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MR imaging of the gastro-intestinal tract in children
European Journal of Radiology 68 (2008) 271–277
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
MR imaging of the gastro-intestinal tract in children Marcus Hörmann ∗ Medical University of Vienna/General Hospital, Department of General and Paediatric Radiology, Währingergürtel 18-20, A-1090 Vienna, Austria
a r t i c l e
i n f o
Article history: Received 1 July 2008 Accepted 2 July 2008 Keywords: MRI Gastro-intestinal tract Inflammatory bowel disease Acute abdomen Paediatric
a b s t r a c t MR imaging (MRI) is an established method for the evaluation of particularly inflammatory bowel disease in adults, as well as for acute abdominal pain in pregnant women. Despite the fact that MRI is ideally suited for the evaluation of children the method is still not established in these patients. The value of MRI in Crohn’s disease, ulcerative colitis and appendicitis as well as intestinal tumors and malformations has been documented in children. There will be more indications in the future depending on the development of new imaging techniques, faster sequences, stronger gradients and increasing availability. Furthermore, the radiologist’s attention must be drawn to decrease the radiation burden in children and to replace ionizing techniques especially in chronic disease with the need for repeated follow-up studies and in younger children. This review will discuss some general considerations for the use of MRI in evaluating the paediatric gastro-intestinal tract. © 2008 Elsevier Ireland Ltd. All rights reserved.
1. Introduction MR imaging (MRI) of the gastro-intestinal (GI) tract is an established method in adults when diagnosing Crohn’s disease and ulcerative colitis (UC). In children MRI still is not established, despite the fact, that the lack of radiation burden would favour much more indications for the assessment of the GI tract. The use of MRI in children is a complex topic bearing some difficulties that limit its employment. Children in school age and particularly older than 9 years of age have no problems with undergoing MRI, but the younger ones may need to be handled gently, since their compliance might be poor. Never the less, MRI is more seldom performed as one would assume. In a literature survey one can only find a few scientific reports and reviews on MRI of the abdomen and the GI tract in children in particular [1–4]. But MRI is very appealing for the paediatric radiologists since it offers superb anatomical contrast without radiation burden. Allergic or hypersensitive reactions secondary to Gadolinium (Gd)-based contrast agents are much rare than with iodine-based contrast agents as used for computed tomography (CT); furthermore – due to the intrinsic MRI abilities – its use is less often necessary. Hence, MRI may more often be truly non-invasive than other imaging modalities. Some concerns in the use of Gdbased contrast agents have recently come to our knowledge, with – for the time being – reported five cases in children suffering from
∗ Tel.: +43 1 40 400 4819; fax: +43 1 40 400 4898. E-mail address: [email protected]. 0720-048X/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2008.07.019
nephrogenic systemic fibrosis (NSF) [5]. Other aspects such as the deposition of Gd in the bone marrow with its potential impact on the hematopoietic system give rise to careful and prudent use of this approach, particularly in infants and small children [5]. Despite the rapid improvement of faster sequences and coils with the use of stronger gradients the need of anesthesia or sedation in neonates, infants and young children persists with a longer preparation- and setup time. Children very often show up in the emergency department or outpatient facility with abdominal pain, on the one hand because the incidence of inflammatory bowel disease is increasing, and on the other hand because they tend to project somatic and socio-psychological disorders and problems in their belly. Thus, fortunately, often no underlying pathology can be found when examining these patients. But one must keep in mind that there are several important and in some cases severe abdominal diseases that can be encountered in children. The most common pathologic finding is mesenteric lymphadenopathy following upper airway infection or unspecific enteritis. Only the minority of children present with acute appendicitis, inflammatory bowel disease (IBD) like CD, UC, eosinophilic enteritis, Behcet’s syndrome, graft versus host disease, radiation- and indeterminate enteritis. Usually the radiological evaluation starts with ultrasound (US) and – in most cases – diagnosis can be established together with clinical examination and laboratory test without needing further radiological evaluation for deciding the therapeutic management. However, in some conditions, other sectional imaging may become necessary, and that’s the area where MRI may come into the game.
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M. Hörmann / European Journal of Radiology 68 (2008) 271–277
1.1. When should MRI be performed in children, and what to expect Indication for MRI is strongly depending on the age of the children since this somehow determines the spectrum of pathology. It might be useful to perform MRI in children who are small and cannot explain, show and name their discomfort to the examiner. In case of an acute abdomen and unclear abdominal pain it is mandatory to rule out surgical conditions. The major advantage in such a setting is the depiction of all abdominal organ systems covering almost all differential diagnosis of acute abdominal pain, avoiding the use of ionizing radiation [6]. The use of MRI for radiation protection is mostly advocated for pregnant women with acute abdominal pain and suspicion of appendicitis, whereas it is far less accepted or recommended as a reasonable approach in children [7,8]. Let us briefly address the most common or important entities and their typical features. 2. Appendicitis Some centres recommend the further use of MRI in cases of uncertain US results, untypical clinical presentation, and the suspicion of acute appendicitis in children [9,10]. Especially in obese children the use of MRI was helpful in depicting the vermiform appendix, again with the advantage of assessing the entire abdomen and ruling out the most common differential diagnoses of lower quadrant pain [11]. This approach is still discussed controversially, as some surgeons and emergency physicians doubt whether further imaging is really necessary and indicated in this condition, particularly in the light of growing economic pressure on medicine. On the other hand there are a lot of reports suggesting CT in uncertain cases of suspected appendicitis, despite its hazardous use of ionizing radiation in children [12]. In most cases children with suspicion of acute appendicitis are in school age and older, and therefore do not need sedation or anesthesia for a satisfactory MRI examination, which would have justified the use of a faster technique with radiation burden as constituted by CT. Acute non-perforated appendicitis has typical imaging features on MRI, similar to the findings on US. The outer diameter of the
Fig. 1. Axial T2-weighted sequence with fat saturation of an appendicitis presenting as a “target lesion” (arrowhead), behind small bowel loops with accompanying ascites. The US examination was unremarkable and the boy presented rather with scrotal pain.
vermiform appendix is exceeding 6 mm. The wall is slightly hyperintense on T2-weighted images, and the lumen of the appendix is fluid filled in most cases. The periappendiceal tissue is hyperintense on T2-weighted and fat suppressed short tau inversion recovery (STIR) images representing edematous changes (Fig. 1). Additionally some free fluid collections in the coecal region or in the cavum douglasi and local lymph nodes can be found. In case of perforated appendicitis an abscess formation can be found in the coecal region. In long standing cases inflammatory reaction of the adjacent small and large bowel can be encountered; in such cases differentiation from IBD or other inflammatory disease can be difficult (Fig. 2).
