Jjy 114

Journal of Crohn's and Colitis, 2018, 273–290
doi:10.1093/ecco-jcc/jjy114
Advance Access publication August 24, 2018
ECCO Guideline/Consensus Paper
ECCO Guideline/Consensus Paper
ECCO-ESGAR Guideline for Diagnostic

Assessment in IBD Part 2: IBD scores and
general principles and technical aspects
Downloaded from https://academic.oup.com/ecco-jcc/article/13/3/273/5078200 by guest on 15 September 2023

Andreas Sturm,a Christian Maaser,b Emma Calabrese,c Vito Annese,d
Gionata Fiorino,e Torsten Kucharzik,f Stephan R. Vavricka,g
Bram Verstockt,h, Patrick van Rheenen,i Damian Tolan,j Stuart A. Taylor,k
Jordi Rimola,l Florian Rieder,m Jimmy K. Limdi,n Andrea Laghi,o
Eduards Krustiņš,p Paulo G. Kotze,q Uri Kopylov,r Konstantinos Katsanos,s
Steve Halligan,t Hannah Gordon,u Yago González Lama,v Pierre Ellul,w
Rami Eliakim,r Fabiana Castiglione,x Johan Burisch,y,
Paula Borralho Nunes,z, Dominik Bettenworth,aa Daniel C. Baumgart,bb
Jaap Stoker,cc on behalf of the European Crohn’s and Colitis
Organisation [ECCO] and the European Society of Gastrointestinal and
Abdominal Radiology [ESGAR]
a
Department of Gastroenterology, DRK Kliniken Berlin I Westend, Berlin, Germany bOutpatients Department of
Gastroenterology, Hospital Lüneburg, Lüneburg, Germany cDepartment of Systems Medicine, University of Rome,
Tor Vergata, Italy dDepartment of Gastroenterology, Valiant Clinic & American Hospital, Dubai, UAE eDepartment
of Gastroenterology, Humanitas Clinical and Research Institute, Milan, Italy fDepartment of Internal Medicine and
Gastroenterology, Hospital Lüneburg, Lüneburg, Germany gGastroenterology and Hepatology Center, Zurich, Switzerland
h
Department of Gastroenterology and Hepatology, University Hospitals Leuven and CHROMETA - Translational
Research in Gastrointestinal Disorders, KU Leuven, Leuven, Belgium iDepartment of Paediatric Gastroenterology,
Hepatology and Nutrition, University Medical Center Groningen, Groningen, The Netherlands jClinical Radiology,
St James’s University Hospital, Leeds, UK kCentre for Medical Imaging, University College London, London, UK lDepartment of
Radiology, Hospital Clínic Barcelona, Barcelona, Spain mDepartment of Gastroenterology, Hepatology & Nutrition, Digestive
Diseases and Surgery Institute, Cleveland Clinic, Cleveland, OH, USA nDepartment of Gastroenterology, Pennine Acute
Hospitals NHS Trust, Manchester; Manchester Academic Health Sciences Centre, University of Manchester, Manchester,
UK oDepartment of Clinical and Surgical Translational Medicine, Sapienza - University of Rome, Rome, Italy pDepartment of of
Gastroenterology, Hepatology and Nutrition, Pauls Stradins Clinical University Hospital, Riga, Latvia qColorectal Surgery Unit,
Catholic University of Paraná PUCPR, Curitiba, Brazil rDepartment of Gastroenterology, Sheba Medical Center, Sackler School of
Medicine, Tel Aviv, Israel sDepartment of Gastroenterology and Hepatology, University and Medical School of Ioannina, Ioannina,
Greece tCentre for Medical Imaging, University College London, London, UK uSection of Gastroenterology & Hepatology, Royal
London Hospital, London, UK vDepartment of Gastroenterology, University Hospital Puerta De Hierro, Majadahonda Madrid,
Spain wDepartment of Medicine, Mater Dei Hospital, Msida, Malta xDepartment of Clinical Medicine and Surgery, “Federico
II” University of Naples, Naples, Italy yDepartment of Gastroenterology, North Zealand University Hospital; Center for Clinical
Research and Prevention, Bispebjerg and Frederiksberg Hospital, Frederiksberg, Denmark zDepartment of Anatomic Pathology,
Hospital Cuf Descobertas; Faculdade de Medicina da Universidade de Lisboa, Lisbon, Portugal aaDepartment of Medicine B,
Gastroenterology and Hepatology, University Hospital Münster, Münster, Germany bbDivision of Gastroenterology, University of
Alberta, Edmonton, AB, Canada ccDepartment of Radiology and Nuclear Medicine, Academic Medical Center AMC, University
of Amsterdam, Amsterdam, The Netherlands
Corresponding author: Andreas Sturm, Head, Department of Gastroenterology, DRK Kliniken Berlin I Westend, Berlin,
Germany. Email: [email protected]
Copyright © 2018 European Crohn’s and Colitis Organisation (ECCO). Published by Oxford University Press. All rights reserved.
273
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274 A. Sturm et al.
Chapter 4: Scores for Inflammatory Bowel and 19 points and include nocturnal bowel movements and faecal
Disease urgency, which affect patient quality of life [QoL].3 An SCCAI score
<2 indicates clinical remission, and a decrease of >1.5 points from
4.1 Clinical and endoscopic scoring systems in baseline correlates with patient-defined significant improvement.5
inflammatory bowel disease The Mayo Clinic Score [or Index] [Partial Mayo Clinic Index and endo-
scopic subscore] and Ulcerative Colitis Disease Activity Index [UCDAI] are
Statement 4.1. ECCO-ESGAR Diagnostics GL [2018] a composite assessment of clinical symptoms [stool frequency and rectal
bleeding] and endoscopic severity [Table 2].6,7 Whereas these indexes are
Clinical indexes are useful for standardising disease not validated, the Mayo Clinic Score is easy to apply and has been used for
activity. However, despite widespread use, no score has assessing therapeutic endpoints in adult clinical trials.8 Clinical improve-
been validated in clinical practice [EL5] ment is defined as the reduction of baseline scores by ≥3 points and clinical
remission as an overall score ≤2 [and no individual subscore >1] or UCDAI
≤1.6–8 A Partial Mayo Score [PMS] <1 indicates remission.1 The PMS has
4.1.1 Clinical and endoscopic scoring systems in ulcerative
been shown to correlate well with the full scoring system.9,10
colitis
The Truelove and Witts Severity Index was described in 1955.11 Its

