REVIEW URRENT C OPINION
Imaging the small bowel Kevin P. Murphy a,b, Patrick D. McLaughlin a,b, Owen J. O’Connor a,b, and Michael M. Maher a,b
Purpose of review Radiologic investigations continue to play a pivotal role in the diagnosis of pathologic conditions of the small intestine despite enhancement of capsule endoscopy and double-balloon endoscopy. Imaging techniques continue to evolve and new techniques in MRI in particular, are being developed. Recent findings Continued advances in computed tomography (CT) and MRI techniques have reinforced the importance of these imaging modalities in small bowel assessment. The more invasive enteroclysis technique yields better small bowel distension for both CT and MRI when compared with peroral enterography, but no clinically significant difference is seen in terms of diagnostic accuracy. Recent concern regarding radiation exposure means that MRI is gaining in popularity. Fluoroscopic studies such as barium follow through and small bowel enteroclysis are being replaced by the cross-sectional alternatives. Contrast-enhanced ultrasound is showing results comparable with CT and MRI, but concern remains regarding reproducibility, especially outside centres that specialize in advanced sonographic techniques. Summary CT and MRI enterography are comparable first-line modalities for patients with suspected small bowel disease, but magnetic resonance enterography is favoured given the absence of ionizing radiation. Capsule endoscopy is a reasonable alternative investigation in exploration of chronic gastrointestinal blood loss, but is best kept as a second-line test in patients with other symptoms. Keywords Crohn disease, CT enterography, MR enterography, small bowel, small intestine
INTRODUCTION Radiological assessment of the small bowel remains essential in assessing patients with suspected small bowel disorder because of the length and tortuosity of the small bowel and the obvious difficulties with conventional endoscopy. Imaging methods have dramatically changed in the last 2 decades. Traditionally, the gold standard imaging study was the small bowel follow through (SBFT), which requires barium ingestion. This is now being superseded by newer predominantly cross-sectional techniques. Computed tomography (CT) and magnetic resonance imaging (MRI) processes form the backbone of modern small bowel imaging options. The mainstay of progression over the last number of years in terms of CT has been the improvement in bowel distension agents as well as radiation dosereduction techniques. Novel assessment techniques are among the most exciting developments in MRI terms. Capsule endoscopy remains a commonly used small bowel imaging modality with recent encouraging studies. Contrast-enhanced ultrasound www.co-gastroenterology.com
(CEUS) has also recently shown excellent efficacy when compared with CT and MRI.
RADIOLOGICAL FINDINGS IN SMALL BOWEL DISEASE Regardless of the modality utilized, the distribution and appearance of the radiological findings is key to small bowel assessment. Positive imaging findings that are frequently encountered include bowel wall thickening, abnormal enhancement, perienteric fat stranding, ascites, perienteric abscess or inflammatory mass, fistula, adenopathy or mass. The presence of these findings, along with the length of segment involved, the presence of multifocal lesions, the a Department of Radiology, Cork University Hospital and bDepartment of Radiology, University College Cork, Wilton, Cork, Ireland
Correspondence to Professor Michael M. Maher, Cork University Hospital & University College Cork, Cork, Ireland. Tel: +353 21 4920274; fax: +353 21 4920319; e-mail: [email protected] Curr Opin Gastroenterol 2014, 30:134–140 DOI:10.1097/MOG.0000000000000038 Volume 30 Number 2 March 2014
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KEY POINTS Peroral CTE or MRE are the first-line modalities of choice for small bowel assessment. MRE has comparable efficacy to CT but does not utilize ionizing radiation, hence is favoured where available. Significant advances are being made in terms of CT radiation dose reduction however. Capsule endoscopy is most frequently utilized in detecting occult gastrointestinal blood loss but is showing good results in detecting other small intestinal pathologies, making it a reasonable alternative firstline investigation. DWI is the most promising of the newer MRI techniques being employed and developed because of its sensitivity, speed of acquisition and availability. CEUS remains a second-line investigation, but demonstrates an efficacy approaching that of CT and MRI.
obstruction. The availability, acquisition speed and the cost of CT are favourable factors in the acute scenario. Positive or negative oral contrast is used where possible. Positive contrast in particular is helpful in patients of low body mass index. Whether in the acute or nonacute setting, however, negative oral contrast is favoured over positive contrast for dedicated enteric assessment [7]. MRI and ultrasound are adjuncts that show comparable findings in assessing patients with obstruction however [8]. The use of MRI, however, in the critically ill patient is much more difficult than CT because of requirements for magnetic resonance-compatible monitoring and anaesthesia equipment, and reduced accessibility to the patient in the long narrow bore of the MRI tunnel, which can lead to difficulties with airway management, intravenous access and patient visualization as well as increased procedure duration compared with CT.