Fig. 2. Coronal (a) and sagittal (b) T1-weighted sequences after intravenous application of Gd demonstrating an enhancing, thickened appendix (arrow a) in a girl with suspected ovarian abnormality on US examination. Additionally there is an abscess formation next to the ovaries with rim enhancement (arrowhead a). (b) Shows the perforated appendicitis in an abscess formation, the arrowheads indicate the reactive thickening of adjacent bowel wall.
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Fig. 3. Axial T1-weighted sequence after Gd-administration showing a thickened duodenum with slight enhancement of the bowel wall (arrowheads) in a 13-year-old girl with histologically proven Crohn’s disease.
2.1. Inflammatory bowel disease The employment of MRI is relatively established in children with CD and UC, although there are only few reports on paediatric patients. In 20–30% of all affected patients, CD and UC are diagnosed at the age of 10–20 years. UC can even be found in young children and infants. In children – opposite to adults – an overlap of symptoms and clinical signs can be encountered making differentiation of both diseases in the paediatric patient difficult [1]. The relapsing course of CD in children necessitates further and repeated imaging with the least invasive technique and the lowest possible – or better even avoiding any – radiation [1]. Crohns disease, as in adults, can affect every part of the GI tract, but unlike in adults, the distribution in children is rather proximal (Fig. 3). Perirectal abscess formation, perineal fistulas in rectal involvement may occur, but are compared to adults more seldom encountered in children (Fig. 4). Typically skip lesions in the small bowel can be found. Imaging features of CD include a general edematous bowel wall with areas of transmural enhancement, terminal involvement and skip lesions. Paraintestinal fibrofatty proliferative changes and mesenteric lymphadenopathy may accompany these findings (Fig. 5). Fistulas and small abscess formation as well as rectal sparing are suggestive for CD, but seldom encountered in the paediatric patient group [3,12]. In chronic disease, fibrosis of the bowel wall can lead to wall thickening and to stenotic bowel loops. Meanwhile, some studies in adults have proven that the degree of wall enhancement correlates with the activity of the disease very well, even better than C-reactive protein and the CD-activity index; but these results were not yet evaluated in paediatric patients [3,14–16]. Ulcerative colitis is – in most cases – localized to the colon with the rectum affected primarily, and subsequent oral continuous extension of the disease. In 14–37% a pancolitis can be found, and if reflux through the ileocecal valve is present, an accompanying “backwash ileitis” may be seen [4,17,18]. Imaging features of florid UC (according to Darbari et al.) are mucosal enhancement with submucosal sparing showing a hypointense line on Gd-enhanced T1-weighted images, without wall thickening, whereas in chronic disease patients have atrophic mucosa and the inflammation can extend to the submucosa and the muscularis propria leading to wall thickening [4,13]. Most of the studies published show that the difference in contrast uptake of the bowel wall is the most valuable tool to differentiate CD from UC. Wall thickening and transmural enhancement of the terminal ileum is highly suggestive for
Fig. 4. Axial short tau inversion recovery (STIR) in a boy with colon involvement of Crohn’s disease (arrows a) shows a fistula reaching the anal sphincter muscle (arrow b). Marked enhancement of the fistula after Gd-administration (arrows c).
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however, are somehow contradictive, ranging from a good correlation of MRI with CD activity index and C-reactive protein to lack of any correlation with these parameters [15,19]. To our knowledge there are no reports, which evaluated the value of MRcolonography in children—particularly for these conditions. But there might be other paediatric interesting application of this novel technique such as evaluation of children with constipation and suspicion of Hirschsprung’s disease; only the future will show if MR-colonography will have the potential to replace barium enema for these queries. The number of children presenting with abdominal pain but normal laboratory findings and unremarkable US reports is quite high. Motility disorders would offer a possible explanation for the discomfort and pain in this patient group, but this condition is still awaiting further evaluation. The presently available techniques for bowel motility imaging are fluoroscopy and US. The use of long time fluoroscopy (at least 5 min for motility studies) is hazardous particularly in children because of the extensive radiation burden. The potential of US is restricted for this query as it cannot comprehensively visualize the entire GI tract simultaneously, additionally lacking a panoramic display and often being impaired by bowel gas. Watanbe et al. used a fast kinematic water selective excitation imaging (WATS-MR cine) MR technique for evaluation of the motility of the entire GI tract. MRI was obtained after overnight fasting and before eating, immediately after drinking 200–500 ml of a clear liquid, and 30 min postprandial. By comparing pre- and postprandial imaging the authors found several entities with motility disorders including hypoganglionosis, duodeno-gastric reflux in mesenteric artery syndrome, adhesive ileus, pseudobstruction and malrotation [20]. Thus, once its diagnostic value has been established, this approach might help in this specific patient subgroup as defined above, and may even give new insight into a variety of clinical conditions without yet known pathogenesis.
3. Other conditions
Fig. 5. Coronal T2-weighted sequence (a) showing the typical appearance of Crohn’s disease with thickened wall of the terminal ileum (arrowheads), marked enhancement of the bowel wall (arrow), collapsed lumen (b), inflammatory infiltration of the mesenteric fat (arrow c), and accompanying lymphadenopathy (arrowheads c).
