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Digestive and Liver Disease 43 (2011) 220–224

Contents lists available at ScienceDirect

Digestive and Liver Disease

journa l homepage: www.e lsev ier .com/ locate /d ld

igestive Endoscopy

sefulness of wireless capsule endoscopy in paediatric inflammatoryowel disease

iovanni Di Nardoa,1 , Salvatore Olivaa,1 , Federica Ferrari a , Maria Elena Riccionib , Annamaria Staianoc,iuliano Lombardid, Guido Costamagnab, Salvatore Cucchiaraa, Laura Stronati a,∗

Pediatric Gastroenterology and Liver Unit, Sapienza University of Rome, ItalyGastrointestinal Endoscopy Unit, Catholic University of Rome, ItalyPediatric Gastroenterology Unit, University of Naples Federico II, ItalyPediatric Gastroenterology Unit, Hospital of Pescara, Italy

r t i c l e i n f o

rticle history:eceived 22 June 2010ccepted 11 October 2010vailable online 18 November 2010

eywords:ndoscopynflammatory bowel disease

a b s t r a c t

Background: Small bowel endoscopy is critical in revealing an inflammatory bowel disease (IBD) previ-ously undetected and in classifying the IBD patients, i.e. Crohn’s disease or ulcerative colitis.Methods: A prospective paediatric study on the usefulness of wireless capsule endoscopy (WCE) wasperformed in 117 children (age range: 4–17 years) with established or suspected IBD and compared withnon endoscopic imaging tools. All patients underwent upper and lower gastrointestinal endoscopy.Results: In Crohn’s disease patients (CD, n = 44), small bowel lesions were revealed by imaging tools in8 and by WCE in 18 patients, respectively (p < 0.01). No small bowel involvement was observed in 29

aediatricsmall bowelideocapsule

ulcerative colitis patients by both imaging tools and WCE. Of 26 unclassified IBD, small bowel lesionstypical of Crohn’s disease were detected by imaging in 7 and by WCE in 16 (p < 0.05). Of 18 patients withsuspected IBD, small bowel lesions typical of Crohn’s disease were observed in 9 with WCE, vs. only in 4with imaging (p < 0.01). No cases of capsule retention occurred.Conclusions: WCE is valuable in revealing small bowel lesions in children with a previous diagnosis of CDand unexplained clinical and laboratory data. It is also helpful in unclassified IBD patients. This tool can

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influence the manageme© 2010 Editrice

. Introduction

An increased incidence of paediatric inflammatory bowel dis-ase (IBD) has recently been reported in western countries, withlmost 10–12 novel cases per 100.000/year [1,2]. Two diseaseubtypes, Crohn’s disease (CD) and ulcerative colitis (UC) are thelassical forms of IBD, and their definite diagnosis is based onidely clinical, endoscopic, histopathologic and imaging criteria

3,4]. Establishing the subtype of IBD is crucial in predicting theisease course as well as in choosing appropriate treatment inter-

entions. In the management of IBD patients, investigation of smallowel is fundamental since its involvement may definitely indicatehe presence of CD; furthermore, assessing small bowel involve-

ent in CD patients may be helpful both in making therapeutic

∗ Corresponding author at: Department of Pediatrics, Pediatric Gastroenterologynd Liver Unit, University Hospital Umberto I, Sapienza University of Rome, Vialeegina Elena 324, 00161, Rome, Italy. Tel.: +39 0649979326/9324/9269;

ax: +39 0649979325.E-mail address: laura.stronati@enea.it (L. Stronati).