IMAGING IN THE NONACUTE SITUATION degree and symmetry of thickening, location of abnormality within the bowel wall, presence of abnormal mural enhancement, fold thickening and peri-enteric findings can aid in the characterization of abnormal findings [1 ,2 ,3]. Length of segment involved is among the most useful of signs. Focal ulceration, neoplasm, foreign-body perforations, reactionary thickening, small-intestinal diverticulitis and endometriosis can cause focal (less than 6 cm) small intestinal abnormalities. Conditions that typically result in segmental (6–40 cm) involvement of the small intestine include inflammatory bowel disease, trauma, infection, radiation enteritis, intramural haemorrhage, and segmental ischemia. When diffuse long-segment abnormalities of the small intestine are found, pathologic processes such as angioedema, graft-versus-host disease, hypoalbuminaemia and generalized intestinal ischemia should be considered [1 ,3]. Metastatic infiltration of the small bowel represents the most commonly encountered small bowel neoplasm. In analysis of primary small bowel tumours, the location of the tumour is very helpful in predicting the likely histology; adenocarcinoma is the commonest duodenal neoplasm, and carcinoid is the most frequent ileal tumour, whereas lymphoma has a relatively even distribution [2 ,4–6]. Of note, the incidence of small bowel carcinoid tumours is increasing [4,6]. &
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ASSESSMENT IN THE ACUTE SETTING CT remains the mainstay in assessing patients with suspected small bowel trauma and small bowel
In patients with chronic or subacute symptoms such as pain, distension, vomiting, weight loss, anaemia or malabsorption, which may suggest a small bowel disorder, CT and MRI are among the most commonly used imaging modalities. Despite the availability of CT and MRI methods that are widely accepted as being superior to SBFT, many recent studies suggest that SBFT continues to be used frequently. A European paediatric study showed a drop of almost 50% in the annual use of SBFT over a 5-year period [9]. In a US study, however, the use of SBFT only fell by 7% over 5 years (2001–2006) [10] and a UK study concludes that SBFT remains the most commonly utilized modality in assessing patients with Crohn’s disease [11].
COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROGRAPHY Owing to the nonspecific presentation of small bowel disease, first-line studies in these patients are frequently not optimized for small bowel evaluation. If the study is being optimized for small intestinal analysis, then peroral magnetic resonance enterography (MRE), magnetic resonance enteroclysis, peroral CT enterography (CTE) or CT enteroclysis should be considered. Peroral MRE and CTE involve oral ingestion of up to 2 l of an agent to fill and distend the bowel. In the case of CTE, a negative or low-density oral contrast agent is used with ‘enteric phase’ intravenous contrast administration to optimize contrast resolution between mucosa and lumen, thereby maximizing conspicuity of abnormalities arising from the small bowel wall
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[12 ]. These negative oral contrast agents may contain water, polyethylene glycol, mannitol or other bulking agents, but vary according to the local protocol. Polyethylene glycol is the agent that is now favoured and most frequently used [12 ,13,14 ]. The commonest side-effect is diarrhoea. MR-ingested distension agents can be classified as biphasic (e.g. water, polyethylene glycol, methylcellulose), negative (e.g. ferumoxsil suspension, superparamagnetic particles) or positive (e.g. gadolinium, manganese) according to the signal intensity produced on T1 and T2 images [15]. Many of the agents cause diarrhoea, result in nausea, are costly or are difficult to source. More variability exists in terms of most frequently employed oral agent when compared with CTE, but polyethylene glycol is marginally favoured [16 ,17]. &
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COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROCLYSIS As alternatives to peroral CTE and MRE, CT and magnetic resonance enteroclysis involve inserting a fluoroscopically guided nasojejunal tube and instilling similar agents at a high flow rate to distend the small bowel. The high frequency of patient discomfort [14 ,18,19], along with the extra time involved and the radiation exposure associated with fluoroscopy, are disadvantages of enteroclysis. Many studies have shown that distension is routinely superior with enteroclysis when compared with enterography. There is, however, no significant difference in terms of detection of clinically significant findings, sensitivity or specificity [20–22]. Enterography is favoured over enteroclysis in terms of many current recommendations [23] and is also recommended in current European Crohn’s disease consensus guidelines [24]. &&
COMPARING COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING When one directly compares CTE and MRE, MRI has excellent contrast resolution, does not result in ionizing radiation exposure, can acquire multiplanar image datasets, is able to acquire sequential image series over a long acquisition time and can acquire multiple phases of imaging. CT, on the contrary, has superior spatial resolution, takes less time to acquire, is less prone to motion artifact associated with peristalsis and has greater availability. Figures 1a and b demonstrate a neuroendocrine small bowel tumour of the distal ileum highlighting the key CT and magnetic resonance differences. European consensus [24] and other guidelines recommend either CTE or MRE as first-line small bowel investigations. 136
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FIGURE 1. (a) Axial T1 fat saturation post gadolinium magnetic resonance enterography (MRE) image of a distal ileal circumferential neuroendocrine tumour (arrows) in a 38-year-old male patient. The image demonstrates excellent contrast resolution. (b) Axial contrast-enhanced computed tomography abdomen and pelvis image from the same patient as Figure 1a, again showing the circumferential tumour (arrows). The spatial resolution is superior, but the contrast resolution is inferior when compared with the MRE.