CD. As shown by Laghi and co-workers these features were especially helpful in cases where the terminal ileum was not reached endoscopically [4]. The use of MR-colonography for IBD has been described in adults using the same imaging criteria as for evaluating the small bowel: wall thickness and contrast enhancement [6]. The results
There are some rare other paediatric GI-tract conditions when MRI may be considered despite the need for anaesthesia, particularly in infants with little fat and thus poor layer discrimination on CT, and when it is important to limit radiation burden. Congenital diseases of the GI-tract are in most cases diagnosed by fetal US and fetal MRI. In some instances a postnatal MRI evaluation may be helpful, for example, in anal atresia—either to determine the type of atresia or to evaluate the (pelvic floor) anatomy in detail pre- or postoperatively (Fig. 6). But despite some initial good experiences, the value of MRI in children with anal atresia for determination of the surgical technique or for (postoperative) functional assessment (MR-defaecography) still needs profound evaluation. Assessment of the preoperative anatomy is important in children with cloacal malformations, till to date this is achieved by fluoroscopy and/or sonographic genitography; In future these techniques may be replaced by (high resolution) MRI—particularly in the light of radiation protection (Fig. 7). Duplications of the intestines can be challenging for the radiologist, and usually are assessed by US and fluoroscopy; however, for unclear cases, differential diagnosis or preoperative assessment of suspected duplication the use of MRI should be considered as radiation free alternative to CT (Fig. 8). Tumours for themselves are no indication for MR imaging of the GI-tract, but one should always keep in mind that tumours of the GI-tract can cause discomfort, complaints, chronic and even acute abdominal pain. Hence, to rule out tumours of the GI-tract
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Fig. 6. Fetal MRI (a) showing a blind ending rectum (arrowhead) behind the bladder on T2-weighted images. The collecting system of the left kidney is dilated. Postnatal examination (b) demonstrates the high ending rectum (arrow) and the multicystic dysplastic right kidney (arrowhead).
the bowel system must always be assessed as well when performing abdominal MR imaging because of pain or discomfort. 3.1. Examination techniques The high soft tissue contrast of MRI often makes the intravenous administration of contrast agent unnecessary; these aspects make the technique ideally suited for the evaluation of bowel conditions in children. In case of an acute abdomen or young children it is important to rule out any indication for urgent surgery, which sometimes may not be achievable by US. In such cases a “fast MRI protocol” can be helpful. This consist of coronal T2weighted or STIR images in combination with axial T2-weighted and/or fat suppressed (STIR) T2-weighted images, and can be very helpful in either localizing the relevant pathology or quite reliably ruling out practically all indications for acute surgery [8]. With these two or three sequences the bowels, the urogenital system and the parenchymal organs can be evaluated. Acute appendicitis, ileus, inflammation of the ovaries, enteritis, lymphadenopathy, and gallbladder disorders can be detected. Further sequences should then be obtained according to the underlying pathology—if neces-
sary for deciding on therapy. Additional T1-weighted imaging in two orthogonal planes before and after Gd-administration should be performed when there is suspicion of ovarian pathology like ovarian torsion due to cysts or tumours, kidney pathology (either infection or obstruction), and suspicion of abscess formation [8]. The MRI assessment of the small intestine can be achieved by two ways. One possibility is the adaption of conventional enteroclysis technique, in which a gastric tube is positioned in the small bowel (= MR-enteroclysis). The placement can either be done with or without fluoroscopy using a balloon catheter to avoid backflow of contrast material into the stomach. Placing a nasojejunal tube is causing discomfort to younger patients and can in most cases be replaced by oral administration of contrast material. This constitutes the alternative approach, which is diagnostically sufficient in nearly all conditions and is more accepted by the children. The preparations are minimal; however, the child should be properly hydrated. One hour before scanning the child is drinking continuously approximately 300–500 ml of a hyperosmolar, nonabsorbable sugar-containing hexose solution (Mannitol) or similar commercially available liquids such as a polyethylene-glycol suspension. The hyperosmolar liquid promotes the transport of water
Fig. 7. Filling of a transversostoma, vaginostoma and catheterization of the cloaca (a) in a small girl with a cloacal malformation. The arrow indicates the rectum with a fecalith, which together with the dilated and refluxive right ureter (arrowheads), opens into the common cloaca. On the coronal T2-weighted sequence (b) arrows indicate the common cloaca, small arrowhead shows the uterus and big arrowhead shows the fecalith in the rectum. Arrows pointing at the rectum and bladder in (c), arrowhead indicates the short common duct of the bladder and rectum.
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nel coils, especially in bigger children where a larger field of view is necessary to cover the entire abdomen and pelvis. In young patients – where usually no sufficient breath holds can be achieved – the use of diaphragmatic tracking may help to reduce motion artefacts. To demonstrate CD rectal involvement or complications like fistulas and abscess formation MRI of the pelvic floor should be additionally performed. Axial and paracoronal (= coronal to the anal canal) T2-weighted and STIR images as well as T1-weighted images (mainly FLASH sequences) before and after i.v. administration of Gadolinium in the paracoronal and axial orientation with fat saturation should be obtained, as the relation of fistulas or abscess formation to the rectal sphincter muscles is crucial for therapy [21]. To my knowledge, no protocols and indications are published for MR-colonography in paediatric patients. Potentially, sequences as presented in a review published by Ajaj may be modified and adapted for use in children [22]. 4. Conclusion
Fig. 8. Sagittal T2-weighted sequence: arrowheads indicating a rectal duplication adjacent to the dorsal rectum wall with small hyperintense inflammatory retentions in the rectal wall.
