Abstract
Small bowel neoplasms, including adenocarcinoma, carcinoid tumour, lymphoma and gastrointestinal stromal tumours, represent a small percentage of gastrointestinal cancers, yet are among those with the poorest prognosis compared with other gastrointestinal malignancies. Unclear clinical scenarios and difficult radiological diagnosis often delay treatment with negative effects on patient survival. Recently, multidetector CT (MDCT) and MRI have been introduced as feasible and accurate diagnostic techniques for the identification and staging of small bowel neoplasms. These techniques are gradually replacing conventional barium radiography as the tool of choice. However, the inherent technical and physiological challenges of small bowel imaging require a familiarity with patient preparation and scan protocols. Adequate knowledge of the histopathology and natural evolution of small bowel neoplasms is also important for differential diagnosis. The aim of this article is to review MDCT and MRI protocols for the evaluation of small bowel tumours and to provide a concise yet comprehensive guide to the most relevant imaging features relative to histopathology.
The small intestine (SI) accounts for 75% of the length and 90% of the mucosal surface of the alimentary tract; however, because of certain unique physiological features (rapid transit, alkaline content, IgA secretion and lymphoid tissue) it is the site of only 2–6% of all gastrointestinal (GI) neoplasms [1,2]. Data from the United State Surveillance Epidemiology and End Results (SEER) programme from 2002 to 2006 [3] show an age-adjusted incidence rate for malignant tumours of 1.9 per 100 000 men and women per year with an age-adjusted death rate of 0.4 per 100 000 men and women per year. Apart from obscure GI bleeding, patients may present with non-specific complaints such as abdominal pain (60%), anaemia (50%), nausea and vomiting (50%), weight loss (40%), diarrhoea (30%) and intestinal obstruction (30%) [4]. However, many patients may remain asymptomatic until the late stages of disease. SI neoplasms are also difficult to identify at diagnostic imaging and as a result delays in diagnosis are common. Maglinte et al [5] estimated that while delays in diagnosis of less than 2 months were common because the patient failed to report symptoms, extended delays occurred as a result of the physician not ordering the appropriate examinations (>8 months) and/or because the radiologist failed to make the correct diagnosis (approximately 12 months). An unfortunate consequence of late diagnosis is poor prognosis [3]. 5 year survival rates range from 0–28% for adenocarcinoma, 14–30% for lymphoma and 60% for carcinoid tumours.
Until recently, barium enteroclysis has been considered the most accurate radiological modality to detect small bowel malignancies [6]. However, this technique requires duodenal intubation and direct injection of barium and methylcellulose into the intestinal lumen and is both time-consuming and poorly tolerated by patients. Furthermore, barium enteroclysis is limited in its ability to accurately depict the mural and extramural extent of disease [6]. Alternatives to barium enteroclysis for imaging the SI are multidetector CT (MDCT) and MRI. Both techniques have good potential for the early diagnosis of both inflammatory and neoplastic conditions. The aims of this review are to present MDCT and MRI protocols for SI imaging, to describe the typical imaging features of common SI neoplasms and to correlate radiological findings with specific histopathological characteristics.
Imaging techniques
Patient preparation
MDCT
The patient should fast on the day of the examination to reduce alimentary residue in the GI tract, which may lead to inhomogeneous intraluminal attenuation. Because the SI can be partly or fully collapsed under normal physiological conditions, luminal distension is a necessary pre-requisite for imaging because collapsed bowel loops can hide even large lesions or mimic wall thickening. Whereas both MRI [7] and MDCT enteroclysis [8] allow optimal lumen distension, oral administration of contrast agent with the proper choice of oral contrast material and adequate timing can produce good results [9,10], is more patient-friendly and less time consuming. For MDCT, the choice of oral contrast agent is usually determined by the anatomical SI region of interest and the clinical question to be answered (Figure 1). While water is often a good option to distend the duodenum and the proximal tract of the jejunum (1–1.5 l of tap water given 10–15 min before examination, with the last 2–3 glasses drunk in the CT room) [11], imaging of the distal jejunum and/or ileum requires a different approach, since water is rapidly absorbed by the intestinal wall during its transit through the lumen. For these regions, a low-concentration contrast agent with bland osmotic activity represents the best compromise between bowel distension and lumen attenuation. Such contrast mixtures (e.g. water, sorbitol and 0.1% barium sulphate) typically require fractioned administration over a period of 50–65 min before the examination [12]. Highly concentrated barium or iodine solutions must be avoided because too high an intraluminal attenuation can jeopardise the identification of small hypervascular masses (i.e. carcinoid tumours) or compromise the evaluation of mesenteric vessels [13,14]. The use of peristalsis inhibitors such hyoscine N-butyl bromide (HBB, Buscopan Boehringer Ingelheim GmbH, Ingelheim am Rhein, Germany) is strongly recommended (intravenous administration after completing intestinal preparation) in order to prolong lumen distension and avoid movement artefacts.
