance, strictures, and severe diverticulosis. Up to 10 % of colonoscopy is technically difficult, even if performed by skilled operators [37]. Moreover, optical colonoscopy is poorly tolerated diagnostic procedure with possible complications, mainly represented by bowel perforation [9].

8. Conclusions

Nowadays, cross-sectional imaging techniques, mainly CT and MRI, have overtaken the conventional radiological methods for the evaluation of small and large bowel, with the possibility to detect both luminal and extraluminal pathological findings [10].

The wider availability of CT equipments, the lower cost of the examination and the rapidity of image acquisition, with less motion artifacts, and a better patient’s compliance represent strengths of CT over MR imaging. In fact, with a 64-slice CT equipment, it is possible to cover the entire abdomen and the pelvis in less than 10 s, while the acquisition of standard MRI sequences for a complete small bowel examination needs approximately 20 min [17].

The sensitivity and specificity of CT and MRI techniques are however referred to be overall comparable [38–43], both in excess of 90 % and 80 %, respectively [11], and so the choice of the best examination has to be suited to the needs of each patient.

Nowadays, CT could be the technique of choice in the detection and follow-up of inflammatory pathologies [15] especially when occurred complications are suspected. MRI should be preferred in pediatric or very young patients who need multiple follow-ups over a lifetime [10, 16], in patients with known chronic renal failure, or in patients allergic to iodinated contrast media.