1 These authors contributed equally to this study.

590-8658/$36.00 © 2010 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevieroi:10.1016/j.dld.2010.10.004

the course of IBD.roenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.

decision and planning the follow up [5,6]. Evaluation of the smallbowel is also mandatory in cases labelled as IBD unclassified (IBDU)for which traditional endoscopy and histopathology do not dis-criminate between CD and UC [7]. This entity, also known asindeterminate colitis (this term should be reserved for patients inwhom surgical specimens of the gut are available) may occur in upto 1/5 of a paediatric population with IBD referred to a tertiary cen-ter [1]. Traditional imaging methods to evaluate small bowel arecontrast X-ray examination, ultrasound and magnetic resonanceimaging (MRI) [8]. The latter seems to have a great sensitivity andspecificity and has recently gained a wide acceptance among paedi-atric gastroenterologists since it is radiation free and suitable bothfor the initial approach and the follow up of IBD [9]. Wireless cap-sule endoscopy (WCE) has dramatically changed the explorationof the intestine and has shown high diagnostic efficacy for vari-ous gut disorders [10]. Whereas WCE has been shown to improvethe diagnostic yield in adults with IBD, paediatric reports are few,

mostly retrospective [11,12] or include small number of patients[13,14].

In this study we aimed to assess prospectively the ability ofWCE in refining the approach to a large cohort of children with

Ltd. All rights reserved.

nd Liver Disease 43 (2011) 220–224 221

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Table 1Clinical characteristics of Crohn’s disease patients undergoing capsule endoscopy.

No. of cases 44Age (years; median and ranges) 12.7 years (6–21)Age at diagnosis (years; median and range) 10.9 years (6–15)Gender

Male (%) 25 (56.8%)Disease locationa

L1 = terminal ileum 6 (13.6%)L2 = colon 9 (20.5%)L3 = ileocolon 27 (61.4%)L4 = upper GI 2 (0.5%)

Behavioura

G. Di Nardo et al. / Digestive a

nown or suspected IBD, referred to tertiary centers of Pediatricastroenterology for small bowel endoscopy.

. Patients and methods

One-hundred and thirty-three paediatric patients with knownr suspected IBD (median age: 11.2 years; range age: 4–17 years)ere consecutively referred to tertiary centers for small bowel

ndoscopy through WCE. Patients were not eligible for WCE if theyad swallowing disorders, oesophageal stenosis, known GI motilitybnormalities, small bowel strictures at ultrasonography ad/or MRInd/or X-ray contrast examination. One-hundred and seventeenatients were suitable for this investigation: 16 were dischargedecause of stenosis at imaging tools [6], previous surgery [4], lack ofooperation [4], high severity of the disease with systemic featuresnd malnutrition [2].

The reasons for performing WCE were: (1) children with anstablished CD (44 cases; median age: 11.0 years; range: 6–17) inost of which clinical and laboratory signs (i.e. diarrhoea, haema-

ochezia, severe abdominal pain, fever, refractory anaemia, lowerum albumine, high plasma levels of acute phase reactants)ere not fully explained by features revealed by conventional

ndoscopy; (2) children with previous diagnosis of UC (29 cases;edian age 11.6; range: 5–17), needing to definitely exclude CD

olitis; (3) further classification of a group of IBD children (26 cases;edian age 10.0 years; range: 4–16) who had received a diagnosis

f IBDU; (4) children with haematochezia and signs of small bowelisorders (18 cases; median age: 10.5 years; range: 5–17), without aefinite diagnosis with traditional gastrointestinal (GI) endoscopy.

All patients underwent diagnostic work-up including ileo-olonoscopy and upper GI endoscopy under general anaesthesia oronscious sedation. Diagnosis and classification of IBD were basedn commonly agreed criteria [3,4]. Infectious and immunologicaliseases as well as malabsorption syndromes and food allergy werexcluded in all. Intestinal obstruction had been excluded with MRIr small intestine contrast ultrasonography (SICUS). The method-logy of MRI has been published elsewhere [9]. The SICUS waserformed after ingestion of a macrogol solution enabling to visu-lise and measure wall thickness and lumen diameter along themall bowel [15,16].