MRI
The dietary recommendations are similar to those for MDCT. Oral contrast agents for MRI can be classified as positive, negative or biphasic according to their action on the signal intensity of bowel lumen [15] (Figure 2). Positive contrast agents are paramagnetic, i.e. water-based gadolinium (Gd) solutions that produce high-signal intensity (the so-called “luminographic” effect) on both T1 and T2 weighted sequences [16]. The main limitations of this approach are the relative high cost and the fact that wall enhancement after intravenous Gd administration can be masked by the higher lumen signal on T1 weighted sequences [17]. Negative contrast agents are superparamagnetic, i.e. water-based solutions of iron oxide particles coated with silicone that produce low-signal intensity (the so-called “dark-lumen” effect) on both T1 and T2 weighted sequences [16]. Although these agents often permit better visualisation of bowel wall and mesenteric fat oedema on T2 weighted sequences [18,19], magnetic susceptibility artefacts that affect image quality may occur on gradient-echo sequences. Biphasic contrast agents are water solutions of hyperosmotic compounds (i.e. polyethelenglycol) that produce both the luminographic effect on T2 weighted sequences and the dark lumen appearance on T1 weighted sequences [16]. Biphasic agents represent the most flexible solution, with the advantage of cost containment [20,21]. MR-enteroclysis with naso-jejunal intubation and 1500–3000 ml of contrast agent (administered at 80–150 ml min−1 using infusion pumps) has proven to be highly effective for the detection of inflammatory bowel diseases and SI cancers [7]. However, in most patients adequate intestinal distension can be obtained with a conventional per os preparation (600 ml to 1 l of tap water with polyethelenglycol for 20–30 min before the examination). Moreover, since there is no radiation exposure, bowel distension can be monitored dynamically and adjusted during the examination [15]. Once sufficient bowel distension is achieved, peristalsis inhibitors may be used to suppress motility induced artefacts that can produce proton dephasation inside the lumen, mimicking filling defects on T2 weighted images.
Imaging protocol
MDCT
A preliminary unenhanced acquisition of the whole abdomen from the dome of the diaphragm to the pelvis is recommended in order to properly detect mesenteric calcifications or intraluminal bleeding and for the imaging of liver parenchyma if a malignancy is suspected. Thereafter, depending on the indication, arterial and/or portal venous phase imaging [14,22] must be performed after intravenous administration of contrast agent (2 ml kg−1 at 3.5–4 ml s−1). Bolus tracking techniques with measurements performed in the abdominal aorta can be used to adapt the delay between contrast agent administration and scan initiation to the cardiac output of the individual patient; however, delays of 35–40 s and 60–65 s are often appropriate for arterial and portal-venous phase acquisitions, respectively. Arterial phase imaging is recommended when a strongly enhancing lesion (e.g. neuroendocrine tumours or metastases from melanoma) is suspected. When using a 4-slice scanner, a collimation of 4 × 2.5 mm should be considered the minimum setting to reconstruct 3 mm slices. Conversely, a collimation of 4 × 1 mm allows 1.25 mm slice reconstruction that can be adapted to image mesenteric vessels, but at the cost of a longer scan duration, which may exceed the breath-hold capability of frail patients. The availability of faster scanners permits the routine use of submillimetre collimations (16 × 0.75 mm and 64 × 0.75 mm) that can generate almost isotropic three-dimensional (3D) data sets from multiphasic acquisitions. Evaluation of MDCT data sets should be performed on off-line consoles dedicated for 3D reconstructions (the availability of maximum intensity projection and multiplanar reformatted images facilitates the evaluation of SB lumen and its relationship with adjacent vessels) [14,22].