into the lumen, which gives a favourable signal difference to the bowel wall. The use of a non-absorbable solution is advantageous because the volume of contrast may be reduced dramatically, making it more tolerable for children. The loss of water into the lumen should be substituted after the examination either by drinking or by i.v. administration of fluids, depending on the child’s ability to cooperate and its general state. Immediately before the examination children are asked to drink water to enable distension of the stomach and duodenum. The use of a spasmolyticum (e.g., Buscopan® ) can be considered shortly before i.v. administration of Gd in order to minimize artefacts due to intestinal peristalsis; however, with modern fast sequences and strong gradients the need for antiperistaltic drugs has dramatically decreased. Normally – with this technique – a sufficient distension of the entire small bowel can be achieved and even the ascending and transverse colon can be evaluated. Borthne et al. reported adverse events with this technique including diarrhoea in 76%, distaste in 58%, nausea in 73%, vomiting in 34%, abdominal discomfort in 71% and overall discomfort in 34% of patients, however, the question if children would repeat the examination was answered with yes by half of the patients. Despite the fact that there is no data about the tolerance of examination with enteroclysis one can assume that intubation and more volume of contrast is less well tolerated [3]. To properly monitor the fluid’s passage and to ensure adequate timing the i.v. Gd-administration coecal filling should be monitored. This can be achieved using either repeated T2-weighted half Fourier single shot turbo spin-echo (HASTE) sequences with single breath holds, or balanced fast field echo (BFFE) sequences with breath holds in 2 or 3 orientations. T1-weighted sequences with fat saturation after Gd-administration are needed to demonstrate inflammation and to assess the activity of the disease. Usually 3D fast-spoiled gradient-echo (GRE) or fast low-angle shot (FLASH) images with fat suppression are obtained in coronal and axial orientation during a single breath hold. True fast imaging with steady state free precession (SSFP = True-FISP, a special GRE sequence, with short TR and short acquisition time) is a fast sequence without the need for breath hold that is very appealing for paediatric use. The signal is neither T1- nor T2-weighted, but a hybrid that increases the signal of (intraluminal) fluid and (wall) contrast uptake. Multi-channel coils should be given favour to single chan-
The number of children showing up in the emergency units and outpatients facilities with abdominal pain and discomfort is increasing. The differential diagnosis of abdominal pain is ranging from motility disorders to IBD, urinary tract infection, gynaecologic pathology, hepato-biliary disease, manifestation of tumours or malformations, and other gastro-intestinal conditions that differ from IBD. Diagnosis can be established in many cases by US in combination with clinical examination and laboratory tests. In uncertain cases and in cases of IBD further imaging may become necessary. Attention must be paid to make use of the least invasive test at possibly lowest radiation burden. The improvement of sequences, coils, availability and imaging protocols, its high soft tissue contrast, and the lack of radiation burden make MRI very appealing for the use in paediatric patients [7,8,23]. Some studies have documented the value of MRI in different diseases of the GI tract, always calling MRI as most promising technique in children. MRI has been proven to be excellent in the evaluation of perforated appendicitis and IBD such as CD and UC, especially for follow-up and for determination of disease activity [1,3,10,11]. Further studies are still necessary to properly assess the value of MRI in monitoring the response to anti-inflammatory therapy [4]. The potential of MRI to evaluate GI tract motility seems promising, but also needs further investigations. MRI has been found valuable in the assessment of pregnant women presenting with “acute abdomen” and distinguishing GI tract disease from the respective differential diagnoses, but this still needs to be evaluated in (young) children [7,8]. MR-colonography is less invasive than colonoscopy, is free of radiation burden, and – in some indications – has the potential to once replace barium enemas. There are still centres that prefer fluoroscopic contrast studies and multislice-CT in the evaluation of the child’s intestines and acute abdomen, and there will be radiologists and clinicians relying primarily on the conventional imaging techniques with radiation hazards [1]. But, the development of the last years promises an increasing value and use of MRI in the evaluation of the paediatric intestines and thus the vision of an almost radiation free assessment of children might once come true. References [1] Mann EH. Inflammatory bowel disease: imaging of the paediatric patient. Semin Roentgenol 2008;43(1):29–38. [2] Durno CA, Sherman P, Williams T, Shuckett B, Dupuis A, Griffiths AM. Magnetic resonance imaging to distinguish the type and severity of pediatric inflammatory bowel disease. J Pediatr Gastroenterol Nutr 2000;30(2):170–4. [3] Borthne AS, Abdelnoor M, Rugtveit J, Perminow G, Reiseter T, Klow NE. Bowel magnetic resonance imaging of pediatric patients with oral mannitol. In: MRI compared to endoscopy and intestinal ultrasound; 2006.
M. Hörmann / European Journal of Radiology 68 (2008) 271–277 [4] Laghi A, Borelli O, Paoloantonio P, et al. Contrast enhanced magnetic resonance imaging of the terminal ileum in children with Crohn’s disease. Gut 2003;52:393–7. [5] Mendichovszky IA, Marks SD, Simcock CM, Olsen OE. Gadolinium and nephrogenic systemic fibrosis: time to tighten practice. Pediatr Radiol 2008;38:489–96. [6] MacKalski BA, Bernstein CN. New diagnostic imaging tools for inflammatory bowel disease. Gut 2006;55:733–41. [7] Singh A, Danrad R, Hahn PF, Blake MA, Mueller PR, Novelline RA. MR imaging of the acute abdomen and pelvis: appendicitis and beyond. Radiographics 2007;27:1419–31. [8] Pedrosa I, Rofsky NM. MR imaging in abdominal emergencies. Radiol Clin N Am 2003;41:1243–73. [9] Hörmann M, Paya K, Eibenberger K, et al. MR imaging in children with non-perforated acute appendicitis: value of unenhanced MR imaging in sonographically selected patients. AJR Am J Roentgenol 1998;171(2):467–70. [10] Inescu L, Coskun A, Selcuk MB, Akan H, Sozubir S, Bernay F. Acute appendicitis: MR imaging and sonographic correlation. AJR Am J Roentgenol 1997;168(3):283–94. [11] Hörmann M, Puig S, Prokesch SR, Partik B, Helbich TH. MR imaging of the normal appendix in children. Eur Radiol 2002;12(9):2313–6. [12] Rosendahl K, Aukland SM, Fosse K. Imaging strategies in children with suspected appendicitis. Eur Radiol 2004;14(Suppl. 4):L138–45. [13] Darbari A, Sena L, Argani P, Oliva-Hemker JM, Thompson R, Cuffari C. Gadolinium-enhanced magnetic resonance imaging: a useful radiological tool in diagnosing pediatric IBD. Inflamm Bowel Dis 2004;10:67–72.