There are several scoring systems presently available to classify dis-
elements reflect levels of systemic toxicity and provide objective criteria
ease severity in ulcerative colitis [UC] within the multiple domains of
for assessment of acute severe colitis, need for hospitalisation, and cor-
disease activity, which aid objective assessment of disease and guide ticosteroid therapy2 [Table 3]. The Lichtiger Index is a modification of
therapeutic and monitoring strategies.1,2 Although somewhat limited the Truelove and Witts Index and was used in the cyclosporine trial for
by subjective definitions, their strength lies in the potential to moni- steroid-refractory UC.12
tor patient progress over time.1 The Pouchitis Disease Activity Index was developed to provide a stand-
The Simple Colitis Clinical Activity Index [SCCAI]2,3 [Table 1] ard definition of pouchitis, including histological subscores.13 A Pouchitis
and the Paediatric Ulcerative Colitis Activity Index [PUCAI]4 Disease Activity Index score ≥7 indicates acute pouchitis, and remission is
[Supplementary Table 1, available as Supplementary data at ECCO- defined as a score ≤2 including endoscopic subscores ≤1 [Supplementary
JCC online] are reliable and responsive scores with clear definitions Table 2, available as Supplementary data at ECCO-JCC online].
for clinical response and remission. SCCAI scores range between 0
Statement 4.1.1. ECCO-ESGAR Diagnostics GL [2018]