In order to optimise visualisation of the jejunum and ileum byCE, patients were given no more than 1 L of PEG 4000 oral solu-

ion, administered in 100–200 mL increments every 10 min in thearly morning of the examination after an overnight fast. Patientsere allowed to resume their usual activities and drink clear liquidsh and 3 h, respectively, after ingesting the capsule. The WCE used

n this study was the PillCam small bowel video capsule (Givenmaging, Israel) that measures 11 mm × 26 mm and weighs lesshan 4 g, with a recording system consisting of a data recorder and aorkstation equipped with image processing software. In patientsnable to swallow the capsule, the latter was released in the proxi-al duodenum with a paediatric video-gastroscope (Olympus PCF180), in which the capsule had been loaded using a foreign bodyoth Net (US Endoscopy, Mentor, OH). All patients underwent WCEithin one week from the completion of the upper and lowerI video-endoscopy. Imaging tools of the ileum (ultrasonography,RI, small bowel follow through) were performed few days beforeCE. Capsule retention was defined as failure of passage of the cap-

ule from the gastrointestinal tract for 2 or more weeks [10]. Thexamination was considered as incomplete if the capsule did noteach the caecum within 8 h [12].

The capsule images were independently interpreted by twoembers of the staff (S.O. and ME.R.), with a great training in GI

ndoscopy and unaware of the clinical history, previous inves-igations and diagnosis. The study was judged to be negative ifo abnormalities were seen and positive if clear abnormalities of

B1 = non stricturing, non penetrating 29 (65.9%)B3p = penetrating 15 (34.1%)

a At enrollment into the study, according to Montreal Classification [30].

the small bowel mucosa (i.e. ulcerations, erosions, polyps, vascularlesions, bleeding lesions) were observed. There was a 100% concor-dance between the observers in classifying the study as positive ornegative.

Features detected by WCE were considered as diagnostic ofactive CD if >3 diffuse small bowel ulcerations or multiple ulcer-ations were seen. Features of ≤3 ulcerations were consideredsuggestive but not diagnostic of small bowel CD. If no abnormalitiesor non specific findings (such as erythematous spots or mucosalbreaks) were seen the examination was considered as non spe-cific or normal [15]. White lesions within a crater with surroundingerythema were considered ulcers, whereas small superficial whitelesions, even with surrounding erythema, were considered ero-sions.

This was a prospective study and the primary end-point wasto compare the usefulness of WCE for assessing small bowel insuspected or established IBD in comparison with non endoscopicimaging tools.

Informed consent for all diagnostic procedures was obtainedby parents (or caregivers) and also by children. The latter wereinformed with an appropriate text reporting descriptive figures.The ethical committee of each hospital approved the diagnosticprocedures.

2.1. Statistical analysis

We performed comparisons between two procedures by usingthe Fisher exact test. Data were analysed using GraphPad InStat3.1 for Mac OSX; p ≤ .05 was considered statistically significant. Alltests were 2-tailed.

3. Results

The WCE procedure was well tolerated by all patients; no casesof capsule retention occurred. Eighteen patients (median age 7.0years; range: 4–12) were unable to swallow the capsule: the latterwas inserted through the videogastroscope using a foreign bodyRoth Net. Fig. 1 shows the diagnostic algorithm in patients under-going WCE.

Overall, colonoscopy with exploration of the terminal ileum (TI)had been performed in all 44 patients with CD: the TI was involvedin 33 (27 also with colonic lesions), in 9 the disease was localised atthe large bowel only, whereas it involved the gastroduodenal tractalone in 2. Table 1 reports the clinical characteristics and the diseaselocalisation of CD patients. CD lesions in the small bowel mucosa,

previously undetected, were revealed by WCE in 18 patients (41%)and by non endoscopic procedures (MRI and/or SICUS) in 8 (18.1%)(p < 0.01); in all patients with colonoscopic TI ulcerations, the lat-ter were also shown by WCE. All 18 CD patients with small bowelinvolvement exhibited clinical and/or laboratory data unexplained

222 G. Di Nardo et al. / Digestive and Liver Disease 43 (2011) 220–224

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ig. 1. Algorithm showing patient population investigated with the wireless capndoscopy; SICUS, small intestine contrast ultrasonography; MRI, magnetic resona

y features detected with conventional endoscopy that suggestedmildly active or quiescent disease: low serum albumine and

naemia in 10, severe abdominal pain with diarrhoea, fever andaematochezia in 14, high plasma levels of acute phase reactantsCRP, ESR, ferritine and fibrinogen) in 12.