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[14] Miao YM, Koh D-M, Amin Z, et al. Ultrasound and magnetic resonance imaging assessment of active bowel segments in Crohn’s disease. Clin Radiol 2002;57:913–8. [15] Schunk K, Kern A, Oberholzer K, et al. Hydro-MRI in Crohn’s disease: appraisal for disease activity. Invest Radiol 2000;35(7):431–7. [16] Schunk K. Small bowel magnetic resonance imaging for inflammatory bowel disease. Top Magn Reson Imaging 2002;13:409–25. [17] Mamula P, Markowitz JE, Baldassano RN. Inflammatory bowel disease in early childhood and adolescence: special considerations. Gastroenterol Clin North Am 2003;32:967–95. [18] Glickmann JN, Bousavaros A, Farraye FA, et al. Pediatric patients with untreated ulcerative colitis may present initially with unusual morphologic findings. Am J Surg Pathol 2004;28:190–7. [19] Maccioni F, Viscido A, Broglia L, et al. Evaluation of Crohn’s disease activity with magnetic resonance imaging Abdom Imaging 2000;25(3):219–28. [20] Watanabe Y, Ikegami R, Osuka A. The usefulness of dynamically balanced FFE WATS-MR imaging with kinematic display for studying pediatric gastrointestinal disease. Pediatr Surg Int 2005;21:868–72. [21] Spencer JA, Ward J, Beckingham IJ, Adams C, Ambrose NS. Dynamic contrast-enhanced MR imaging of perianal fistulas. AJR Am J Roentgenol 1996;167(3):735–41. [22] Ajaj W, Goyen M. MR imaging of the colon: “technique, indications, results and limitations”. Eur J Radiol 2007;61(3):415–23. [23] Kern A, Schunk K, Kessler M, Oberholzer K, Thelen M. Hydro-MRI for abdominal diagnostics in children. Rofo 2001;173(11):984–90.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
MR imaging of the gastro-intestinal tract in children Marcus Hörmann ∗ Medical University of Vienna/General Hospital, Department of General and Paediatric Radiology, Währingergürtel 18-20, A-1090 Vienna, Austria
a r t i c l e
i n f o
Article history: Received 1 July 2008 Accepted 2 July 2008 Keywords: MRI Gastro-intestinal tract Inflammatory bowel disease Acute abdomen Paediatric
a b s t r a c t MR imaging (MRI) is an established method for the evaluation of particularly inflammatory bowel disease in adults, as well as for acute abdominal pain in pregnant women. Despite the fact that MRI is ideally suited for the evaluation of children the method is still not established in these patients. The value of MRI in Crohn’s disease, ulcerative colitis and appendicitis as well as intestinal tumors and malformations has been documented in children. There will be more indications in the future depending on the development of new imaging techniques, faster sequences, stronger gradients and increasing availability. Furthermore, the radiologist’s attention must be drawn to decrease the radiation burden in children and to replace ionizing techniques especially in chronic disease with the need for repeated follow-up studies and in younger children. This review will discuss some general considerations for the use of MRI in evaluating the paediatric gastro-intestinal tract. © 2008 Elsevier Ireland Ltd. All rights reserved.
1. Introduction MR imaging (MRI) of the gastro-intestinal (GI) tract is an established method in adults when diagnosing Crohn’s disease and ulcerative colitis (UC). In children MRI still is not established, despite the fact, that the lack of radiation burden would favour much more indications for the assessment of the GI tract. The use of MRI in children is a complex topic bearing some difficulties that limit its employment. Children in school age and particularly older than 9 years of age have no problems with undergoing MRI, but the younger ones may need to be handled gently, since their compliance might be poor. Never the less, MRI is more seldom performed as one would assume. In a literature survey one can only find a few scientific reports and reviews on MRI of the abdomen and the GI tract in children in particular [1–4]. But MRI is very appealing for the paediatric radiologists since it offers superb anatomical contrast without radiation burden. Allergic or hypersensitive reactions secondary to Gadolinium (Gd)-based contrast agents are much rare than with iodine-based contrast agents as used for computed tomography (CT); furthermore – due to the intrinsic MRI abilities – its use is less often necessary. Hence, MRI may more often be truly non-invasive than other imaging modalities. Some concerns in the use of Gdbased contrast agents have recently come to our knowledge, with – for the time being – reported five cases in children suffering from
∗ Tel.: +43 1 40 400 4819; fax: +43 1 40 400 4898. E-mail address: [email protected]. 0720-048X/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2008.07.019
nephrogenic systemic fibrosis (NSF) [5]. Other aspects such as the deposition of Gd in the bone marrow with its potential impact on the hematopoietic system give rise to careful and prudent use of this approach, particularly in infants and small children [5]. Despite the rapid improvement of faster sequences and coils with the use of stronger gradients the need of anesthesia or sedation in neonates, infants and young children persists with a longer preparation- and setup time. Children very often show up in the emergency department or outpatient facility with abdominal pain, on the one hand because the incidence of inflammatory bowel disease is increasing, and on the other hand because they tend to project somatic and socio-psychological disorders and problems in their belly. Thus, fortunately, often no underlying pathology can be found when examining these patients. But one must keep in mind that there are several important and in some cases severe abdominal diseases that can be encountered in children. The most common pathologic finding is mesenteric lymphadenopathy following upper airway infection or unspecific enteritis. Only the minority of children present with acute appendicitis, inflammatory bowel disease (IBD) like CD, UC, eosinophilic enteritis, Behcet’s syndrome, graft versus host disease, radiation- and indeterminate enteritis. Usually the radiological evaluation starts with ultrasound (US) and – in most cases – diagnosis can be established together with clinical examination and laboratory test without needing further radiological evaluation for deciding the therapeutic management. However, in some conditions, other sectional imaging may become necessary, and that’s the area where MRI may come into the game.