Table 1. Clinical scoring system for the Simple Clinical Colitis
Activity Index.3 Endoscopic scores in ulcerative colitis [UC] should be
used for standardisation of care [EL5]. The Mayo Clinic
Symptom Score
Subscore [MCS] is accepted and extensively used, and
Bowel frequency [day] the UC Endoscopic Index of Severity [UCEIS] and the UC
1–3 0 Colonoscopic Index of Severity [UCCIS] are formally vali-
4–6 1 dated [EL2]. The Pouchitis Disease Activity Index provides
7–9 2 a standard definition of pouchitis [EL4]
>9 3
Bowel frequency [night]
1–3 1 Endoscopic scoring systems in ulcerative colitis
4–6 2 A plethora of UC endoscopic scoring systems have been developed
Urgency of defaecation over the years.1,2,14,15 These systems are also increasingly used in clini-
Hurry 1
cal practice to guide treatment decisions with the aim of achieving
Immediately 2
mucosal healing [MH] [Table 4].16–19
Incontinence 3
The first attempt to classify endoscopic UC severity was performed
Blood in stool
by Truelove and Witts.11 Mucosal appearance is classified into the fol-
Trace 1
Occasionally frank 2 lowing three categories: [1] normal or near normal; [2] improved; or
Usually frank 3 [3] no change or worse. This classification lacks well-defined endoscopic
General well-being descriptors.
Very well 0 Baron et al. subsequently evaluated interobserver agreement
Slightly below par 1 using rigid sigmoidoscopy.20 The degree of disease activity is based
Poor 2 on a 4-point scale [0–3] mainly according to bleeding severity. The
Very poor 3 presence of ulceration is not taken into account. A Baron Score ≤1
Terrible 4 [0, normal mucosa; 1, abnormal mucosa but non-haemorrhagic] is
Extracolonic features [joints, eyes, 1 per manifestation defined as endoscopic remission. The Baron Score has not been for-
mouth, skin, perianal]
mally validated. Feagan et al. described the Modified Baron Score
Table 2. Mayo score for ulcerative colitis.6
Mayo Score [Index] 0 1 2 3
Stool frequency Normal 1–2/day >normal 3–4/day >normal 5/day >normal

Rectal bleeding None Streaks Obvious Mostly blood
Mucosa Normal Mild friability Moderate friability Spontaneous bleeding
Physician’s global assessment Normal Mild Moderate Severe
Guideline for Diagnostic Assessment in IBD 275
[MBS] in a placebo-controlled trial.21,22 Endoscopic activity is cat- The Rachmilewitz Endoscopic Index24 was developed during a
egorised according to a 5-point scale [0–4]. controlled trial. The index includes the following four variables: [1]
The Powell-Tuck Index [also known as St Mark’s Index]23 grades vascular pattern; [2] granularity; [3] mucosal damage [mucus, fibrin,
the severity of inflammation using a 3-point scale [0–2], focusing exudate, erosions, ulcers]; and [4] bleeding. The cut-off for endo-
on mucosal bleeding as the predominant variable [Supplementary scopic remission is ≤4 points.
Table 3, available as Supplementary data at ECCO-JCC online]. The endoscopic component of the Mayo Clinic Score [MCS]6
The Sutherland Index [UC Disease Activity Index, UCDAI]7 was assesses inflammation based on a 4-point scale [0–3] as follows: [0]
developed during a placebo-controlled trial. Mucosal appearance normal; [1] erythema; decreased vascular pattern, mild friability; [2]
is described on a 4-point scale [0–3] evaluating the following three marked erythema, absent vascular pattern, friability, erosions; and [3]
endoscopic findings: [1] friability; [2] exudation; and [3] spontane- ulceration, spontaneous bleeding. The MCS is most commonly used in
ous haemorrhage. clinical trials.8 Clinical response is defined as reduction from baseline
MCS by ≥3 points and a decrease of 30% from the baseline score
with a decrease of at least 1 point on the rectal bleeding subscale or an
Table 3. Disease activity in ulcerative colitis, adapted from Truelove
absolute rectal bleeding score of 0 or 1.18 Clinical remission is defined
and Witts.11

as an MCS ≤2 and no individual subscore >1. MH has been defined as
Mild Moderate‘between Severe a subscore of 0 to 1.18 Interobserver agreement can vary markedly.18
mild and severe’ For the MCS, the most inflamed part determines the overall score.
The Modified Mayo Score [MMES] divides the colon into five
Bloody stools/day <4 4–6 ≥6 and
segments and the score for each segment is added to give a modified
Pulse <90 bpm ≤90 bpm >90 bpm or
score,25 which is multiplied by the maximal extent of inflammation
Temperature <37.5°C ≤37.8°C >37.8°C or
Haemoglobin >11.5 g/dL ≥10.5 g/dL <10.5 g/dL or
and divided by the number of segments with active inflammation to
ESR <20 mm/hr ≤30 mm/h >30 mm/h or give the final MMES.
CRP Normal ≤30 mg/L >30 mg/L The Ulcerative Colitis Endoscopic Index of Severity [UCEIS] is a val-
idated endoscopic index that was developed due to wide interobserver
ESR, erythrocyte sedimentation rate; CRP, C-reactive protein; bpm, beats variation [Supplementary Table 4, available as Supplementary data at
per min. ECCO-JCC online]. UCEIS grades three endoscopic findings in the
Table 4. Comparison of endoscopic scoring indexes in ulcerative colitis. Adapted from Annese V et al.14
Score Endoscopic Strengths Weaknesses Proposed

variables remission
score
Truelove and Witts11 No endoscopic descriptor definitions ----- ----- -----