MRI
The effects of breathing artefacts and bowel wall motion during data acquisition are the main causes of image degradation and poor diagnostic accuracy in MRI of the SI. For this reason later generation MRI scanners operating at 1.5–3 T are preferable while parallel imaging protocols and fast sequences are mandatory. Regarding acquisition geometry, the coronal plane optimally demonstrates the anatomy of the SI, mesentery and abdominal vessels, but additional axial and sagittal planes should also be considered for precise evaluation of the SI and to avoid problems with partial volume effects. According to most literature reports, there are three types of sequence that must be included in a complete MRI protocol for SI imaging:
The main advantage of T2 weighted fast spin-echo sequences, or turbo spin-echo (TSE) acquisitions, is the excellent soft-tissue contrast, which permits detection of diseased bowel segments and evaluation of the surrounding mesentery [23,24]. The use of half-Fourier acquisition single-shot turbo spin-echo (HASTE) technique increases the speed of acquisition resulting in reduced or absent movement artefacts [25]. On the other hand, these sequences are susceptible to flow-related artefacts (owing to the long echo time (TE)) and thus rapid peristaltic movements may result in intraluminal flow voids that may be perceived as pseudolesions.
True fast imaging with steady-state precession (true-FISP) sequences are fully balanced gradient-echo sequences and provide the highest signal among steady-state sequences. Contrast is a function of T1/T2. If short repetition time (TR) and TE are used the T1 portion remains constant and the images are mainly T2 weighted, with bowel lumen appearing hyperintense. The speed and motion insensitivity of the acquisition completely eliminates breathing or peristalsis induced artefacts [17,26]. Unlike the half-Fourier technique, intraluminal flow voids do not affect steady-state precession sequences; moreover, selective fat-suppression pulses can be used to increase the luminographic effect and remove “black boundary” artefacts caused by magnetic susceptibility [27,28].
T1 weighted spoiled gradient-echo (SPGRE) sequences with fat suppression are sequences that use a semi-random spoiler gradient after each echo to spoil the remaining transverse magnetisation. These T1 weighted sequences can be acquired as two dimensional (fewer motion artefacts) or 3D (higher spatial resolution) data sets. Their use after intravenous Gd administration permits excellent depiction of the mesenteric vessels and identification of hypervascular bowel walls if coupled with a selective spectral fat-suppression pulse [27,29,30].
Histopathology and imaging findings
Adenocarcinoma
Adenocarcinoma is the most common primary malignancy of the SI and accounts for 40% of cancers (Table 1). The predominant location of adenocarcinoma is the duodenum and proximal jejunum, with the incidence decreasing distally [31]. The exception to this presentation is seen in Crohn's disease, where most adenocarcinomas occur in the ileum. Adenocarcinomas may be polypoid, infiltrating or stenosing [32]. Duodenal adenocarcinomas are usually more circumscribed with a polypoid or protuberant appearance (Figure 3). Conversely, jejunal or ileal lesions tend to be larger, annular, constricting tumours with circumferential involvement of the intestine wall; at the time of diagnosis most show a fully parietal penetration and involvement of the serosal surface [33] (Table 2). An increased incidence of small bowel adenocarcinoma has been described in patients affected by familiary adenomatous polyposis (mainly periampullary) and Lynch syndrome. Small bowel carcinomas resemble their counterparts in the colon, but with a higher proportion of poorly differentiated tumours with glandular, squamous and undifferentiated neuroendocrine components [34].
Table 1. Epidemiology and demographics of small intestine neoplasms.