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M. Hörmann / European Journal of Radiology 68 (2008) 271–277
1.1. When should MRI be performed in children, and what to expect Indication for MRI is strongly depending on the age of the children since this somehow determines the spectrum of pathology. It might be useful to perform MRI in children who are small and cannot explain, show and name their discomfort to the examiner. In case of an acute abdomen and unclear abdominal pain it is mandatory to rule out surgical conditions. The major advantage in such a setting is the depiction of all abdominal organ systems covering almost all differential diagnosis of acute abdominal pain, avoiding the use of ionizing radiation [6]. The use of MRI for radiation protection is mostly advocated for pregnant women with acute abdominal pain and suspicion of appendicitis, whereas it is far less accepted or recommended as a reasonable approach in children [7,8]. Let us briefly address the most common or important entities and their typical features. 2. Appendicitis Some centres recommend the further use of MRI in cases of uncertain US results, untypical clinical presentation, and the suspicion of acute appendicitis in children [9,10]. Especially in obese children the use of MRI was helpful in depicting the vermiform appendix, again with the advantage of assessing the entire abdomen and ruling out the most common differential diagnoses of lower quadrant pain [11]. This approach is still discussed controversially, as some surgeons and emergency physicians doubt whether further imaging is really necessary and indicated in this condition, particularly in the light of growing economic pressure on medicine. On the other hand there are a lot of reports suggesting CT in uncertain cases of suspected appendicitis, despite its hazardous use of ionizing radiation in children [12]. In most cases children with suspicion of acute appendicitis are in school age and older, and therefore do not need sedation or anesthesia for a satisfactory MRI examination, which would have justified the use of a faster technique with radiation burden as constituted by CT. Acute non-perforated appendicitis has typical imaging features on MRI, similar to the findings on US. The outer diameter of the
Fig. 1. Axial T2-weighted sequence with fat saturation of an appendicitis presenting as a “target lesion” (arrowhead), behind small bowel loops with accompanying ascites. The US examination was unremarkable and the boy presented rather with scrotal pain.
vermiform appendix is exceeding 6 mm. The wall is slightly hyperintense on T2-weighted images, and the lumen of the appendix is fluid filled in most cases. The periappendiceal tissue is hyperintense on T2-weighted and fat suppressed short tau inversion recovery (STIR) images representing edematous changes (Fig. 1). Additionally some free fluid collections in the coecal region or in the cavum douglasi and local lymph nodes can be found. In case of perforated appendicitis an abscess formation can be found in the coecal region. In long standing cases inflammatory reaction of the adjacent small and large bowel can be encountered; in such cases differentiation from IBD or other inflammatory disease can be difficult (Fig. 2).
Fig. 2. Coronal (a) and sagittal (b) T1-weighted sequences after intravenous application of Gd demonstrating an enhancing, thickened appendix (arrow a) in a girl with suspected ovarian abnormality on US examination. Additionally there is an abscess formation next to the ovaries with rim enhancement (arrowhead a). (b) Shows the perforated appendicitis in an abscess formation, the arrowheads indicate the reactive thickening of adjacent bowel wall.
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Fig. 3. Axial T1-weighted sequence after Gd-administration showing a thickened duodenum with slight enhancement of the bowel wall (arrowheads) in a 13-year-old girl with histologically proven Crohn’s disease.
2.1. Inflammatory bowel disease The employment of MRI is relatively established in children with CD and UC, although there are only few reports on paediatric patients. In 20–30% of all affected patients, CD and UC are diagnosed at the age of 10–20 years. UC can even be found in young children and infants. In children – opposite to adults – an overlap of symptoms and clinical signs can be encountered making differentiation of both diseases in the paediatric patient difficult [1]. The relapsing course of CD in children necessitates further and repeated imaging with the least invasive technique and the lowest possible – or better even avoiding any – radiation [1]. Crohns disease, as in adults, can affect every part of the GI tract, but unlike in adults, the distribution in children is rather proximal (Fig. 3). Perirectal abscess formation, perineal fistulas in rectal involvement may occur, but are compared to adults more seldom encountered in children (Fig. 4). Typically skip lesions in the small bowel can be found. Imaging features of CD include a general edematous bowel wall with areas of transmural enhancement, terminal involvement and skip lesions. Paraintestinal fibrofatty proliferative changes and mesenteric lymphadenopathy may accompany these findings (Fig. 5). Fistulas and small abscess formation as well as rectal sparing are suggestive for CD, but seldom encountered in the paediatric patient group [3,12]. In chronic disease, fibrosis of the bowel wall can lead to wall thickening and to stenotic bowel loops. Meanwhile, some studies in adults have proven that the degree of wall enhancement correlates with the activity of the disease very well, even better than C-reactive protein and the CD-activity index; but these results were not yet evaluated in paediatric patients [3,14–16]. Ulcerative colitis is – in most cases – localized to the colon with the rectum affected primarily, and subsequent oral continuous extension of the disease. In 14–37% a pancolitis can be found, and if reflux through the ileocecal valve is present, an accompanying “backwash ileitis” may be seen [4,17,18]. Imaging features of florid UC (according to Darbari et al.) are mucosal enhancement with submucosal sparing showing a hypointense line on Gd-enhanced T1-weighted images, without wall thickening, whereas in chronic disease patients have atrophic mucosa and the inflammation can extend to the submucosa and the muscularis propria leading to wall thickening [4,13]. Most of the studies published show that the difference in contrast uptake of the bowel wall is the most valuable tool to differentiate CD from UC. Wall thickening and transmural enhancement of the terminal ileum is highly suggestive for
Fig. 4. Axial short tau inversion recovery (STIR) in a boy with colon involvement of Crohn’s disease (arrows a) shows a fistula reaching the anal sphincter muscle (arrow b). Marked enhancement of the fistula after Gd-administration (arrows c).