Multiple studies, predominantly in patients with Crohn’s disease, have also shown CTE and MRE to be comparable in terms of sensitivity and specificity [25–28,29 ,30–32]. Both have sensitivities in excess of 90% and specificities in excess of 80%. Key findings of diffuse small bowel disorders such as Crohn’s disease are wall thickening, abnormal enhancement, adenopathy and enlarged mesenteric vasculature. Complications such as inflammatory mass, fistula and abscess may also be seen. &
CAPSULE ENDOSCOPY The use of wireless capsule endoscopy (WCE) or video capsule endoscopy is a frequently used alternative to cross-sectional enterography. It involves ingestion of a small disposable capsule of up to 2-cm length that acquires images at a rate of Volume 30 Number 2 March 2014
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approximately 2 per second over 7–8 h and transmits the data to a small external receiver that the patient wears. The only commonly quoted contraindication is the presence of a bowel stricture. Many studies have shown that WCE is superior in terms of detection of small mucosal lesions with a marginally superior sensitivity but a slightly inferior specificity [33,34 ,35,36 ,37,38]. A significant shortcoming of the technology is that it gives no extraluminal information. Time for interpretation and cost also represent limitations of the technique that currently prevent uptake of this method in everyday practice. The European consensus group [24] recommends that capsule endoscopy should be utilized when imaging and endoscopy are negative. Chronic occult gastrointestinal blood loss remains the most common indication for capsule endoscopy in practice [39]. &&
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NEW TECHNIQUES IN MAGNETIC RESONANCE IMAGING Many studies have shown that gut motility at MRI is decreased in active or chronic Crohn’s disease and possibly in other diffuse small bowel diseases [40 ,41,42 ,43,44]. MRI is particularly useful in this assessment because of rapid acquisition time, the ability to image in any plane and the facility to perform multiple sequences (including cine sequences) because of the absence of exposure to ionizing radiation. An assessment of the level of motility disturbance or obstruction secondary to a stricture can then be quantitatively and qualitatively assessed. Recent investigations have shown significant correlations between motility and histology [42 ], and between motility, C-reactive protein and faecal calprotectin [44]. Manual and automated software packages and acquisition techniques for assessment of motility continue to be developed, but currently are not in mainstream use, however. Inclusion of diffusion-weighted imaging (DWI) continues to show encouraging results. Studies suggest that DWI is comparable with contrastenhanced imaging in Crohn’s assessment [45 , 46 ,47] and apparently superior to dynamic contrast enhancement [48]. In comparison with MRI motility assessment and other newer MRI assessment mechanisms, DWI is more commonly performed in practice. The sequence is quick to perform and the sequence software is freely available in commercial units, as DWI is now a standard imaging sequence in other body systems including neuroimaging, making it the most promising of the ‘new’ MRI techniques. Dynamic contrast enhancement curve analysis remains an experimental adjunct in small bowel &
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MRI. The technique involves sequential imaging of the bowel before and after gadolinium injection with subsequent creation of enhancement curves with estimation of peak enhancement and other parameters. The main reported benefit currently is in assessing active inflammation from fibrosis in patients with Crohn’s disease [48–54]. Spectroscopy remains an experimental entity in the setting of small bowel imaging.
ALTERNATIVE MODALITIES TO COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING Ultrasound, and in particular, CEUS, has been gaining popularity in the last decade. The absence of ionizing radiation, the portable nature and low cost make it an excellent modality especially in the paediatric population. A long-standing problem with the use of ultrasound in clinical practice has been the limitation of user variation. A recent study however suggests that CEUS is a useful modality, even in nonexpert hands [55 ] with high specificity and sensitivity achieved in the evaluation of Crohn’s disease patients. Impressive results with CEUS in the evaluation of Crohn’s disease have been reported in recent studies. CEUS is the application of contrast material to medical ultrasonography. The contrast is provided by intravenous injection of microbubbles. The main benefit of CEUS is characterizing bowelwall thickening by differentiating inflammatory neovascularization, edema, and fibrosis [56–58,59 ,60]. A small study recently showed a high correlation between CEUS and MRI of the small bowel when assessing wall thickness, lymph nodes and comb sign [60]. Ultrasound elastography is another ultrasound application, which remains experimental in the setting of inflammatory bowel disease, at present. Commonly used nuclear medicine options in small bowel assessment include Meckels diverticulum scintigraphy, white blood cell inflammatory imaging, labelled red cell studies for assessment of bowel haemorrhage, neuroendocrine tumour detection or staging (e.g. octreotide or metaiodobenzylguanidine studies), as well as fluorodeoxyglucose positron emission tomography CT (FDG PET CT). Though the idea of molecular imaging remains a key topic of research, the majority of the studies are complementary assessments. They have a valuable role in patient assessment when other modalities have been negative [61 ]. PET CT shows comparable results when compared with MRI and endoscopy in assessment of patients with Crohn’s disease [62 ], but obvious issues include high radiation exposure and access. The main benefit of PET CT in small bowel assessment is in the setting of small bowel
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FIGURE 2. (a and b) Coronal reformatted images from a computed tomography (CT) enterography in a 24-year-old female patient with terminal ileitis (arrows), mesenteric fat stranding and small volume mesenteric adenopathy (arrowhead) secondary to Crohn’s disease. Figure 2a is from a conventional-dose CT with standard reconstruction. Image 2b is from a contemporaneously acquired low-dose study performed at 21% of the conventional radiation dose study and reconstructed with pure model based iterative reconstruction.
neoplasms [63]. PET MRI at present remains an experimental modality, although units are now being made commercially available [64].