Sigmoidoscopic assessment
Baron Score[20] Vascular pattern, friability, bleeding Easy to calculate Does not evaluate ulcers 0–1
Subjective interpretation of
friability and bleeding
Poor interobserver agreement
Powell-Tuck Index [St Mark’s Bleeding [non-haemorrhagic vs ------- Only evaluates bleeding Not defined
Index]23 haemorrhagic mucosa] Subjective interpretation
Sutherland Index7 Friability, exudation, spontaneous ------- Does not evaluate ulcers 0
haemorrhage Not accurate in discriminating
between mild to moderate
friability
Mayo Endoscopic Subscore6 Erythema, vascular pattern, friability, Easy to calculate Not accurate in discriminating 0–1
erosions, ulcers, bleeding Widely used in clinical trials between mild to moderate
friability
Rachmilewitz Index24 Vascular pattern, granularity, mucosal Easy to calculate Subjective interpretation of 0–4
damage [mucus, fibrin, exudate, mucosal damage and bleeding
erosions, ulcers, bleeding]
Modified Baron Score21 Vascular pattern, granularity, Easy to calculate No discrimination between 0
hyperaemia, friability, ulceration, Used in clinical trials superficial and deep ulceration
bleeding
UCEIS26 Vascular pattern, bleeding, erosions, Accurate for the assessment of Low agreement for normal Validated
ulcers disease severity appearance of the mucosa
Developed following rigorous
methodology
UCCIS33 Vascular pattern, granularity, Accurate, easy scoring as Single-centre development, high Validated
ulceration, bleeding, friability based on only four different expertise required
parameters Broader validation needed
Developed and validated
following rigorous
methodology
Covers the entire colon
276 A. Sturm et al.
most severely affected part of the colon, namely vascular pattern, bleed- primarily on assessment of patient symptoms with scattered use of
ing, and erosions and ulcers. Initially developed as an 11-point score, objective parameters. It correlates poorly with biological evidence of
UCEIS was simplified to an 8-point tool scoring erosions and ulcers active disease, including endoscopic assessments and C-reactive pro-
[0–2], vascular pattern [0–2], and bleeding [1–4], with a satisfactory tein levels. Furthermore, the HBI has the limitation of overestimating
interobserver agreement [κ 0.5].26 Friability has been excluded from this disease activity in the setting of concomitant functional bowel symp-
index. The extent of disease is not relevant in this score. Although this toms while underestimating disease in a subset of patients who may
score appears more responsive to change following treatment than the have subclinical stricturing or penetrating luminal complications.40
MCS, UCEIS is still not extensively used due to lack of familiarity.27,28 Patients with CD who have an HBI score ≤3 are very likely to be in
The remission target is a score ≤1. The UCEIS shows strong correlation remission according to the CDAI. Patients with a score of 8 to 9 or
with patient-reported outcomes.29–31 Both UCEIS and MCS have dem- higher are considered to have severe disease.
onstrated a high degree of correlation for UC [Supplementary Table 4, The Crohn’s Disease Digestive Damage Score [the Lémann score]
available as Supplementary data at ECCO-JCC online].32 [Supplementary Table 5, available as Supplementary data at ECCO-
The Ulcerative Colitis Colonoscopic Index of Severity [UCCIS] JCC online] considers damage location, severity, extent, progression,
has recently been prospectively validated.33 The UCCIS includes and reversibility as measured by diagnostic imaging modalities and

