REVIEW URRENT C OPINION
Imaging modalities in pediatric inflammatory bowel disease Ross Maltz a, Daniel J. Podberesky b, and Shehzad A. Saeed c
Purpose of review To review the various imaging modalities in the evaluation of pediatric inflammatory bowel disease (IBD) to determine disease location, clinical phenotype and the severity of disease in order to optimize treatment. Recent findings Assessment of the extent, location and severity of IBD routinely involves imaging of the gastrointestinal tract. Cross-sectional modalities such as magnetic resonance enterography (MRE) and computed tomography enterography visualize the lumen, transmural involvement, extraintestinal manifestations and may facilitate decision-making in disease management. MRE has evolved as the imaging modality of choice for many pediatric IBD indications because it does not involve exposure to ionizing radiation. Summary Advances in imaging modalities have revolutionized the assessment of children with IBD in recent years. Small-bowel follow-through is no longer considered the imaging modality of choice in this setting. Crosssectional enterography is now preferred because, among other advantages, it can potentially distinguish active inflammation from fibrosis, characterize stricturing and penetrating complications, and diagnose extraintestinal manifestations. Although MRE avoids ionizing radiation exposure, it remains costly. Crosssectional imaging and endoscopy complement each other in the development of objective measures for the assessment of disease activity and monitoring of response to treatment. Keywords computed tomography enterography, inflammatory bowel disease, magnetic resonance enterography, Porto criteria, small intestinal contrast ultrasonography
INTRODUCTION Inflammatory bowel disease (IBD) comprises Crohn’s disease and ulcerative colitis. There are a total of 4 million people worldwide with IBD, with 1.4 million residing in the United States, with approximately 25–30% presenting in childhood or adolescence [1]. The incidence of pediatric Crohn’s disease and ulcerative colitis within the United States is 43 per 100 000 and 28 per 100 000, respectively [2,3]. Studies indicate that 9–38% of pediatric Crohn’s disease cases only affect the small bowel, signifying the importance of determining disease location, clinical phenotype (inflammation, stricturing, or penetrating) and the severity of disease for treatment optimization [4,5]. The presentation of adult Crohn’s disease patients generally differs from that of pediatric Crohn’s disease patients. Pediatric patients typically present initially with inflammatory disease and progress to penetrating and stricturing disease over time [6]. Indeterminate colitis, more www.co-pediatrics.com
recently termed inflammatory bowel disease unclassified (IBDU), is an IBD that cannot be classified as Crohn’s disease or ulcerative colitis. There are higher rates of IBDU in pediatric patients compared with adult patients (13% in children vs. 6% in adults) [7]. The diagnosis of IBDU could alter the management and treatment [8]. Patients may have absence of symptoms, and undertreated or underappreciated
a Division of Gastroenterology, Hepatology and Nutrition, Nationwide Children’s Hospital, Columbus, Ohio, bDepartment of Radiology and c Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA
Correspondence to Shehzad A. Saeed, MD, Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, MLC 2010, Cincinnati, OH 45229, USA. Tel: +1 513 636 4415; fax: +1 513 636 7805; e-mail: Shehzad. [email protected] Curr Opin Pediatr 2014, 26:590–596 DOI:10.1097/MOP.0000000000000131 Volume 26 Number 5 October 2014
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Pediatric inflammatory bowel disease Maltz et al.
KEY POINTS The European Society of Pediatric Gastroenterology, Hepatology and Nutrition recommends that MRE should be the imaging modality of choice in pediatric patients with inflammatory bowel disease. The American College of Radiology rates CTE and MRE equally in the initial evaluation of a child with IBD, and MRE above CTE for surveillance. Cross-sectional modalities such as MRE and CTE are now frequently used to evaluate pediatric patients with IBD because of their ability to visualize the lumen, transmural involvement and extraintestinal manifestations. MRI is the preferred modality for evaluating the pelvis and perineum for abscesses and fistulas, but may be limited because of the cost and availability.
disease can increase the risk of developing complications [9]. Traditional radiologic techniques and endoscopy typically assess the mucosa, whereas newer radiologic technologies such as MRI and computed tomography (CT) are able to determine whether inflammation exists in the deeper layers of the bowel wall and surrounding tissue [10]. Radiologic information facilitates the diagnosis and characterization of IBD, differentiation of ulcerative colitis from Crohn’s disease and aids in the monitoring of treatment efficacy [11]. A variety of imaging modalities are used to evaluate the gastrointestinal tract, each with its own advantages, disadvantages, risks and benefits. Specific tests are chosen for various reasons to supplement clinical data. When selecting an imaging modality, important factors to consider include reliability, accuracy, cost, side-effects, tolerability, accessibility, availability of expertise and radiation exposure. Additionally, it is crucial to use imaging at the time of diagnosis, to establish a baseline of disease activity and extent prior to escalating medical therapy, and to assess extraintestinal manifestations. Traditionally, imaging of the bowel relied on fluoroscopic barium studies such as small-bowel follow-through and contrast enema. However, new technologies such as magnetic resonance enterography (MRE) and computed tomography enterography (CTE) examine the intestinal cross-sections which provides more accurate diagnosis of inflammation, fibrosis and extraintestinal manifestations [12 ]. Video capsule endoscopy (VCE) is also used to visualize the gastrointestinal tract [13 ]. Abdominal radiographs are often still utilized to diagnose toxic megacolon, bowel obstruction and perforation [14]. &&
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CROSS-SECTIONAL IMAGING: MAGNETIC RESONANCE ENTEROGRAPHY VS. COMPUTED TOMOGRAPHY ENTEROGRAPHY Cross-sectional modalities such as MRE and CTE are now frequently used to evaluate pediatric patients with IBD because of their ability to visualize the lumen, transmural involvement and extraintestinal manifestations by utilizing intravenous contrast and neutral density oral contrast, which distends the small bowel, and allows better visualization and assessment of small bowel wall enhancement [11,15 ]. CTE is typically the preferred imaging of choice because of its wider availability and many benefits such as shorter scan duration, better spatial resolution, fewer motion artifacts, ubiquitous availability and lower cost. The major drawback of CTE is its inherent ionizing radiation exposure and the associated theoretical risk of malignancy induction. This risk is of particular concern in children who are at greater risk than adults from radiation exposure and of particular concern in those children with IBD because of the need for repeated examinations over the long time-course of the disease. MRE, on the other hand, is an