Histology | Incidence per year | m/f ratio | Risk factors | 5 year survival rate |
Adenocarcinoma | Overall = 0.4 per 100 000 | W m/f = 1.5 | Crohn disease, | 26.6–39% |
Wm = 30.8% | B m/f = 1.2 | coeliac disease, | ||
Wf = 32.7% | familiary adenomatous | |||
Bm = 37.2% | polyposis, | |||
Bf = 45.5% | Meckel diverticulum | |||
Carcinoid | Overall = 0.4 per 100 000 | W m/f = 1.4 | MEN1 | 60–76.5% |
Wm = 36.0% | B m/f = 1.6 | |||
Wf = 39.2% | ||||
Bm = 43.9% | ||||
Bf = 39.7% | ||||
Lymphoma | Overall = 0.3 per 100 000 | W m/f = 1.9 | EBV, AIDS (B cell) | 8–25% |
Wm = 22.9% | B m/f = 2.3 | Coeliac disease (T cell) | ||
Bm = 11.4% | Chemotherapy | |||
Wf = 17.9% | ||||
Bf = 7.3% | ||||
GIST | Overall = 0.2 per 100 000 | W m/f = 1.4 | No | 45–55% |
Wm = 10.3% | B m/f = 1.4 | |||
Bm = 7.4% | ||||
Wf = 10.2% | ||||
Bf = 7.5% | ||||
Metastases | Autopsy series: | Lung cancer | End stage of disease, resection of solitary lesions may prolong survival | |
Lung cancer (12%) | Melanoma | |||
Breast cancer (16%) | Breast cancer | |||
Melanoma (42%) |
W, white; B, black; m, male; f, female; EBV, Epstein-Barr virus; AIDS, acquired immune deficiency syndrome; GIST, gastrointestinal stromal tumour.
Table 2. Summary of typical and atypical imaging findings of small intestine neoplasms.
Histology | Typical appearance | Atypical appearance |
Adenocarcinoma | Concentric lumen narrowing with irregular edges | Polypoid lesions with well-defined surface and margins |
Complete bowel obstruction | Central ulcerations | |
Heterogenous enhancement | Duodenal localisation | |
Carcinoid | Small (<2 cm) single or multiple filling defects | Ill-defined thickening of bowel wall without discrete mass |
Desmoplastic reaction of the mesentery | Absence of desmoplastic reaction | |
Hypervascular | Duodenal or jejunal localisation | |
Lymphoma | Coarse segmental wall thickening with ulceration and necrosis | Discrete polyp that may be a lead point of intussusception |
Bulky lymphyadenopathies | Absence of significant lymphoadenopathies | |
Aneurysmal dilatation of bowel loops | No signs of bowel occlusion | |
GIST | Large regular mass with inhomogeneous enhancement | Irregular mass with low attenuation and poor enhancement |
Necrosis and/or ulceration | Larger calcifications | |
Ileal localisation | Direct vascular encasement | |
Metastases | Intraluminal nodules develeloping from haematogenous spread to submucosal layers | Large serosal masses developed from intraperitoneal seeding from gastrointestinal cancers |
GIST, gastrointestinal stromal tumour.
At imaging duodenal carcinomas often appear as polypoid, well-delineated lesions [35,36] (Figures 4 and 5), although high-grade cancers may show more aggressive behaviour. Central ulceration may be present in 10% of cases. Adenocarcinomas of the jejunum and ileum usually appear as an annular narrowing with abrupt concentric or irregular “overhanging edge” stenosis (Figure 6) that could lead to partial or complete obstruction [17,22]. After intravenous contrast agent administration, moderate heterogeneous enhancement is usually seen [14]. Extraluminal infiltration may appear as fat stranding on MDCT and hyperintensity of the outer wall layers and fat on T2 weighted fat suppressed MR sequences. Adenocarcinoma of the ileum may mimic Crohn's disease for its clinical and radiological features; however, in our experience the absence of significant engorgement of the vasa recta (the “comb” sign in Crohn's disease) and the presence of a single focal lesion rather than multiple “skip” areas of wall thickening may be useful criteria to suspect malignancy (Figure 7). Secondary lymphadenopathies may be present at the time of diagnosis and must be differentiated from the bulkier nodes that occur when there is lymphomatous involvement of the mesentery.