Both WCE and non endoscopic procedures did not detect specificmall bowel lesions in all 29 patients with a previous diagnosis ofC. The latter was subsequently confirmed at a long term followp. In 10 patients WCE revealed non specific lesions such as areasf hyperaemia intermingled with granularity, both in small bowelreas close to the TI and in the latter: in all cases histology revealedmild mixed inflammatory infiltrate of the lamina propria withoutrypt distortion and epithelial changes.

Of 26 patients with a diagnosis of IBDU, small bowel lesionsiagnostic of CD were detected in 7 by non endoscopic proce-ures (26.9%) and in 16 by WCE (61.5%) (p < 0.05): the disease wase-classified as CD in them. The diagnosis of CD was then con-rmed by endoscopic and histological findings at the single-balloonnteroscopy performed not later than 2 months after WCE study.n 10 patients with no lesions at WCE the diagnosis of IBDU wasonfirmed.

Of 18 patients investigated because of recurrent haematocheziand clinical signs of GI disorders, small bowel lesions diagnos-ic of CD were seen by WCE in 9 (50%), but only in 4 by MRInd/or SICUS (22.2%) (p < 0.01): in all of them upper and lower GIndoscopy as well as histology had not revealed specific inflam-atory lesions. Of the remaining patients, WCE showed polyps

n 2, drug-related lesions in 3, nodular hyperplasia related toultiple food allergy in 3, vascular abnormalities in 1. The CD

iagnosis in this group of patients was subsequent confirmed byndoscopic and histological features as detected by single balloonnteroscopy.

In all investigated patients there were no features detected atRI or SICUS but not visualised by WCE. The exam was incomplete

n 5 patients (all with a previous diagnosis of CD): however it washought to be valuable because most of the small bowel was clearlyisualised.

. Discussion

Currently, in the management of IBD, WCE is thought to be ahird stage examination, useful to define the extent and the severity

endoscopy and the diagnostic outcome. SB, small bowel; WCE, wireless capsuleaging.

of already known CD, as well as for detecting small bowel lesions incases of suspected CD [6]. The WCE is also of value in subjects withobscure GI symptoms in whom traditional endoscopy and imagingtools are negative [18–20]. A large meta-analysis study has shownthat WCE has an overall diagnostic yield better than other nonendoscopic imaging techniques in managing patients with definiteor probable IBD [21].

Whereas previous reports have mainly highlighted the useful-ness of WCE in patients with obscure GI bleeding or undefinedintestinal disorders, less studies have been focused on IBD, only aminority of them including paediatric patients [22–26]. We inves-tigated paediatric subjects both with a previous diagnosis of IBDand with signs suggestive of IBD. Of the CD group, small bowellesions were disclosed by WCE in a significantly higher percent-age of patients than by non endoscopic imaging: these subjectswere characterised by clinical features and laboratory findingsunexplained by conventional endoscopy that had revealed featuresindicating a mildly active or quiescent disease. Of the non endo-scopic tools commonly used in the management of IBD, MRI andSICUS have recently been reported as reliable methods to docu-ment small bowel inflammation in CD, mainly if transmural damageoccurs [8,9,15]. It is conceivable that most small bowel lesions inour patients were superficial, thus more detectable through a directendoscopic inspection. However, prospective studies comparingWCE and non endoscopic tools in assessing small bowel involve-ment in IBD are warranted. Results in our patients with a previousCD diagnosis are in accordance with a statement from a recentinternational consensus that small bowel endoscopy in CD is nota routine procedure and should be performed in cases with unex-plained symptoms and inconclusive imaging and ileo-colonoscopy[6].

In a previous retrospective study on WCE in 28 IBD children, 4of 5 UC patients and 1 of 2 IBDU patients changed their diagnosisin CD, whereas in 13 of 21 CD a more extensive small bowel dis-ease than previously thought was revealed [27]. The use of WCE hasalso been reported in a group of 50 adult patients with known orsuspected IBD and no evidence of active disease on classical inves-

tigation: WCE revealed features diagnostic or suspected of CD in 20and 10, respectively; the examination was normal or nonspecific inthe remaining 20 [17].