ionizing radiation-free modality that has a better contrast resolution than CTE, the potential ability to distinguish between acute and chronic disease with novel techniques such as diffusion-weighted imaging, better performance in the evaluation of perianal disease compared with CT, and the ability to dynamically evaluate peristalsis, thereby facilitating the assessment of luminal narrowing, strictures, and adynamic segments due to inflammation. On the basis of the American College of Radiology (ACR) appropriateness criteria, CTE and MRE are equally recommended in the initial evaluation in pediatric patients with IBD [16]. The ACR recommends MRE for surveillance and mild symptoms [16]. CTE and CT of the abdomen and pelvis with positive enteric contrast is the recommended imaging modality for the evaluation of fever, acute abdomen and concerns for abscess in pediatric patients with an established diagnosis of IBD [16]. The revised Porto criteria by the European Society of Pediatric Gastroenterology, Hepatology and Nutrition recommend that MRE be the modality of choice at the time of initial diagnosis of IBD [15 ]. A recent study compared the accuracy of CTE and MRE in pediatric IBD patients and concluded that there is no statistically significant difference in the diagnostic accuracy in detecting active inflammation between the two methods [17 ]. MRE had higher sensitivity in diagnosing fibrosis in comparison with CTE in the same study, although not an
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increased specificity [17 ]. MRE was presumed to be better at distinguishing fibrosis from inflammation because of the superior soft-tissue contrast and the ability to assess bowel wall enhancement at multiple timepoints, which was proven by comparing MRE and CTE with full-thickness surgical and endoscopic histology [17 ]. The higher sensitivity of MRE in detecting fibrosis has led to a recommendation by some authors of using this exam as the modality of choice for assessing fibrosis. This point is important as it may impact the medical management and decision making [17 ,18]. Dedicated pelvic MRI is also considered the gold standard for evaluating pelvic anatomy for fistulas by identifying fluid-containing sinus tracts with peripheral enhancement and abscesses, which appear as extraluminal focal fluid collections with a contrast-enhanced rim [12 ,19]. Of note, 10% of pediatric Crohn’s disease patients have perianal fistula and an abscess at diagnosis [20]. MRI is often a very useful tool for surgeons to guide surgical management and can also help distinguish the perianal fistulas from a pilonidal sinus [21]. MRE and CTE are the useful tools to monitor response to biologic therapy, with studies showing correlation with clinical and endoscopic response [22,23]. One disadvantage of MRE and CTE is that it requires the patient to ingest large amounts of liquid contrast (20 ml/kg) in a short period of time to distend the bowel lumen. Inadequate ingestion or a delay in scanning decreases the accuracy of the test and the confidence in interpretation. The average scan time of MRE is 45 min compared to 2 min or less for CTE. In order to obtain quality images via MRE, the patient must lie still for an extended length of time and hold his or her breath at different points during the study, which can be difficult for young children. Sedation may be required in young patients if they are unable to lie still for the duration of the scan, with respiration and movement causing motion artifact [17 ,19]. Consultation with pediatric anesthesiologists may be warranted in this scenario to minimize the risk of aspiration following the ingestion of large amounts of oral contrast. There are less motion artifacts in CTE [24]. Intravenous glucagon can be administered during MRE to reduce bowel peristalsis, which will reduce motion artifact and improve image quality, but causes nausea and potentially emesis [25]. Another disadvantage is the cost difference, with MRE being costlier than a CTE. The Magnetic Resonance Index of Activity (MaRIA) score has been studied and validated in adults, and has shown a significant correlation with Crohn’s Disease Endoscopic Index of Severity (CDEIS) [26 ]. A multicenter trial assessing a similar index in children is currently &&
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underway. Interpretation of pediatric MRE and CTE is subjective and may require an experienced radiologist to interpret the scan, thereby somewhat limiting its availability [27]. In general, there is greater familiarity and comfort for radiologists with the interpretation of CTE than MRE [24]. CTE has been proven to be an effective imaging modality to evaluate the small intestine [17 ]. However, given the chronic relapsing course of disease in pediatric IBD patients, they often undergo repeated evaluations which may increase the risk of repeated ionizing radiation exposure. This may have additional impact upon the increased risk of malignancy secondary to disease and medical therapy [28]. Newer CT scanners and new protocols have reduced the radiation exposure by decreasing scan coverage, tube potential and current, and using novel reconstruction algorithms and image postprocessing techniques [29 ]. These techniques can reduce radiation exposure on average by 53–69%, from 15–20 to 5–7 mSv in adults [29 ]. When reduced radiation techniques are used, radiation exposure from CTE is similar to a small-bowel follow-through [24]. &&
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INTESTINAL FINDINGS Intestinal findings seen on cross-sectional imaging include bowel wall thickening, mucosal hyperenhancement, skip lesions, luminal narrowing, strictures, mural stratification and fistulae (Figs. 1–4).
EXTRAINTESTINAL MANIFESTATIONS Extraintestinal findings that can be seen on crosssectional imaging (CTE or MRE) include inflammatory fat stranding, engorgement of vasa recta, cutaneous manifestations, pancreatitis, urolithiasis, hepatobiliary lesions such as sclerosing cholangitis and hepatic steatosis, phlegmons and abscesses, lymphadenopathy, venous thromboembolism, enteropathic arthropathy and cholelithiasis [25]. The reader is referred to several excellent review articles in the radiology literature covering the imaging findings of IBD on MRE and CTE in the pediatric population [12 ,25]. &&
SMALL-BOWEL FOLLOW-THROUGH Fluoroscopy was traditionally considered the imaging modality of choice to examine the small bowel. However, small-bowel follow-through has been found to be relatively poor at evaluating transmural inflammation, and less sensitive than CTE and MRE in detecting terminal ileal inflammation [30]. Volume 26 Number 5 October 2014
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FIGURE 1. A 15-year-old boy with a history of small-bowel Crohn’s disease. (a) Spot image from small-bowel follow-through demonstrates several jejunal strictures (arrows). (b) Axial, postcontrast, fat-saturated T1-weighted image from subsequent MR enterography 1 year later demonstrates several loops of thick-walled, hyperenhancing small bowel (arrows) with adjacent inflammatory change consistent with active disease. A CT enterography was performed 1 year after the MR enterography. Axial (c) and coronal (d) images again demonstrate multiple loops of actively inflamed small bowel (arrows). CT, computed tomography; MR, magnetic resonance.