RADIATION SAFETY ISSUES AND METHODS OF DOSE REDUCTION Patients with chronic small bowel conditions such as Crohn’s disease are at an elevated risk for high lifetime cumulative radiation exposures, predominantly from CT, with a potential increased risk of neoplasm [65–68]. The issue of radiation exposure associated with CT is receiving increasing attention in the mainstream media and this has contributed to increased awareness among the public, patients, physicians and radiologists, and also contributed to the introduction of strategies such as the ‘Image Gently’ campaign [69 ,70]. Obvious dose reduction strategies include choosing a modality that does not use ionizing radiation, and ensuring that studies that utilize radiation are unequivocally indicated and are likely to alter patient management. Multiple strategies can be utilized to decrease the dose from a CT during study acquisition. These include omitting ‘extra’ images at the ends of the acquired volumes, omitting extra imaging phases that do not contribute diagnostically and employing automated exposure control as opposed to fixed tube current techniques [71–74]. New image reconstruction techniques have
also been developed in an effort to reduce radiation exposure. Traditionally, CT images were reconstructed with filtered back projection, whereas new techniques utilize iterative reconstruction algorithms, which are the subject of significant research and development by industry [75–81,82 ]. These iterative reconstruction algorithms are typically noise-efficient and are becoming computationally fast, and studies to date have, for the most part, produced images with good low-contrast detail at much reduced radiation doses (Fig. 2 a and b). Image quality is preserved in the context of radiation dose reductions of 50% or greater. More recent studies suggest that diagnostically acceptable CT abdomen and pelvis studies can be attained for a radiation dose close to that of an abdominal radiograph (approximately 1 millisievert) [82 ,83 ,84 ]. &
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CONCLUSION In recent years, MRE is becoming the first-line investigation in assessment of the majority of small bowel disorders. The more invasive method of MR enteroclysis results in better distension but does not have a measureable improvement in diagnostic efficacy. CTE has a comparable sensitivity and specificity to its MR alternative but results in exposure to ionizing radiation. Capsule endoscopy and CEUS are now showing improved effectiveness in small bowel assessment. Volume 30 Number 2 March 2014
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Acknowledgements None. Conflicts of interest The authors have no conflicts of interest in terms of grants, financial support or other matters.
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66. Kroeker KI, Lam S, Birchall I, Fedorak RN. Patients with IBD are exposed to high levels of ionizing radiation through CT scan diagnostic imaging: a five-year study. J Clin Gastroenterol 2011; 45:34–39. 67. Newnham E, Hawkes E, Surender A, et al. Quantifying exposure to diagnostic medical radiation in patients with inflammatory bowel disease: are we contributing to malignancy? Aliment Pharmacol Ther 2007; 26:1019–1024. 68. Butcher RO, Nixon E, Sapundzieski M, et al. Radiation exposure in patients with inflammatory bowel disease–primum non nocere? Scand J Gastroenterol 2012; 47:1192–1199. 69. Don S, Macdougall R, Strauss K, et al. Image gently campaign back to basics && initiative: ten steps to help manage radiation dose in pediatric digital radiography. AJR Am J Roentgenol 2013; 200:W431–W436. The study outlines the key points in the radiation safety awareness campaign. 70. Applegate KE, Cost NG. Image Gently: a campaign to reduce children’s and adolescents’ risk for cancer during adulthood. J Adolesc Health 2013; 52 (5 Suppl):S93–S97. 71. Swanson G, Behara R, Braun R, Keshavarzian A. Diagnostic medical radiation in inflammatory bowel disease: how to limit risk and maximize benefit. Inflamm Bowel Dis 2013; 19:2501–2508. 72. Mc Laughlin PD, O’Connor OJ, O’Neill SB, et al. Minimization of radiation exposure due to computed tomography in inflammatory bowel disease. ISRN Gastroenterol 2012; 2012:790279. 73. Kalra MK, Maher MM, Toth TL, et al. Radiation from ‘extra’ images acquired with abdominal and/or pelvic CT: effect of automatic tube current modulation. Radiology 2004; 232:409–414. 74. Allen BC, Baker ME, Einstein DM, et al. Effect of altering automatic exposure control settings and quality reference mAs on radiation dose, image quality, and diagnostic efficacy in MDCT enterography of active inflammatory Crohn’s disease. AJR Am J Roentgenol 2010; 195:89–100. 75. Kambadakone AR, Prakash P, Hahn PF, Sahani DV. Low-dose CT examinations in Crohn’s disease: impact on image quality, diagnostic performance, and radiation dose. AJR Am J Roentgenol 2010; 195:78–88. 76. Singh S, Kalra MK, Hsieh J, et al. Abdominal CT: comparison of adaptive statistical iterative and filtered back projection reconstruction techniques. Radiology 2010; 257:373–383. 