Carcinoid tumours
Carcinoid is the second most common malignancy, accounting for approximately 20–25% of all SI lesions, although its frequency has been recently reported to be increased up to 35%. These tumours arise from enterochromaffin cells situated in the crypts of Lieberkühn and produce serotonin and other histamine-like substances [37]. Carcinoid tumours are more common in the ileum (most within 60 cm of the ileocecal valve) than in the jejunum or duodenum, and lesions may be multiple and/or metastatic (liver and lungs) at the time of diagnosis. Prognosis is usually negatively related to the age of the patient and the size of tumour. Macroscopically carcinoid presents as an intramural or mucosal mass that may infiltrate the mesentery causing a strong desmoplastic reaction that results in calcification, fat stranding and eventually kinking of the bowel segments (Figure 8), often with intestinal obstruction [38]. Histologically, the tumours resemble adenocarcinomas, but with a less aggressive evolution. SI lesions show a strong argentaffin reaction and immunohistochemical staining (chromogranin, neuron specific enolase, sinaptophysin) is mandatory in order to confirm the histological classification (Figure 8).
At diagnostic imaging carcinoid usually appears as a parietal nodule with avid contrast enhancement in the arterial phase [14,17,22] (Figure 9). Since most lesions are small (<2 cm) at the time of the examination, optimal distension of the bowel lumen must be achieved in order to properly identify the nodules. On unenhanced MR scans, carcinoid tumours usually appear as isointense to muscle on T1 weighted images and iso- or mildly hyperintense to muscle on T2 weighted images [39]. In some cases no discrete mass can be identified and in such cases the tumour usually develops as a focal thickening of the wall of a bowel loop. The most characteristic feature of carcinoid tumours is an intense desmoplastic reaction in the mesentery induced by extraparietal infiltration [14,40]. Both MDCT and MRI can show an ill-defined soft-tissue mass with irregular margins and infiltrative character related to mesenteric fibrosis (Figure 10). In up to 70% of cases these mesenteric masses contain calcifications that are correctly identified only at MDCT [14]. Moreover, mesenteric calcifications can be used to differentiate carcinoid-induced fibrosis from other conditions such as mesenteric fibromatosis in which calcium precipitation is uncommon [41]. Mesenteric vessel can be involved as a result of direct tumour encasement or desmoplastic reaction. Narrowing or engorgement of the vasa recta as well as secretory discharge (Figure 11) can occur owing to the action of hormones secreted by the neoplasm. Special attention should be paid to the identification of synchronous localisations in the SI and to the possible presence of hypervascular liver metastases. Alternative diagnostic modalities such as somatostastin receptor scan or positron emission tomography (PET) with C11-hydroxytrytophan can be a feasible option for suspected carcinoid in the absence of confirmatory conventional cross-sectional imaging data.
Lymphoma
The third most common neoplasm is non-Hodgkin lymphoma (10–15% of cases). This neoplasm is more common in patients with coeliac disease and in patients with acquired immune deficiency syndrome (AIDS), and particularly prevalent in developing countries. Early lesions may appear as plaque-like mucosal expansions while advanced, infiltrating lesions produce full mural thickening and mucosal ulceration. Other lesions may appear as polipoid masses protruding into the lumen. The involvement of the outer layer of the intestinal wall often leads to wide infiltration of the muscularis propria and myenteric plexus, causing motility failure and secondary obstruction [42] (Figure 12). Moreover, the lack of stromal support in larger lesions may determine ischaemia, necrosis and wall perforation. Atypical lymphoid cells populate the superficial epithelium, subsequently replacing the submucosa and even muscle wall in advanced cases (Figure 12). Most SI lymphomas are B cell-type lesions, while a small percentage are T-cell lymphomas, evenly distributed between low- and high-grade lesions [43].
Owing to the proteiform aspects of this neoplasm, small bowel lymphoma has a wide variety of radiological appearances. At least four major patterns of lymphomatous involvement of the SI have been described [14,44]. The most common type of alteration (50% of cases) is represented by a full-thickness infiltrative lesion with destruction of the normal mucosal folds (Figure 13), which can involve the muscular layer, blocking peristalsis and causing aneurysmal dilatation of the bowel loops. Adenocarcinoma should usually be considered for differential diagnosis, although this lesion typically presents without aneurysmal dilatation of the bowel [14]. Lymphoma can also present as multifocal nodules at multiple sites along the SI (requiring differentiation from carcinoid tumour) or as a single mass-forming lesion that may cause intussusceptions or obstruction (Figure 14). Alternatively, an exophytic sarcoma-like form has been described. After contrast agent administration lymphoma demonstrates homogeneous, mild enhancement. Necrosis or fistulous tracts to the adjacent bowel loops have been described, mainly in the exophytic form [45], with increased risk of perforation during chemotherapy. Satellite lymphadenopaties are usually bulky (Figure 14), larger than in other neoplasms and may be used as a differential sign [14].