Fluoroscopy involves ionizing radiation exposure. Although fluoroscopy is readily available and relatively inexpensive, it has lost favor as a primary imaging modality in this clinical setting and is no longer recommended as a primary diagnostic tool in the imaging evaluation of IBD by the ACR appropriateness criteria [16,31].
TRANSABDOMINAL ULTRASONOGRAPHY Transabdominal ultrasonography (TUS) is a noninvasive, easily accessible and inexpensive tool to evaluate the bowel. However, TUS has its limitations in evaluating small-bowel disease. The examination is time consuming, intestinal gas can interfere with sonographic visualization, lack of bowel loop distention may limit complete evaluation and incomplete intestinal imaging provides only a partial assessment of the entire bowel. TUS sensitivity is variable in highly qualified centers with experienced sonographers. TUS is not routinely performed in most United States pediatric institutions because of the steep learning curve for the ultrasound technologists, the relatively long scan durations and the
relative high risk of false-negative results in Crohn’s disease patients because of the limited evaluation of the mucosa and submucosa [32,33].
SMALL INTESTINE CONTRAST ULTRASOUND A newer technique called small intestinal contrast ultrasound (SICUS) has been developed, mostly in Europe, to enhance visualization of the small bowel by utilizing a nondigestible, nonabsorbable and nonfermenting anechoic polyethylene glycol 4000 (PEG) solution which attracts water and is excreted in the stool [32]. On average, it takes 45 min to perform the ultrasound after ingestion of the contrast. The study requires the patient to drink a comparatively reduced volume of 250–500 ml of contrast [34 ]. To date, there are no studies published evaluating the use of SICUS in the United States; most of the literature published is from Italy. SICUS has been suggested as a first-line tool to assess the small intestine because it avoids ionizing radiation exposure, is noninvasive, inexpensive, less
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FIGURE 2. A 15-year-old girl with a history of Crohn’s disease. Axial, fat-saturated, T2-weighted pelvic MRI image demonstrates a hyperintense, horseshoe-shaped perianal collection (arrows). Postcontrast, fat-saturated, T1-weighted image demonstrates rim enhancement of this collection (arrow) with surrounding inflammation consistent with a perianal horseshoe abscess. &
time-consuming and has no side-effects [32,34 ]. However, ultrasound is an operator-dependent technique that requires an experienced sonographer to improve accuracy [32,34 ]. In the United States, MRE and CTE are still considered the gold standard in evaluating small intestinal lesions, with further research needed to compare the efficacy between MRE and SICUS. &
worn on the patient’s waist. It is indicated in patients with Crohn’s disease with poor growth, to assess their disease activity, and to differentiate Crohn’s disease from ulcerative colitis in patients with the diagnosis of IBDU. Studies have shown that VCE has the potential to identify greater disease
VIDEO CAPSULE ENDOSCOPY VCE allows for direct visualization of the small intestinal tract. The capsule measures 26 mm 11 mm and transmits images by radiofrequency to a sensor
FIGURE 3. A 13-year-old boy with a history of Crohn’s disease. Coronal, inversion recovery, weighted pelvic MRI image demonstrates a transsphincteric perianal fistula (arrow). 594
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FIGURE 4. A 13-year-old boy with a history of newly diagnosed Crohn’s disease. Coronal, postcontrast, fatsaturated T1-weighted image demonstrates multiple loops of thick-walled hyperenhancing mid-to-distal small bowel (arrows) consistent with active inflammation. Volume 26 Number 5 October 2014
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activity than was originally shown on small-bowel imaging using other modalities [13 ]. The disadvantages of VCE include missed lesions secondary to uncontrolled capsule movement, inability to obtain biopsies and the potential to cause an obstruction in patients with prior abdominal surgery or a stricture. Subsequently, it is recommended that patients undergo MRE or CTE, or receive a patency capsule prior to undergoing the VCE [15 ,35,36]. It is also recommended that patients who will be undergoing MRE following VCE obtain an abdominal radiograph if there is any uncertainty in whether the capsule has passed, as the capsules are not magnetic resonance compatible. &
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CONCLUSION Imaging plays a critical role in the evaluation of pediatric IBD patients. Imaging aids in the diagnosis of inflammation, strictures, fistulas and abscesses. Small-bowel follow-through is no longer considered the imaging modality of choice in these patients, and MRE is now the gold standard in most clinical scenarios in the pediatric population, though CTE remains a recommended modality for the initial diagnosis of a newly suspected child with IBD. MRE is preferred for surveillance purposes because it often can aid in distinguishing inflammation from fibrosis, eliminate exposure to ionizing radiation and, in combination with a pelvic MRI, can evaluate perianal disease. Ultrasound may also have a role in the diagnosis and surveillance of pediatric IBD. Selecting the most appropriate imaging modality for the evaluation of IBD in pediatric patients still remains patient specific, and close communication and collaboration between gastroenterologist and radiologist is critical in ensuring an optimal imaging algorithm. Cross-sectional imaging and endoscopy complement each other to create objective measures to assess the disease activity and monitor the response to treatment. Acknowledgements None. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Kim SC, Ferry GD. Inflammatory bowel diseases in pediatric and adolescent patients: clinical, therapeutic, and psychosocial considerations. Gastroenterology 2004; 126:1550–1560.