77. Silva AC, Lawder HJ, Hara A, et al. Innovations in CT dose reduction strategy: application of the adaptive statistical iterative reconstruction algorithm. AJR Am J Roentgenol 2010; 194:191–199. 78. May MS, Wu¨st W, Brand M, et al. Dose reduction in abdominal computed tomography: intraindividual comparison of image quality of full-dose standard and half-dose iterative reconstructions with dual-source computed tomography. Invest Radiol 2011; 46:465–470. 79. Winklehner A, Karlo C, Puippe G, et al. Raw data-based iterative reconstruction in body CTA: evaluation of radiation dose saving potential. Eur Radiol 2011; 21:2521–2526. 80. Craig O, O’Neill S, O’Neill F, et al. Diagnostic accuracy of computed tomography using lower doses of radiation for patients with Crohn’s disease. Clin Gastroenterol Hepatol 2012; 10:886–892. 81. Singh S, Kalra MK, Do S, et al. Comparison of hybrid and pure iterative reconstruction techniques with conventional filtered back projection: dose reduction potential in the abdomen. J Comput Assis Tomogr 2012; 36:347– 353. 82. O’Neill SB, Mc Laughlin PD, Crush L, et al. A prospective feasibility study of & sub-millisievert abdominopelvic CT using iterative reconstruction in Crohn’s disease. Eur Radiol 2013; 23:2503–2512. The impact of iterative reconstruction on low-dose CT images is examined. 83. Volders D, Bols A, Haspeslagh M, Coenegrachts K. Model-based iterative & reconstruction and adaptive statistical iterative reconstruction techniques in abdominal CT: comparison of image quality in the detection of colorectal liver metastases. Radiology 2013; 269:469–474. [Epub ahead of print]. This study further highlights the benefit of iterative reconstruction on low-dose CT image quality. 84. Yasaka K, Katsura M, Akahane M, et al. Model-based iterative reconstruction && for reduction of radiation dose in abdominopelvic CT: comparison to adaptive statistical iterative reconstruction. Springer Plus 2013; 2:209. The excellent, promising results from the latest iterative reconstruction method are outlined.
Volume 30 Number 2 March 2014
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Imaging the small bowel Kevin P. Murphy a,b, Patrick D. McLaughlin a,b, Owen J. O’Connor a,b, and Michael M. Maher a,b
Purpose of review Radiologic investigations continue to play a pivotal role in the diagnosis of pathologic conditions of the small intestine despite enhancement of capsule endoscopy and double-balloon endoscopy. Imaging techniques continue to evolve and new techniques in MRI in particular, are being developed. Recent findings Continued advances in computed tomography (CT) and MRI techniques have reinforced the importance of these imaging modalities in small bowel assessment. The more invasive enteroclysis technique yields better small bowel distension for both CT and MRI when compared with peroral enterography, but no clinically significant difference is seen in terms of diagnostic accuracy. Recent concern regarding radiation exposure means that MRI is gaining in popularity. Fluoroscopic studies such as barium follow through and small bowel enteroclysis are being replaced by the cross-sectional alternatives. Contrast-enhanced ultrasound is showing results comparable with CT and MRI, but concern remains regarding reproducibility, especially outside centres that specialize in advanced sonographic techniques. Summary CT and MRI enterography are comparable first-line modalities for patients with suspected small bowel disease, but magnetic resonance enterography is favoured given the absence of ionizing radiation. Capsule endoscopy is a reasonable alternative investigation in exploration of chronic gastrointestinal blood loss, but is best kept as a second-line test in patients with other symptoms. Keywords Crohn disease, CT enterography, MR enterography, small bowel, small intestine
INTRODUCTION Radiological assessment of the small bowel remains essential in assessing patients with suspected small bowel disorder because of the length and tortuosity of the small bowel and the obvious difficulties with conventional endoscopy. Imaging methods have dramatically changed in the last 2 decades. Traditionally, the gold standard imaging study was the small bowel follow through (SBFT), which requires barium ingestion. This is now being superseded by newer predominantly cross-sectional techniques. Computed tomography (CT) and magnetic resonance imaging (MRI) processes form the backbone of modern small bowel imaging options. The mainstay of progression over the last number of years in terms of CT has been the improvement in bowel distension agents as well as radiation dosereduction techniques. Novel assessment techniques are among the most exciting developments in MRI terms. Capsule endoscopy remains a commonly used small bowel imaging modality with recent encouraging studies. Contrast-enhanced ultrasound www.co-gastroenterology.com
(CEUS) has also recently shown excellent efficacy when compared with CT and MRI.