Gastrointestinal stromal tumours
GI stromal cell tumour (GIST) is the fourth most common SI malignancy, accounting for less than 10% of cases. GISTs develop from the interstitial cells of Cajal, within the Auerbach plexus [46]. Grossly, GISTs appear as rounded, well-defined masses arising from the muscular layer and often developing exophytically or intraluminally, they may be mucosal ulceration present. The size of the lesion may vary from a few millimetres to more than 30 cm. Larger lesions often present central necrosis and haemorrhage (Figure 15). Histologically, GISTs can be classified into spindle cell and epithelioid varieties. The cellular expression of c-kit (CD117), a transmembrane protein receptor with an intracellular tyrosine kinase domain, is typical of GISTs (85–95% of cases) and can be demonstrated with immunohistochemical staining [47] (Figure 15). Epithelioid c-kit negative GISTs usually show early lymphonodal involvement and have a poorer prognosis. The number of mitotic figures per high power-field (HPF) is usually adopted as an empirical cut-off to predict the behaviour of the lesion: 1–5 mitoses per 10 HPFs suggest potential malignancy, while more than 5 per 10 HPFs indicate malignancy [48]. GISTs occur almost anywhere in the SI, although malignant lesions arise mainly in the distal ileum. GISTs may be classified as:
submucosal: smooth, round-to-oval filling defect in the SI lumen;
subserosal: extrinsic or exocentric masses that displace adjacent bowel loops;
intraluminal: hypervascular lesions often correlated with haemorrhage and ulceration.
Other radiological findings that may suggest a malignant form include an irregular shape with low attenuation and internal necrosis on MDCT [49,50] (Figure 16) and hyperintensity on T2 weighted MRI indicating central necrosis [16,51]. Direct spread to adjacent bowel loops, vascular encasement and metastases are common for malignant lesions (Figure 17). Small bowel neurofibromas are similar to benign GISTs and may be equally hypervascular. In patients with acquired immunodeficiency, multiple GISTs must be distinguished from intestinal Kaposi sarcoma [52]. Both MDCT and MRI are important in assessing the response to treatment.
Metastases
Although metastases are the least common SI malignancies, the small bowel remains the main site of metastatic disease in the GI tract. While GISTs, adenocarcinoma and carcinoid tumours often metastasise to the SI, the most frequent extra-abdominal causes of SI metastases are melanoma [53], lung [54], breast and thyroid cancers [55]. Usually macroscopic features such as multifocality, no ulceration and a predominant extramural component may suggest metastatic disease (Figure 18). Histologically, metastases are typically submucosal or subserosal and are easy to distinguish from primary tumours; nevertheless, immunohistochemistry may also help to differentiate primary cancer from metastases (Figure 18). Metastatic spread to the small bowel usually appears as a smooth, round or polypoid mass with the “target” aspect of an ulcerated lesion that may result in intussusception or occlusion [22,56] (Figure 19). Metastases in the small bowel can also occur as extramural nodules following intraperitoneal seeding especially from primary mucinous tumours (ovaries, appendix and colon). An increase in bowel wall thickness with infiltration of the mesenteric fat (omental cake) is the classic radiological feature of intraperitoneal seeding on MDCT and MRI [57]. Since the radiological diagnosis of metastasis is not diagnostic for the primary tumour, a whole body CT scan may be beneficial to reveal the primary site.
Conclusion
Since primary and secondary small bowel neoplasms are rare, present with non-specific symptoms and are small at an early stage, they continue to pose a diagnostic challenge to radiologists. The use of state of the art MDCT and MRI with appropriate application of tailored scan protocols and an understanding of the imaging signs of each pathological entity, as compared with the natural history of the tumour and microscopic histology, may be of significant help in the daily routine of GI radiologists.
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