2. Kappelman MD, Rifas-Shiman SL, Kleinman K, et al. The prevalence and geographic distribution of Crohn’s disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol 2007; 5:1424–1429. 3. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 2004; 126: 1504–1517. 4. Cuffari C, Dubinsky M, Darbari A, et al. Crohn’s jejunoileitis: the pediatrician’s perspective on diagnosis and management. Inflamm Bowel Dis 2005; 11: 696–704. 5. Griffiths AM. Specificities of inflammatory bowel disease in childhood. Best Pract Res Clin Gastroenterol 2004; 18:509–523. 6. Sauer CG, Kugathasan S. Pediatric inflammatory bowel disease: highlighting pediatric differences in IBD. Gastroenterol Clin North Am 2009; 38:611– 628. 7. Prenzel F, Uhlig HH. Frequency of indeterminate colitis in children and adults with IBD – a metaanalysis. J Crohns Colitis 2009; 3:277–281. 8. Malaty HM, Mehta S, Abraham B, et al. The natural course of inflammatory bowel disease – indeterminate from childhood to adulthood: within a 25 year period. Clin Exp Gastroenterol 2013; 6:115–121. 9. Solberg IC, Vatn MH, Hoie O, et al. Clinical course in Crohn’s disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol 2007; 5:1430–1438. 10. Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn’s disease in the SONIC trial. Gut 2014; 63:88–95. 11. Gee MS, Nimkin K, Hsu M, et al. Prospective evaluation of MR enterography as the primary imaging modality for pediatric Crohn disease assessment. AJR Am J Roentgenol 2011; 197:224–231. 12. Towbin AJ, Sullivan J, Denson LA, et al. CT and MR enterography in children && and adolescents with inflammatory bowel disease. Radiographics 2013; 3:1843–1860. A review article discussing the benefits, imaging characteristics and findings from CT and MR enterography. 13. Min SB, Le-Carlson M, Singh N, et al. Video capsule endoscopy impacts & decision making in pediatric IBD: a single tertiary care center experience. Inflamm Bowel Dis 2013; 19:2139–2145. This study showed VCE is useful in pediatric Crohn’s disease patients not in remission, with poor growth, or to identify small-bowel disease. 14. Turner D, Griffiths AM. Acute severe ulcerative colitis in children: a systematic review. Inflamm Bowel Dis 2011; 17:440–449. 15. Levine A, Koletzko S, Turner D, et al. The ESPGHAN Revised Porto Criteria && for the diagnosis of inflammatory bowel disease in children and adolescents. J Pediatr Gastroenterol Nutr 2014; 58:795–806. ESPGHAN recommends that MRE is the imaging modality of choice in pediatric IBD. 16. Huprich JE, Rosen MP, Fidler JL, et al. ACR appropriateness criteria on Crohn’s disease. J Am Coll Radiol 2010; 7:94–102. 17. Quencer KB, Nimkin K, Mino-Kenudson M, Gee MS. Detecting active && inflammation and fibrosis in pediatric Crohn’s disease: prospective evaluation of MR-E and CT-E. Abdom Imaging 2013; 38:705–713. This study showed MRE and CTE in pediatric Crohn’s disease patients is comparable in detecting active inflammation, but MRE is superior in detecting fibrosis. 18. Siddiki HA, Fidler JL, Fletcher JG, et al. Prospective comparison of state-ofthe-art MR enterography and CT enterography in small-bowel Crohn’s disease. AJR Am J Roentgenol 2009; 193:113–121. 19. Schmidt S, Guibal A, Meuwly JY, et al. Acute complications of Crohn’s disease: comparison of multidetector-row computed tomographic enterography with magnetic resonance enterography. Digestion 2010; 82:229– 238. 20. Keljo DJ, Markowitz J, Langton C, et al. Course and treatment of perianal disease in children newly diagnosed with Crohn’s disease. Inflamm Bowel Dis 2009; 15:383–387. 21. Essary B, Kim J, Anupindi S, et al. Pelvic MRI in children with Crohn disease and suspected perianal involvement. Pediatr Radiol 2007; 37: 201–208. 22. Karmiris K, Bielen D, Vanbeckevoort D, et al. Long-term monitoring of infliximab therapy for perianal fistulizing Crohn’s disease by using magnetic resonance imaging. Clin Gastroenterol Hepatol 2011; 9:130–136. 23. Bruining DH, Loftus EV Jr, Ehman EC, et al. Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with Crohn’s disease. Clin Gastroenterol Hepatol 2011; 9:679–683. 24. Dillman JR, Adler J, Zimmermann EM, Strouse PJ. CT enterography of pediatric Crohn disease. Pediatr Radiol 2010; 40:97–105. 25. Hammer MR, Podberesky DJ, Dillman JR. Multidetector computed tomographic and magnetic resonance enterography in children: state of the art. Radiol Clin North Am 2013; 51:615–636. 26. Ordas I, Rimola J, Rodriguez S, et al. Accuracy of magnetic resonance && enterography in assessing response to therapy and mucosal healing in patients with Crohn’s disease. Gastroenterology 2014; 146:374.e1–382. e1. This is the first study which demonstrated that Magnetic Resonance Index of Activity (MaRIA) is a valid, accurate and reliable tool to assess therapeutic response in adults.
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Gastroenterology and nutrition 27. Horsthuis K, de Ridder L, Smets AM, et al. Magnetic resonance enterography for suspected inflammatory bowel disease in a pediatric population. J Pediatr Gastroenterol Nutr 2010; 51:603–609. 28. Fuchs Y, Markowitz J, Weinstein T, et al. Pediatric inflammatory bowel disease and imaging-related radiation: are we increasing the likelihood of malignancy? J Pediatr Gastroenterol Nutr 2011; 52:280–285. 29. Del Gaizo AJ, Fletcher JG, Yu L, et al. Reducing radiation dose in CT & enterography. Radiographics 2013; 33:1109–1124. This study showed that the use of low-dose techniques has reduced the radiation exposure by 53–69% for CTE examinations. 30. Lee SS, Kim AY, Yang SK, et al. Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology 2009; 251:751–761. 31. Fletcher JG, Fidler JL, Bruining DH, Huprich JE. New concepts in intestinal imaging for inflammatory bowel diseases. Gastroenterology 2011; 140: 1795–1806.
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32. Pallotta N, Baccini F, Corazziari E. Contrast ultrasonography of the normal small bowel. Ultrasound Med Biol 1999; 25:1335–1340. 33. Pallotta N, Tomei E, Viscido A, et al. Small intestine contrast ultrasonography: an alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis 2005; 11:146–153. 34. Pallotta N, Civitelli F, Di Nardo G, et al. Small intestine contrast ultrasono& graphy in pediatric Crohn’s disease. J Pediatr 2013; 163:778–784. This is the first study to demonstrate high sensitivity and specificity in detecting small-bowel lesions via SICUS in pediatric patients. 35. Fork FT, Karlsson N, Kadhem S, Ohlsson B. Small bowel enteroclysis with magnetic resonance imaging and computed tomography in patients with failed and uncertain passage of a patency capsule. BMC Med Imaging 2012; 12:3. 36. Cheifetz AS, Kornbluth AA, Legnani P, et al. The risk of retention of the capsule endoscope in patients with known or suspected Crohn’s disease. Am J Gastroenterol 2006; 101:2218–2222.