We also investigated children with a previous diagnosis of UC:in none of them WCE revealed specific small bowel lesions. This

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G. Di Nardo et al. / Digestive a

utlines the appropriateness of the diagnostic criteria adopted inur study [3,4]. Indeed, the UC diagnosis was subsequently con-rmed in all subjects at a long term follow up. It is widely agreedhat the diagnosis of UC does not require small bowel endoscopyith WCE; however, these patients had been referred for small

owel endoscopic evaluation due to some diagnostic uncertain-ies related either to the aspect and the topography of colonicndoscopic lesions or to the type and distribution of the inflam-atory infiltrate at histology. Interestingly, in 10 UC patients areas

f granularity and hyperaemia were observed in the TI and in moreroximal areas: histology revealed only a mild mixed inflammatory

nfiltrate of the lamina propria and no epithelial or crypt changed,hus excluding CD.

Interestingly, 26 subjects had been diagnosed as IBDU, due toack of endoscopic and histological criteria discriminating betweenD and UC. Of these patients, 16 were reclassified as CD because ofeculiar small bowel lesions at WCE; imaging tools detected ileal

nflammatory lesions suggesting CD in only 7 of them. In a previousulticenter study in 30 adults with IBDU and negative serology,CE was useful for categorising them whereas a normal small

owel imaging could not exclude a diagnosis of CD [22]. Interest-ngly, a previous report in adults with UC or IBDU who underwent

CE has shown that small bowel lesions consistent with CD coulde detected in almost 16% of investigated subjects [28]. The unclas-ified forms of IBD are peculiar of the paediatric age since IBD inhildhood not uncommonly exhibits clinical, endoscopic and histo-ogical phenotypes that do not allow a clear differentiation betweenC and CD, with consequent uncertainty in choosing therapeuticptions and in the long term prognosis [3]. In paediatric series, therevalence of IBDU ranges from 5% to 30%, suggesting a variation

n classification criteria [3].In 18 patients evaluated for haematochezia and signs of chronic

nteropathy, WCE revealed a CD in 9, whereas other entities wereetected in the remaining patients. These data confirm the diag-ostic value of WCE in subjects with undefined GI disorders [20].reviously, in children with obscure small bowel disorders, WCEetected lesions consistent with CD in almost 50% of the patients,ith a sensitivity higher than imaging tools [29].

Our study confirms that WCE is well tolerated and safe in paedi-tric patients. We did not observe any capsule retention, whereasata from previous paediatric studies indicate a WCE retention rateanging from 2% to 5% [11], that is comparable with data from adultatients [24]. The absence of capsule retention in our populationan likely be attributed to the strong criteria to exclude patientsrom WCE. It is worth noting that all subjects recruited for WCEnderwent a preliminary imaging tool of the small bowel to detecttrictures.

In conclusion, WCE is a very useful approach to children pre-enting with symptoms suggesting IBD or with an established IBD.t is of particular helpful in identifying small bowel ulcerations inhildren with CD exhibiting clinical and laboratory features unex-lained by conventional GI endoscopy and imaging tools. It is alsoritical in reclassifying children with IBDU. While it is widely agreedhat WCE in IBD should be recommended as a third stage examina-ion after conventional upper and lower GI endoscopy, it remainsnsettled how this examination will influence the management of

BD and how it should be used in conjunction with other investiga-ive modalities (i.e. MRI, ultrasound). Finally, one important issueill be how to integrate capsule endoscopy with balloon assisted

nteroscopy, a novel technique that allows both endoscopic explo-ation of the small bowel and histological assessment as well as

herapeutic interventions.

onflict of interest statementone declared. Dr. Laura Stronati, Research Assistant at ENEA,

s performing several research projects on paediatric IBD at

[

r Disease 43 (2011) 220–224 223

the Department of Pediatrics of the Sapienza University inRome.

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