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however, are somehow contradictive, ranging from a good correlation of MRI with CD activity index and C-reactive protein to lack of any correlation with these parameters [15,19]. To our knowledge there are no reports, which evaluated the value of MRcolonography in children—particularly for these conditions. But there might be other paediatric interesting application of this novel technique such as evaluation of children with constipation and suspicion of Hirschsprung’s disease; only the future will show if MR-colonography will have the potential to replace barium enema for these queries. The number of children presenting with abdominal pain but normal laboratory findings and unremarkable US reports is quite high. Motility disorders would offer a possible explanation for the discomfort and pain in this patient group, but this condition is still awaiting further evaluation. The presently available techniques for bowel motility imaging are fluoroscopy and US. The use of long time fluoroscopy (at least 5 min for motility studies) is hazardous particularly in children because of the extensive radiation burden. The potential of US is restricted for this query as it cannot comprehensively visualize the entire GI tract simultaneously, additionally lacking a panoramic display and often being impaired by bowel gas. Watanbe et al. used a fast kinematic water selective excitation imaging (WATS-MR cine) MR technique for evaluation of the motility of the entire GI tract. MRI was obtained after overnight fasting and before eating, immediately after drinking 200–500 ml of a clear liquid, and 30 min postprandial. By comparing pre- and postprandial imaging the authors found several entities with motility disorders including hypoganglionosis, duodeno-gastric reflux in mesenteric artery syndrome, adhesive ileus, pseudobstruction and malrotation [20]. Thus, once its diagnostic value has been established, this approach might help in this specific patient subgroup as defined above, and may even give new insight into a variety of clinical conditions without yet known pathogenesis.
3. Other conditions
Fig. 5. Coronal T2-weighted sequence (a) showing the typical appearance of Crohn’s disease with thickened wall of the terminal ileum (arrowheads), marked enhancement of the bowel wall (arrow), collapsed lumen (b), inflammatory infiltration of the mesenteric fat (arrow c), and accompanying lymphadenopathy (arrowheads c).
CD. As shown by Laghi and co-workers these features were especially helpful in cases where the terminal ileum was not reached endoscopically [4]. The use of MR-colonography for IBD has been described in adults using the same imaging criteria as for evaluating the small bowel: wall thickness and contrast enhancement [6]. The results
There are some rare other paediatric GI-tract conditions when MRI may be considered despite the need for anaesthesia, particularly in infants with little fat and thus poor layer discrimination on CT, and when it is important to limit radiation burden. Congenital diseases of the GI-tract are in most cases diagnosed by fetal US and fetal MRI. In some instances a postnatal MRI evaluation may be helpful, for example, in anal atresia—either to determine the type of atresia or to evaluate the (pelvic floor) anatomy in detail pre- or postoperatively (Fig. 6). But despite some initial good experiences, the value of MRI in children with anal atresia for determination of the surgical technique or for (postoperative) functional assessment (MR-defaecography) still needs profound evaluation. Assessment of the preoperative anatomy is important in children with cloacal malformations, till to date this is achieved by fluoroscopy and/or sonographic genitography; In future these techniques may be replaced by (high resolution) MRI—particularly in the light of radiation protection (Fig. 7). Duplications of the intestines can be challenging for the radiologist, and usually are assessed by US and fluoroscopy; however, for unclear cases, differential diagnosis or preoperative assessment of suspected duplication the use of MRI should be considered as radiation free alternative to CT (Fig. 8). Tumours for themselves are no indication for MR imaging of the GI-tract, but one should always keep in mind that tumours of the GI-tract can cause discomfort, complaints, chronic and even acute abdominal pain. Hence, to rule out tumours of the GI-tract
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Fig. 6. Fetal MRI (a) showing a blind ending rectum (arrowhead) behind the bladder on T2-weighted images. The collecting system of the left kidney is dilated. Postnatal examination (b) demonstrates the high ending rectum (arrow) and the multicystic dysplastic right kidney (arrowhead).
the bowel system must always be assessed as well when performing abdominal MR imaging because of pain or discomfort. 3.1. Examination techniques The high soft tissue contrast of MRI often makes the intravenous administration of contrast agent unnecessary; these aspects make the technique ideally suited for the evaluation of bowel conditions in children. In case of an acute abdomen or young children it is important to rule out any indication for urgent surgery, which sometimes may not be achievable by US. In such cases a “fast MRI protocol” can be helpful. This consist of coronal T2weighted or STIR images in combination with axial T2-weighted and/or fat suppressed (STIR) T2-weighted images, and can be very helpful in either localizing the relevant pathology or quite reliably ruling out practically all indications for acute surgery [8]. With these two or three sequences the bowels, the urogenital system and the parenchymal organs can be evaluated. Acute appendicitis, ileus, inflammation of the ovaries, enteritis, lymphadenopathy, and gallbladder disorders can be detected. Further sequences should then be obtained according to the underlying pathology—if neces-
sary for deciding on therapy. Additional T1-weighted imaging in two orthogonal planes before and after Gd-administration should be performed when there is suspicion of ovarian pathology like ovarian torsion due to cysts or tumours, kidney pathology (either infection or obstruction), and suspicion of abscess formation [8]. The MRI assessment of the small intestine can be achieved by two ways. One possibility is the adaption of conventional enteroclysis technique, in which a gastric tube is positioned in the small bowel (= MR-enteroclysis). The placement can either be done with or without fluoroscopy using a balloon catheter to avoid backflow of contrast material into the stomach. Placing a nasojejunal tube is causing discomfort to younger patients and can in most cases be replaced by oral administration of contrast material. This constitutes the alternative approach, which is diagnostically sufficient in nearly all conditions and is more accepted by the children. The preparations are minimal; however, the child should be properly hydrated. One hour before scanning the child is drinking continuously approximately 300–500 ml of a hyperosmolar, nonabsorbable sugar-containing hexose solution (Mannitol) or similar commercially available liquids such as a polyethylene-glycol suspension. The hyperosmolar liquid promotes the transport of water
Fig. 7. Filling of a transversostoma, vaginostoma and catheterization of the cloaca (a) in a small girl with a cloacal malformation. The arrow indicates the rectum with a fecalith, which together with the dilated and refluxive right ureter (arrowheads), opens into the common cloaca. On the coronal T2-weighted sequence (b) arrows indicate the common cloaca, small arrowhead shows the uterus and big arrowhead shows the fecalith in the rectum. Arrows pointing at the rectum and bladder in (c), arrowhead indicates the short common duct of the bladder and rectum.