Volume 26 Number 5 October 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Imaging modalities in pediatric inflammatory bowel disease Ross Maltz a, Daniel J. Podberesky b, and Shehzad A. Saeed c
Purpose of review To review the various imaging modalities in the evaluation of pediatric inflammatory bowel disease (IBD) to determine disease location, clinical phenotype and the severity of disease in order to optimize treatment. Recent findings Assessment of the extent, location and severity of IBD routinely involves imaging of the gastrointestinal tract. Cross-sectional modalities such as magnetic resonance enterography (MRE) and computed tomography enterography visualize the lumen, transmural involvement, extraintestinal manifestations and may facilitate decision-making in disease management. MRE has evolved as the imaging modality of choice for many pediatric IBD indications because it does not involve exposure to ionizing radiation. Summary Advances in imaging modalities have revolutionized the assessment of children with IBD in recent years. Small-bowel follow-through is no longer considered the imaging modality of choice in this setting. Crosssectional enterography is now preferred because, among other advantages, it can potentially distinguish active inflammation from fibrosis, characterize stricturing and penetrating complications, and diagnose extraintestinal manifestations. Although MRE avoids ionizing radiation exposure, it remains costly. Crosssectional imaging and endoscopy complement each other in the development of objective measures for the assessment of disease activity and monitoring of response to treatment. Keywords computed tomography enterography, inflammatory bowel disease, magnetic resonance enterography, Porto criteria, small intestinal contrast ultrasonography
INTRODUCTION Inflammatory bowel disease (IBD) comprises Crohn’s disease and ulcerative colitis. There are a total of 4 million people worldwide with IBD, with 1.4 million residing in the United States, with approximately 25–30% presenting in childhood or adolescence [1]. The incidence of pediatric Crohn’s disease and ulcerative colitis within the United States is 43 per 100 000 and 28 per 100 000, respectively [2,3]. Studies indicate that 9–38% of pediatric Crohn’s disease cases only affect the small bowel, signifying the importance of determining disease location, clinical phenotype (inflammation, stricturing, or penetrating) and the severity of disease for treatment optimization [4,5]. The presentation of adult Crohn’s disease patients generally differs from that of pediatric Crohn’s disease patients. Pediatric patients typically present initially with inflammatory disease and progress to penetrating and stricturing disease over time [6]. Indeterminate colitis, more www.co-pediatrics.com
recently termed inflammatory bowel disease unclassified (IBDU), is an IBD that cannot be classified as Crohn’s disease or ulcerative colitis. There are higher rates of IBDU in pediatric patients compared with adult patients (13% in children vs. 6% in adults) [7]. The diagnosis of IBDU could alter the management and treatment [8]. Patients may have absence of symptoms, and undertreated or underappreciated
a Division of Gastroenterology, Hepatology and Nutrition, Nationwide Children’s Hospital, Columbus, Ohio, bDepartment of Radiology and c Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, USA
Correspondence to Shehzad A. Saeed, MD, Division of Gastroenterology, Hepatology and Nutrition, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, MLC 2010, Cincinnati, OH 45229, USA. Tel: +1 513 636 4415; fax: +1 513 636 7805; e-mail: Shehzad. [email protected] Curr Opin Pediatr 2014, 26:590–596 DOI:10.1097/MOP.0000000000000131 Volume 26 Number 5 October 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Pediatric inflammatory bowel disease Maltz et al.
KEY POINTS The European Society of Pediatric Gastroenterology, Hepatology and Nutrition recommends that MRE should be the imaging modality of choice in pediatric patients with inflammatory bowel disease. The American College of Radiology rates CTE and MRE equally in the initial evaluation of a child with IBD, and MRE above CTE for surveillance. Cross-sectional modalities such as MRE and CTE are now frequently used to evaluate pediatric patients with IBD because of their ability to visualize the lumen, transmural involvement and extraintestinal manifestations. MRI is the preferred modality for evaluating the pelvis and perineum for abscesses and fistulas, but may be limited because of the cost and availability.
disease can increase the risk of developing complications [9]. Traditional radiologic techniques and endoscopy typically assess the mucosa, whereas newer radiologic technologies such as MRI and computed tomography (CT) are able to determine whether inflammation exists in the deeper layers of the bowel wall and surrounding tissue [10]. Radiologic information facilitates the diagnosis and characterization of IBD, differentiation of ulcerative colitis from Crohn’s disease and aids in the monitoring of treatment efficacy [11]. A variety of imaging modalities are used to evaluate the gastrointestinal tract, each with its own advantages, disadvantages, risks and benefits. Specific tests are chosen for various reasons to supplement clinical data. When selecting an imaging modality, important factors to consider include reliability, accuracy, cost, side-effects, tolerability, accessibility, availability of expertise and radiation exposure. Additionally, it is crucial to use imaging at the time of diagnosis, to establish a baseline of disease activity and extent prior to escalating medical therapy, and to assess extraintestinal manifestations. Traditionally, imaging of the bowel relied on fluoroscopic barium studies such as small-bowel follow-through and contrast enema. However, new technologies such as magnetic resonance enterography (MRE) and computed tomography enterography (CTE) examine the intestinal cross-sections which provides more accurate diagnosis of inflammation, fibrosis and extraintestinal manifestations [12 ]. Video capsule endoscopy (VCE) is also used to visualize the gastrointestinal tract [13 ]. Abdominal radiographs are often still utilized to diagnose toxic megacolon, bowel obstruction and perforation [14]. &&
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CROSS-SECTIONAL IMAGING: MAGNETIC RESONANCE ENTEROGRAPHY VS. COMPUTED TOMOGRAPHY ENTEROGRAPHY Cross-sectional modalities such as MRE and CTE are now frequently used to evaluate pediatric patients with IBD because of their ability to visualize the lumen, transmural involvement and extraintestinal manifestations by utilizing intravenous contrast and neutral density oral contrast, which distends the small bowel, and allows better visualization and assessment of small bowel wall enhancement [11,15 ]. CTE is typically the preferred imaging of choice because of its wider availability and many benefits such as shorter scan duration, better spatial resolution, fewer motion artifacts, ubiquitous availability and lower cost. The major drawback of CTE is its inherent ionizing radiation exposure and the associated theoretical risk of malignancy induction. This risk is of particular concern in children who are at greater risk than adults from radiation exposure and of particular concern in those children with IBD because of the need for repeated examinations over the long time-course of the disease. MRE, on the other hand, is an ionizing radiation-free modality that has a better contrast resolution than CTE, the potential ability to distinguish between acute and chronic