RADIOLOGICAL FINDINGS IN SMALL BOWEL DISEASE Regardless of the modality utilized, the distribution and appearance of the radiological findings is key to small bowel assessment. Positive imaging findings that are frequently encountered include bowel wall thickening, abnormal enhancement, perienteric fat stranding, ascites, perienteric abscess or inflammatory mass, fistula, adenopathy or mass. The presence of these findings, along with the length of segment involved, the presence of multifocal lesions, the a Department of Radiology, Cork University Hospital and bDepartment of Radiology, University College Cork, Wilton, Cork, Ireland
Correspondence to Professor Michael M. Maher, Cork University Hospital & University College Cork, Cork, Ireland. Tel: +353 21 4920274; fax: +353 21 4920319; e-mail: [email protected] Curr Opin Gastroenterol 2014, 30:134–140 DOI:10.1097/MOG.0000000000000038 Volume 30 Number 2 March 2014
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Imaging the small bowel Murphy et al.
KEY POINTS Peroral CTE or MRE are the first-line modalities of choice for small bowel assessment. MRE has comparable efficacy to CT but does not utilize ionizing radiation, hence is favoured where available. Significant advances are being made in terms of CT radiation dose reduction however. Capsule endoscopy is most frequently utilized in detecting occult gastrointestinal blood loss but is showing good results in detecting other small intestinal pathologies, making it a reasonable alternative firstline investigation. DWI is the most promising of the newer MRI techniques being employed and developed because of its sensitivity, speed of acquisition and availability. CEUS remains a second-line investigation, but demonstrates an efficacy approaching that of CT and MRI.
obstruction. The availability, acquisition speed and the cost of CT are favourable factors in the acute scenario. Positive or negative oral contrast is used where possible. Positive contrast in particular is helpful in patients of low body mass index. Whether in the acute or nonacute setting, however, negative oral contrast is favoured over positive contrast for dedicated enteric assessment [7]. MRI and ultrasound are adjuncts that show comparable findings in assessing patients with obstruction however [8]. The use of MRI, however, in the critically ill patient is much more difficult than CT because of requirements for magnetic resonance-compatible monitoring and anaesthesia equipment, and reduced accessibility to the patient in the long narrow bore of the MRI tunnel, which can lead to difficulties with airway management, intravenous access and patient visualization as well as increased procedure duration compared with CT.
IMAGING IN THE NONACUTE SITUATION degree and symmetry of thickening, location of abnormality within the bowel wall, presence of abnormal mural enhancement, fold thickening and peri-enteric findings can aid in the characterization of abnormal findings [1 ,2 ,3]. Length of segment involved is among the most useful of signs. Focal ulceration, neoplasm, foreign-body perforations, reactionary thickening, small-intestinal diverticulitis and endometriosis can cause focal (less than 6 cm) small intestinal abnormalities. Conditions that typically result in segmental (6–40 cm) involvement of the small intestine include inflammatory bowel disease, trauma, infection, radiation enteritis, intramural haemorrhage, and segmental ischemia. When diffuse long-segment abnormalities of the small intestine are found, pathologic processes such as angioedema, graft-versus-host disease, hypoalbuminaemia and generalized intestinal ischemia should be considered [1 ,3]. Metastatic infiltration of the small bowel represents the most commonly encountered small bowel neoplasm. In analysis of primary small bowel tumours, the location of the tumour is very helpful in predicting the likely histology; adenocarcinoma is the commonest duodenal neoplasm, and carcinoid is the most frequent ileal tumour, whereas lymphoma has a relatively even distribution [2 ,4–6]. Of note, the incidence of small bowel carcinoid tumours is increasing [4,6]. &
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ASSESSMENT IN THE ACUTE SETTING CT remains the mainstay in assessing patients with suspected small bowel trauma and small bowel
In patients with chronic or subacute symptoms such as pain, distension, vomiting, weight loss, anaemia or malabsorption, which may suggest a small bowel disorder, CT and MRI are among the most commonly used imaging modalities. Despite the availability of CT and MRI methods that are widely accepted as being superior to SBFT, many recent studies suggest that SBFT continues to be used frequently. A European paediatric study showed a drop of almost 50% in the annual use of SBFT over a 5-year period [9]. In a US study, however, the use of SBFT only fell by 7% over 5 years (2001–2006) [10] and a UK study concludes that SBFT remains the most commonly utilized modality in assessing patients with Crohn’s disease [11].
COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROGRAPHY Owing to the nonspecific presentation of small bowel disease, first-line studies in these patients are frequently not optimized for small bowel evaluation. If the study is being optimized for small intestinal analysis, then peroral magnetic resonance enterography (MRE), magnetic resonance enteroclysis, peroral CT enterography (CTE) or CT enteroclysis should be considered. Peroral MRE and CTE involve oral ingestion of up to 2 l of an agent to fill and distend the bowel. In the case of CTE, a negative or low-density oral contrast agent is used with ‘enteric phase’ intravenous contrast administration to optimize contrast resolution between mucosa and lumen, thereby maximizing conspicuity of abnormalities arising from the small bowel wall
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[12 ]. These negative oral contrast agents may contain water, polyethylene glycol, mannitol or other bulking agents, but vary according to the local protocol. Polyethylene glycol is the agent that is now favoured and most frequently used [12 ,13,14 ]. The commonest side-effect is diarrhoea. MR-ingested distension agents can be classified as biphasic (e.g. water, polyethylene glycol, methylcellulose), negative (e.g. ferumoxsil suspension, superparamagnetic particles) or positive (e.g. gadolinium, manganese) according to the signal intensity produced on T1 and T2 images [15]. Many of the agents cause diarrhoea, result in nausea, are costly or are difficult to source. More variability exists in terms of most frequently employed oral agent when compared with CTE, but polyethylene glycol is marginally favoured [16 ,17]. &
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COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE ENTEROCLYSIS As alternatives to peroral CTE and MRE, CT and magnetic resonance enteroclysis involve inserting a fluoroscopically guided nasojejunal tube and instilling similar agents at a high flow rate to distend the small bowel. The high frequency of patient discomfort [14 ,18,19], along with the extra time involved and the radiation exposure associated with fluoroscopy, are disadvantages of enteroclysis. Many studies have shown that distension is routinely superior with enteroclysis when compared with enterography. There is, however, no significant difference in terms of detection of clinically significant findings, sensitivity or specificity [20–22]. Enterography is favoured over enteroclysis in terms of many current recommendations [23] and is also recommended in current European Crohn’s disease consensus guidelines [24]. &&
COMPARING COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING When one directly compares CTE and MRE, MRI has excellent contrast resolution, does not result in ionizing radiation exposure, can acquire multiplanar image datasets, is able to acquire sequential image series over a long acquisition time and can acquire multiple phases of imaging. CT, on the contrary, has superior spatial resolution, takes less time to acquire, is less prone to motion artifact associated with peristalsis and has greater availability. Figures 1a and b demonstrate a neuroendocrine small bowel tumour of the distal ileum highlighting the key CT and magnetic resonance differences. European consensus [24] and other guidelines recommend either CTE or MRE as first-line small bowel investigations. 136
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FIGURE 1. (a) Axial T1 fat saturation post gadolinium magnetic resonance enterography (MRE) image of a distal ileal circumferential neuroendocrine tumour (arrows) in a 38-year-old male patient. The image demonstrates excellent contrast resolution. (b) Axial contrast-enhanced computed tomography abdomen and pelvis image from the same patient as Figure 1a, again showing the circumferential tumour (arrows). The spatial resolution is superior, but the contrast resolution is inferior when compared with the MRE.
Multiple studies, predominantly in patients with Crohn’s disease, have also shown CTE and MRE to be comparable in terms of sensitivity and specificity [25–28,29 ,30–32]. Both have sensitivities in excess of 90% and specificities in excess of 80%. Key findings of diffuse small bowel disorders such as Crohn’s disease are wall thickening, abnormal enhancement, adenopathy and enlarged mesenteric vasculature. Complications such as inflammatory mass, fistula and abscess may also be seen. &
CAPSULE ENDOSCOPY The use of wireless capsule endoscopy (WCE) or video capsule endoscopy is a frequently used alternative to cross-sectional enterography. It involves ingestion of a small disposable capsule of up to 2-cm length that acquires images at a rate of Volume 30 Number 2 March 2014
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approximately 2 per second over 7–8 h and transmits the data to a small external receiver that the patient wears. The only commonly quoted contraindication is the presence of a bowel stricture. Many studies have shown that WCE is superior in terms of detection of small mucosal lesions with a marginally superior sensitivity but a slightly inferior specificity [33,34 ,35,36 ,37,38]. A significant shortcoming of the technology is that it gives no extraluminal information. Time for interpretation and cost also represent limitations of the technique that currently prevent uptake of this method in everyday practice. The European consensus group [24] recommends that capsule endoscopy should be utilized when imaging and endoscopy are negative. Chronic occult gastrointestinal blood loss remains the most common indication for capsule endoscopy in practice [39]. &&
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NEW TECHNIQUES IN MAGNETIC RESONANCE IMAGING Many studies have shown that gut motility at MRI is decreased in active or chronic Crohn’s disease and possibly in other diffuse small bowel diseases [40 ,41,42 ,43,44]. MRI is particularly useful in this assessment because of rapid acquisition time, the ability to image in any plane and the facility to perform multiple sequences (including cine sequences) because of the absence of exposure to ionizing radiation. An assessment of the level of motility disturbance or obstruction secondary to a stricture can then be quantitatively and qualitatively assessed. Recent investigations have shown significant correlations between motility and histology [42 ], and between motility, C-reactive protein and faecal calprotectin [44]. Manual and automated software packages and acquisition techniques for assessment of motility continue to be developed, but currently are not in mainstream use, however. Inclusion of diffusion-weighted imaging (DWI) continues to show encouraging results. Studies suggest that DWI is comparable with contrastenhanced imaging in Crohn’s assessment [45 , 46 ,47] and apparently superior to dynamic contrast enhancement [48]. In comparison with MRI motility assessment and other newer MRI assessment mechanisms, DWI is more commonly performed in practice. The sequence is quick to perform and the sequence software is freely available in commercial units, as DWI is now a standard imaging sequence in other body systems including neuroimaging, making it the most promising of the ‘new’ MRI techniques. Dynamic contrast enhancement curve analysis remains an experimental adjunct in small bowel &
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MRI. The technique involves sequential imaging of the bowel before and after gadolinium injection with subsequent creation of enhancement curves with estimation of peak enhancement and other parameters. The main reported benefit currently is in assessing active inflammation from fibrosis in patients with Crohn’s disease [48–54]. Spectroscopy remains an experimental entity in the setting of small bowel imaging.