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nel coils, especially in bigger children where a larger field of view is necessary to cover the entire abdomen and pelvis. In young patients – where usually no sufficient breath holds can be achieved – the use of diaphragmatic tracking may help to reduce motion artefacts. To demonstrate CD rectal involvement or complications like fistulas and abscess formation MRI of the pelvic floor should be additionally performed. Axial and paracoronal (= coronal to the anal canal) T2-weighted and STIR images as well as T1-weighted images (mainly FLASH sequences) before and after i.v. administration of Gadolinium in the paracoronal and axial orientation with fat saturation should be obtained, as the relation of fistulas or abscess formation to the rectal sphincter muscles is crucial for therapy [21]. To my knowledge, no protocols and indications are published for MR-colonography in paediatric patients. Potentially, sequences as presented in a review published by Ajaj may be modified and adapted for use in children [22]. 4. Conclusion
Fig. 8. Sagittal T2-weighted sequence: arrowheads indicating a rectal duplication adjacent to the dorsal rectum wall with small hyperintense inflammatory retentions in the rectal wall.
into the lumen, which gives a favourable signal difference to the bowel wall. The use of a non-absorbable solution is advantageous because the volume of contrast may be reduced dramatically, making it more tolerable for children. The loss of water into the lumen should be substituted after the examination either by drinking or by i.v. administration of fluids, depending on the child’s ability to cooperate and its general state. Immediately before the examination children are asked to drink water to enable distension of the stomach and duodenum. The use of a spasmolyticum (e.g., Buscopan® ) can be considered shortly before i.v. administration of Gd in order to minimize artefacts due to intestinal peristalsis; however, with modern fast sequences and strong gradients the need for antiperistaltic drugs has dramatically decreased. Normally – with this technique – a sufficient distension of the entire small bowel can be achieved and even the ascending and transverse colon can be evaluated. Borthne et al. reported adverse events with this technique including diarrhoea in 76%, distaste in 58%, nausea in 73%, vomiting in 34%, abdominal discomfort in 71% and overall discomfort in 34% of patients, however, the question if children would repeat the examination was answered with yes by half of the patients. Despite the fact that there is no data about the tolerance of examination with enteroclysis one can assume that intubation and more volume of contrast is less well tolerated [3]. To properly monitor the fluid’s passage and to ensure adequate timing the i.v. Gd-administration coecal filling should be monitored. This can be achieved using either repeated T2-weighted half Fourier single shot turbo spin-echo (HASTE) sequences with single breath holds, or balanced fast field echo (BFFE) sequences with breath holds in 2 or 3 orientations. T1-weighted sequences with fat saturation after Gd-administration are needed to demonstrate inflammation and to assess the activity of the disease. Usually 3D fast-spoiled gradient-echo (GRE) or fast low-angle shot (FLASH) images with fat suppression are obtained in coronal and axial orientation during a single breath hold. True fast imaging with steady state free precession (SSFP = True-FISP, a special GRE sequence, with short TR and short acquisition time) is a fast sequence without the need for breath hold that is very appealing for paediatric use. The signal is neither T1- nor T2-weighted, but a hybrid that increases the signal of (intraluminal) fluid and (wall) contrast uptake. Multi-channel coils should be given favour to single chan-
The number of children showing up in the emergency units and outpatients facilities with abdominal pain and discomfort is increasing. The differential diagnosis of abdominal pain is ranging from motility disorders to IBD, urinary tract infection, gynaecologic pathology, hepato-biliary disease, manifestation of tumours or malformations, and other gastro-intestinal conditions that differ from IBD. Diagnosis can be established in many cases by US in combination with clinical examination and laboratory tests. In uncertain cases and in cases of IBD further imaging may become necessary. Attention must be paid to make use of the least invasive test at possibly lowest radiation burden. The improvement of sequences, coils, availability and imaging protocols, its high soft tissue contrast, and the lack of radiation burden make MRI very appealing for the use in paediatric patients [7,8,23]. Some studies have documented the value of MRI in different diseases of the GI tract, always calling MRI as most promising technique in children. MRI has been proven to be excellent in the evaluation of perforated appendicitis and IBD such as CD and UC, especially for follow-up and for determination of disease activity [1,3,10,11]. Further studies are still necessary to properly assess the value of MRI in monitoring the response to anti-inflammatory therapy [4]. The potential of MRI to evaluate GI tract motility seems promising, but also needs further investigations. MRI has been found valuable in the assessment of pregnant women presenting with “acute abdomen” and distinguishing GI tract disease from the respective differential diagnoses, but this still needs to be evaluated in (young) children [7,8]. MR-colonography is less invasive than colonoscopy, is free of radiation burden, and – in some indications – has the potential to once replace barium enemas. There are still centres that prefer fluoroscopic contrast studies and multislice-CT in the evaluation of the child’s intestines and acute abdomen, and there will be radiologists and clinicians relying primarily on the conventional imaging techniques with radiation hazards [1]. But, the development of the last years promises an increasing value and use of MRI in the evaluation of the paediatric intestines and thus the vision of an almost radiation free assessment of children might once come true. References [1] Mann EH. Inflammatory bowel disease: imaging of the paediatric patient. Semin Roentgenol 2008;43(1):29–38. [2] Durno CA, Sherman P, Williams T, Shuckett B, Dupuis A, Griffiths AM. Magnetic resonance imaging to distinguish the type and severity of pediatric inflammatory bowel disease. J Pediatr Gastroenterol Nutr 2000;30(2):170–4. [3] Borthne AS, Abdelnoor M, Rugtveit J, Perminow G, Reiseter T, Klow NE. Bowel magnetic resonance imaging of pediatric patients with oral mannitol. In: MRI compared to endoscopy and intestinal ultrasound; 2006.
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