disease with novel techniques such as diffusion-weighted imaging, better performance in the evaluation of perianal disease compared with CT, and the ability to dynamically evaluate peristalsis, thereby facilitating the assessment of luminal narrowing, strictures, and adynamic segments due to inflammation. On the basis of the American College of Radiology (ACR) appropriateness criteria, CTE and MRE are equally recommended in the initial evaluation in pediatric patients with IBD [16]. The ACR recommends MRE for surveillance and mild symptoms [16]. CTE and CT of the abdomen and pelvis with positive enteric contrast is the recommended imaging modality for the evaluation of fever, acute abdomen and concerns for abscess in pediatric patients with an established diagnosis of IBD [16]. The revised Porto criteria by the European Society of Pediatric Gastroenterology, Hepatology and Nutrition recommend that MRE be the modality of choice at the time of initial diagnosis of IBD [15 ]. A recent study compared the accuracy of CTE and MRE in pediatric IBD patients and concluded that there is no statistically significant difference in the diagnostic accuracy in detecting active inflammation between the two methods [17 ]. MRE had higher sensitivity in diagnosing fibrosis in comparison with CTE in the same study, although not an
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increased specificity [17 ]. MRE was presumed to be better at distinguishing fibrosis from inflammation because of the superior soft-tissue contrast and the ability to assess bowel wall enhancement at multiple timepoints, which was proven by comparing MRE and CTE with full-thickness surgical and endoscopic histology [17 ]. The higher sensitivity of MRE in detecting fibrosis has led to a recommendation by some authors of using this exam as the modality of choice for assessing fibrosis. This point is important as it may impact the medical management and decision making [17 ,18]. Dedicated pelvic MRI is also considered the gold standard for evaluating pelvic anatomy for fistulas by identifying fluid-containing sinus tracts with peripheral enhancement and abscesses, which appear as extraluminal focal fluid collections with a contrast-enhanced rim [12 ,19]. Of note, 10% of pediatric Crohn’s disease patients have perianal fistula and an abscess at diagnosis [20]. MRI is often a very useful tool for surgeons to guide surgical management and can also help distinguish the perianal fistulas from a pilonidal sinus [21]. MRE and CTE are the useful tools to monitor response to biologic therapy, with studies showing correlation with clinical and endoscopic response [22,23]. One disadvantage of MRE and CTE is that it requires the patient to ingest large amounts of liquid contrast (20 ml/kg) in a short period of time to distend the bowel lumen. Inadequate ingestion or a delay in scanning decreases the accuracy of the test and the confidence in interpretation. The average scan time of MRE is 45 min compared to 2 min or less for CTE. In order to obtain quality images via MRE, the patient must lie still for an extended length of time and hold his or her breath at different points during the study, which can be difficult for young children. Sedation may be required in young patients if they are unable to lie still for the duration of the scan, with respiration and movement causing motion artifact [17 ,19]. Consultation with pediatric anesthesiologists may be warranted in this scenario to minimize the risk of aspiration following the ingestion of large amounts of oral contrast. There are less motion artifacts in CTE [24]. Intravenous glucagon can be administered during MRE to reduce bowel peristalsis, which will reduce motion artifact and improve image quality, but causes nausea and potentially emesis [25]. Another disadvantage is the cost difference, with MRE being costlier than a CTE. The Magnetic Resonance Index of Activity (MaRIA) score has been studied and validated in adults, and has shown a significant correlation with Crohn’s Disease Endoscopic Index of Severity (CDEIS) [26 ]. A multicenter trial assessing a similar index in children is currently &&
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underway. Interpretation of pediatric MRE and CTE is subjective and may require an experienced radiologist to interpret the scan, thereby somewhat limiting its availability [27]. In general, there is greater familiarity and comfort for radiologists with the interpretation of CTE than MRE [24]. CTE has been proven to be an effective imaging modality to evaluate the small intestine [17 ]. However, given the chronic relapsing course of disease in pediatric IBD patients, they often undergo repeated evaluations which may increase the risk of repeated ionizing radiation exposure. This may have additional impact upon the increased risk of malignancy secondary to disease and medical therapy [28]. Newer CT scanners and new protocols have reduced the radiation exposure by decreasing scan coverage, tube potential and current, and using novel reconstruction algorithms and image postprocessing techniques [29 ]. These techniques can reduce radiation exposure on average by 53–69%, from 15–20 to 5–7 mSv in adults [29 ]. When reduced radiation techniques are used, radiation exposure from CTE is similar to a small-bowel follow-through [24]. &&
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INTESTINAL FINDINGS Intestinal findings seen on cross-sectional imaging include bowel wall thickening, mucosal hyperenhancement, skip lesions, luminal narrowing, strictures, mural stratification and fistulae (Figs. 1–4).
EXTRAINTESTINAL MANIFESTATIONS Extraintestinal findings that can be seen on crosssectional imaging (CTE or MRE) include inflammatory fat stranding, engorgement of vasa recta, cutaneous manifestations, pancreatitis, urolithiasis, hepatobiliary lesions such as sclerosing cholangitis and hepatic steatosis, phlegmons and abscesses, lymphadenopathy, venous thromboembolism, enteropathic arthropathy and cholelithiasis [25]. The reader is referred to several excellent review articles in the radiology literature covering the imaging findings of IBD on MRE and CTE in the pediatric population [12 ,25]. &&
SMALL-BOWEL FOLLOW-THROUGH Fluoroscopy was traditionally considered the imaging modality of choice to examine the small bowel. However, small-bowel follow-through has been found to be relatively poor at evaluating transmural inflammation, and less sensitive than CTE and MRE in detecting terminal ileal inflammation [30]. Volume 26 Number 5 October 2014
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(a)
(b)
(c)
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FIGURE 1. A 15-year-old boy with a history of small-bowel Crohn’s disease. (a) Spot image from small-bowel follow-through demonstrates several jejunal strictures (arrows). (b) Axial, postcontrast, fat-saturated T1-weighted image from subsequent MR enterography 1 year later demonstrates several loops of thick-walled, hyperenhancing small bowel (arrows) with adjacent inflammatory change consistent with active disease. A CT enterography was performed 1 year after the MR enterography. Axial (c) and coronal (d) images again demonstrate multiple loops of actively inflamed small bowel (arrows). CT, computed tomography; MR, magnetic resonance.
Fluoroscopy involves ionizing radiation exposure. Although fluoroscopy is readily available and relatively inexpensive, it has lost favor as a primary imaging modality in this clinical setting and is no longer recommended as a primary diagnostic tool in the imaging evaluation of IBD by the ACR appropriateness criteria [16,31].