ALTERNATIVE MODALITIES TO COMPUTED TOMOGRAPHY AND MAGNETIC RESONANCE IMAGING Ultrasound, and in particular, CEUS, has been gaining popularity in the last decade. The absence of ionizing radiation, the portable nature and low cost make it an excellent modality especially in the paediatric population. A long-standing problem with the use of ultrasound in clinical practice has been the limitation of user variation. A recent study however suggests that CEUS is a useful modality, even in nonexpert hands [55 ] with high specificity and sensitivity achieved in the evaluation of Crohn’s disease patients. Impressive results with CEUS in the evaluation of Crohn’s disease have been reported in recent studies. CEUS is the application of contrast material to medical ultrasonography. The contrast is provided by intravenous injection of microbubbles. The main benefit of CEUS is characterizing bowelwall thickening by differentiating inflammatory neovascularization, edema, and fibrosis [56–58,59 ,60]. A small study recently showed a high correlation between CEUS and MRI of the small bowel when assessing wall thickness, lymph nodes and comb sign [60]. Ultrasound elastography is another ultrasound application, which remains experimental in the setting of inflammatory bowel disease, at present. Commonly used nuclear medicine options in small bowel assessment include Meckels diverticulum scintigraphy, white blood cell inflammatory imaging, labelled red cell studies for assessment of bowel haemorrhage, neuroendocrine tumour detection or staging (e.g. octreotide or metaiodobenzylguanidine studies), as well as fluorodeoxyglucose positron emission tomography CT (FDG PET CT). Though the idea of molecular imaging remains a key topic of research, the majority of the studies are complementary assessments. They have a valuable role in patient assessment when other modalities have been negative [61 ]. PET CT shows comparable results when compared with MRI and endoscopy in assessment of patients with Crohn’s disease [62 ], but obvious issues include high radiation exposure and access. The main benefit of PET CT in small bowel assessment is in the setting of small bowel
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FIGURE 2. (a and b) Coronal reformatted images from a computed tomography (CT) enterography in a 24-year-old female patient with terminal ileitis (arrows), mesenteric fat stranding and small volume mesenteric adenopathy (arrowhead) secondary to Crohn’s disease. Figure 2a is from a conventional-dose CT with standard reconstruction. Image 2b is from a contemporaneously acquired low-dose study performed at 21% of the conventional radiation dose study and reconstructed with pure model based iterative reconstruction.
neoplasms [63]. PET MRI at present remains an experimental modality, although units are now being made commercially available [64].
RADIATION SAFETY ISSUES AND METHODS OF DOSE REDUCTION Patients with chronic small bowel conditions such as Crohn’s disease are at an elevated risk for high lifetime cumulative radiation exposures, predominantly from CT, with a potential increased risk of neoplasm [65–68]. The issue of radiation exposure associated with CT is receiving increasing attention in the mainstream media and this has contributed to increased awareness among the public, patients, physicians and radiologists, and also contributed to the introduction of strategies such as the ‘Image Gently’ campaign [69 ,70]. Obvious dose reduction strategies include choosing a modality that does not use ionizing radiation, and ensuring that studies that utilize radiation are unequivocally indicated and are likely to alter patient management. Multiple strategies can be utilized to decrease the dose from a CT during study acquisition. These include omitting ‘extra’ images at the ends of the acquired volumes, omitting extra imaging phases that do not contribute diagnostically and employing automated exposure control as opposed to fixed tube current techniques [71–74]. New image reconstruction techniques have
also been developed in an effort to reduce radiation exposure. Traditionally, CT images were reconstructed with filtered back projection, whereas new techniques utilize iterative reconstruction algorithms, which are the subject of significant research and development by industry [75–81,82 ]. These iterative reconstruction algorithms are typically noise-efficient and are becoming computationally fast, and studies to date have, for the most part, produced images with good low-contrast detail at much reduced radiation doses (Fig. 2 a and b). Image quality is preserved in the context of radiation dose reductions of 50% or greater. More recent studies suggest that diagnostically acceptable CT abdomen and pelvis studies can be attained for a radiation dose close to that of an abdominal radiograph (approximately 1 millisievert) [82 ,83 ,84 ]. &
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CONCLUSION In recent years, MRE is becoming the first-line investigation in assessment of the majority of small bowel disorders. The more invasive method of MR enteroclysis results in better distension but does not have a measureable improvement in diagnostic efficacy. CTE has a comparable sensitivity and specificity to its MR alternative but results in exposure to ionizing radiation. Capsule endoscopy and CEUS are now showing improved effectiveness in small bowel assessment. Volume 30 Number 2 March 2014
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Acknowledgements None. Conflicts of interest The authors have no conflicts of interest in terms of grants, financial support or other matters.
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Volume 30 Number 2 March 2014
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