TRANSABDOMINAL ULTRASONOGRAPHY Transabdominal ultrasonography (TUS) is a noninvasive, easily accessible and inexpensive tool to evaluate the bowel. However, TUS has its limitations in evaluating small-bowel disease. The examination is time consuming, intestinal gas can interfere with sonographic visualization, lack of bowel loop distention may limit complete evaluation and incomplete intestinal imaging provides only a partial assessment of the entire bowel. TUS sensitivity is variable in highly qualified centers with experienced sonographers. TUS is not routinely performed in most United States pediatric institutions because of the steep learning curve for the ultrasound technologists, the relatively long scan durations and the
relative high risk of false-negative results in Crohn’s disease patients because of the limited evaluation of the mucosa and submucosa [32,33].
SMALL INTESTINE CONTRAST ULTRASOUND A newer technique called small intestinal contrast ultrasound (SICUS) has been developed, mostly in Europe, to enhance visualization of the small bowel by utilizing a nondigestible, nonabsorbable and nonfermenting anechoic polyethylene glycol 4000 (PEG) solution which attracts water and is excreted in the stool [32]. On average, it takes 45 min to perform the ultrasound after ingestion of the contrast. The study requires the patient to drink a comparatively reduced volume of 250–500 ml of contrast [34 ]. To date, there are no studies published evaluating the use of SICUS in the United States; most of the literature published is from Italy. SICUS has been suggested as a first-line tool to assess the small intestine because it avoids ionizing radiation exposure, is noninvasive, inexpensive, less
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FIGURE 2. A 15-year-old girl with a history of Crohn’s disease. Axial, fat-saturated, T2-weighted pelvic MRI image demonstrates a hyperintense, horseshoe-shaped perianal collection (arrows). Postcontrast, fat-saturated, T1-weighted image demonstrates rim enhancement of this collection (arrow) with surrounding inflammation consistent with a perianal horseshoe abscess. &
time-consuming and has no side-effects [32,34 ]. However, ultrasound is an operator-dependent technique that requires an experienced sonographer to improve accuracy [32,34 ]. In the United States, MRE and CTE are still considered the gold standard in evaluating small intestinal lesions, with further research needed to compare the efficacy between MRE and SICUS. &
worn on the patient’s waist. It is indicated in patients with Crohn’s disease with poor growth, to assess their disease activity, and to differentiate Crohn’s disease from ulcerative colitis in patients with the diagnosis of IBDU. Studies have shown that VCE has the potential to identify greater disease
VIDEO CAPSULE ENDOSCOPY VCE allows for direct visualization of the small intestinal tract. The capsule measures 26 mm 11 mm and transmits images by radiofrequency to a sensor
FIGURE 3. A 13-year-old boy with a history of Crohn’s disease. Coronal, inversion recovery, weighted pelvic MRI image demonstrates a transsphincteric perianal fistula (arrow). 594
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FIGURE 4. A 13-year-old boy with a history of newly diagnosed Crohn’s disease. Coronal, postcontrast, fatsaturated T1-weighted image demonstrates multiple loops of thick-walled hyperenhancing mid-to-distal small bowel (arrows) consistent with active inflammation. Volume 26 Number 5 October 2014
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activity than was originally shown on small-bowel imaging using other modalities [13 ]. The disadvantages of VCE include missed lesions secondary to uncontrolled capsule movement, inability to obtain biopsies and the potential to cause an obstruction in patients with prior abdominal surgery or a stricture. Subsequently, it is recommended that patients undergo MRE or CTE, or receive a patency capsule prior to undergoing the VCE [15 ,35,36]. It is also recommended that patients who will be undergoing MRE following VCE obtain an abdominal radiograph if there is any uncertainty in whether the capsule has passed, as the capsules are not magnetic resonance compatible. &
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CONCLUSION Imaging plays a critical role in the evaluation of pediatric IBD patients. Imaging aids in the diagnosis of inflammation, strictures, fistulas and abscesses. Small-bowel follow-through is no longer considered the imaging modality of choice in these patients, and MRE is now the gold standard in most clinical scenarios in the pediatric population, though CTE remains a recommended modality for the initial diagnosis of a newly suspected child with IBD. MRE is preferred for surveillance purposes because it often can aid in distinguishing inflammation from fibrosis, eliminate exposure to ionizing radiation and, in combination with a pelvic MRI, can evaluate perianal disease. Ultrasound may also have a role in the diagnosis and surveillance of pediatric IBD. Selecting the most appropriate imaging modality for the evaluation of IBD in pediatric patients still remains patient specific, and close communication and collaboration between gastroenterologist and radiologist is critical in ensuring an optimal imaging algorithm. Cross-sectional imaging and endoscopy complement each other to create objective measures to assess the disease activity and monitor the response to treatment. Acknowledgements None. Conflicts of interest There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Kim SC, Ferry GD. Inflammatory bowel diseases in pediatric and adolescent patients: clinical, therapeutic, and psychosocial considerations. Gastroenterology 2004; 126:1550–1560.
2. Kappelman MD, Rifas-Shiman SL, Kleinman K, et al. The prevalence and geographic distribution of Crohn’s disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol 2007; 5:1424–1429. 3. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology 2004; 126: 1504–1517. 4. Cuffari C, Dubinsky M, Darbari A, et al. Crohn’s jejunoileitis: the pediatrician’s perspective on diagnosis and management. Inflamm Bowel Dis 2005; 11: 696–704. 5. Griffiths AM. Specificities of inflammatory bowel disease in childhood. Best Pract Res Clin Gastroenterol 2004; 18:509–523. 6. Sauer CG, Kugathasan S. Pediatric inflammatory bowel disease: highlighting pediatric differences in IBD. Gastroenterol Clin North Am 2009; 38:611– 628. 7. Prenzel F, Uhlig HH. Frequency of indeterminate colitis in children and adults with IBD – a metaanalysis. J Crohns Colitis 2009; 3:277–281. 8. Malaty HM, Mehta S, Abraham B, et al. The natural course of inflammatory bowel disease – indeterminate from childhood to adulthood: within a 25 year period. Clin Exp Gastroenterol 2013; 6:115–121. 9. Solberg IC, Vatn MH, Hoie O, et al. Clinical course in Crohn’s disease: results of a Norwegian population-based ten-year follow-up study. Clin Gastroenterol Hepatol 2007; 5:1430–1438. 10. Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn’s disease in the SONIC trial. Gut 2014; 63:88–95. 11. Gee MS, Nimkin K, Hsu M, et al. Prospective evaluation of MR enterography as the primary imaging modality for pediatric Crohn disease assessment. AJR Am J Roentgenol 2011; 197:224–231. 12. Towbin AJ, Sullivan J, Denson LA, et al. CT and MR enterography in children && and adolescents with inflammatory bowel disease. Radiographics 2013; 3:1843–1860. A review article discussing the benefits, imaging characteristics and findings from CT and MR enterography. 13. Min SB, Le-Carlson M, Singh N, et al. Video capsule endoscopy impacts & decision making in pediatric IBD: a single tertiary care center experience. Inflamm Bowel Dis 2013; 19:2139–2145. This study showed VCE is useful in pediatric Crohn’s disease patients not in remission, with poor growth, or to identify small-bowel disease. 14. Turner D, Griffiths AM. Acute severe ulcerative colitis in children: a systematic review. Inflamm Bowel Dis 2011; 17:440–449. 15. Levine A, Koletzko S, Turner D, et al. The ESPGHAN Revised Porto Criteria && for the diagnosis of inflammatory bowel disease in children and adolescents. J Pediatr Gastroenterol Nutr 2014; 58:795–806. ESPGHAN recommends that MRE is the imaging modality of choice in pediatric IBD. 16. Huprich JE, Rosen MP, Fidler JL, et al. ACR appropriateness criteria on Crohn’s disease. J Am Coll Radiol 2010; 7:94–102. 17. Quencer KB, Nimkin K, Mino-Kenudson M, Gee MS. Detecting active && inflammation and fibrosis in pediatric Crohn’s disease: prospective evaluation of MR-E and CT-E. Abdom Imaging 2013; 38:705–713. This study showed MRE and CTE in pediatric Crohn’s disease patients is comparable in detecting active inflammation, but MRE is superior in detecting fibrosis. 18. Siddiki HA, Fidler JL, Fletcher JG, et al. Prospective comparison of state-ofthe-art MR enterography and CT enterography in small-bowel Crohn’s disease. AJR Am J Roentgenol 2009; 193:113–121. 19. Schmidt S, Guibal A, Meuwly JY, et al. Acute complications of Crohn’s disease: comparison of multidetector-row computed tomographic enterography with magnetic resonance enterography. Digestion 2010; 82:229– 238. 20. Keljo DJ, Markowitz J, Langton C, et al. Course and treatment of perianal disease in children newly diagnosed with Crohn’s disease. Inflamm Bowel Dis 2009; 15:383–387. 21. Essary B, Kim J, Anupindi S, et al. Pelvic MRI in children with Crohn disease and suspected perianal involvement. Pediatr Radiol 2007; 37: 201–208. 22. Karmiris K, Bielen D, Vanbeckevoort D, et al. Long-term monitoring of infliximab therapy for perianal fistulizing Crohn’s disease by using magnetic resonance imaging. Clin Gastroenterol Hepatol 2011; 9:130–136. 23. Bruining DH, Loftus EV Jr, Ehman EC, et al. Computed tomography enterography detects intestinal wall changes and effects of treatment in patients with Crohn’s disease. Clin Gastroenterol Hepatol 2011; 9:679–683. 24. Dillman JR, Adler J, Zimmermann EM, Strouse PJ. CT enterography of pediatric Crohn disease. Pediatr Radiol 2010; 40:97–105. 25. Hammer MR, Podberesky DJ, Dillman JR. Multidetector computed tomographic and magnetic resonance enterography in children: state of the art. Radiol Clin North Am 2013; 51:615–636. 26. Ordas I, Rimola J, Rodriguez S, et al. Accuracy of magnetic resonance && enterography in assessing response to therapy and mucosal healing in patients with Crohn’s disease. Gastroenterology 2014; 146:374.e1–382. e1. This is the first study which demonstrated that Magnetic Resonance Index of Activity (MaRIA) is a valid, accurate and reliable tool to assess therapeutic response in adults.
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Gastroenterology and nutrition 27. Horsthuis K, de Ridder L, Smets AM, et al. Magnetic resonance enterography for suspected inflammatory bowel disease in a pediatric population. J Pediatr Gastroenterol Nutr 2010; 51:603–609. 28. Fuchs Y, Markowitz J, Weinstein T, et al. Pediatric inflammatory bowel disease and imaging-related radiation: are we increasing the likelihood of malignancy? J Pediatr Gastroenterol Nutr 2011; 52:280–285. 29. Del Gaizo AJ, Fletcher JG, Yu L, et al. Reducing radiation dose in CT & enterography. Radiographics 2013; 33:1109–1124. This study showed that the use of low-dose techniques has reduced the radiation exposure by 53–69% for CTE examinations. 30. Lee SS, Kim AY, Yang SK, et al. Crohn disease of the small bowel: comparison of CT enterography, MR enterography, and small-bowel follow-through as diagnostic techniques. Radiology 2009; 251:751–761. 31. Fletcher JG, Fidler JL, Bruining DH, Huprich JE. New concepts in intestinal imaging for inflammatory bowel diseases. Gastroenterology 2011; 140: 1795–1806.
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32. Pallotta N, Baccini F, Corazziari E. Contrast ultrasonography of the normal small bowel. Ultrasound Med Biol 1999; 25:1335–1340. 33. Pallotta N, Tomei E, Viscido A, et al. Small intestine contrast ultrasonography: an alternative to radiology in the assessment of small bowel disease. Inflamm Bowel Dis 2005; 11:146–153. 34. Pallotta N, Civitelli F, Di Nardo G, et al. Small intestine contrast ultrasono& graphy in pediatric Crohn’s disease. J Pediatr 2013; 163:778–784. This is the first study to demonstrate high sensitivity and specificity in detecting small-bowel lesions via SICUS in pediatric patients. 35. Fork FT, Karlsson N, Kadhem S, Ohlsson B. Small bowel enteroclysis with magnetic resonance imaging and computed tomography in patients with failed and uncertain passage of a patency capsule. BMC Med Imaging 2012; 12:3. 36. Cheifetz AS, Kornbluth AA, Legnani P, et al. The risk of retention of the capsule endoscope in patients with known or suspected Crohn’s disease. Am J Gastroenterol 2006; 101:2218–2222.
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