the following six variables: [1] vascular pattern; [2] granularity; [3] history of surgical resection [see section 4.3]. The Lémann score is
ulceration; [4] bleeding and friability; [5] grading of segmental and expected to represent a patient’s disease course and to assess the
global assessment of endoscopic severity with a predefined 4-point effect of various medical therapies.41
scale; and [6] global assessment of endoscopic severity on a 10-cm Irvine developed the PDAI.42 Each of the five elements identified
visual analogue scale [VAS] scale. The UCCIS has good-to-excellent was graded on a 5-point Likert scale. Correlation between the PDAI
interobserver agreement, but a cut-off level for endoscopic response [maximum 20 points] and the physician and patient global assess-
and remission is currently lacking. ment is good. A more recent scoring system proposed by Pikarsky
et al.43 attempts to predict the outcome following surgical interven-
4.1.2 Clinical and endoscopic scoring systems in Crohn’s tion in patients with perianal CD. However, the lack of a validated
disease clinical outcome measure in CD seems to be most obvious in peri-
Numerous tools are available for assessing disease activity in Crohn’s anal Crohn’s disease.
disease [CD] patients.34 The most commonly used clinical activity indexes
are the Harvey-Bradshaw Index [HBI], the Crohn’s Disease Activity Statement 4.1.2. ECCO-ESGAR Diagnostics GL [2018]
Index [CDAI], and the Perianal Disease Activity Index [PDAI] [Table 5].35
Measuring clinical activity is important but no longer sufficient, and both The Crohn’s Disease Endoscopic Index Of Severity [CDEIS]
CDAI and HBI are limited by subjective interpretation [Table 5].36,37 and the Simple Endoscopic Score for Crohn’s disease
The CDAI36 was developed by Best et al. in 1976. The CDAI con- [SES-CD] are validated and reproducible scoring systems
sists of eight factors, each summed after adjustment with a weighting measuring luminal endoscopic activity [EL2]. There is no
factor. Remission is defined as CDAI <150, and a value >450 repre- validated definition of or score for mucosal healing [MH]
sents severe disease. Most major research studies on medications in in Crohn’s disease [CD]. The severity of postoperative CD
CD define response as decrease in CDAI of >70 points; however, in recurrence in the neo-terminal ileum should be stratified
some studies a drop of 100 points is required for response.38 The
using the Rutgeerts score [EL2]
CDAI system has some limitations. These include: interobserver vari-
ability; relevant weight for scores of ‘general well-being’ and ‘intensity
of abdominal pain’ items, which are subjective and reflect patients’ There are currently three endoscopic scoring systems for CD, namely
perceptions of their disease; and the calculation of the CDAI is based the Crohn’s Disease Endoscopic Index of Severity [CDEIS],44 the
on a diary completed by the patient for 7 days before evaluation. Simple Endoscopic Score for Crohn’s Disease [SES-CD],45 and the
This requirement precludes the use of the CDAI in everyday practice. Rutgeerts endoscopic grading scale for postoperative recurrence
Furthermore, the CDAI is not accurate in patients with fistulising or [Supplementary Tables 6 and 6a, available as Supplementary data at
stenotic behaviour and it is not useful in patients with previous exten- ECCO-JCC online].14,46
sive ileocolonic resections or stoma. Currently, however, the CDAI is The CDEIS scores CD activity [from 0 to 44] in five bowel seg-
the most frequently used index for clinical trials.39 However, explora- ments [terminal ileum, right colon, transverse, left colon and sig-
tory and until now unvalidated patient-related outcomes scores [PRO] moid, rectum] and considers specific mucosal lesions [such as ulcers
are asked by the authorities. and stenosis] and extent of disease.44,47 The CDEIS is complicated to
The Harvey-Bradshaw Index [HBI] was developed in 1980 as a use, and requires training and experience in estimating the extent of
simpler version of CDAI. The HBI consists of only clinical param- ulcerated or diseased mucosal surfaces and expertise in distinguish-
eters; the first three items are scored from the previous day. These ing deep from superficial ulcerations. The CDEIS is also time-con-
items include general well-being, abdominal pain, number of liquid suming. It has consequently not become routine in clinical practice
stools per day, abdominal mass, and complications. The HBI relies and is used mainly in clinical trials.
Table 5. Non-endoscopic Crohn’s disease activity indexes in clinical practice.
Activity index Acronym Range and [remission] values Comments for clinical practice
Crohn’s Disease Activity Index3 CDAI 0–600 [<150] Calculation based on a 7-day diary;
difficulty in assessment of perianal disease activity
Harvey - Bradshaw Index37 HBI 0–50 [≤4] Simple and more practical
Perianal Crohn’s Disease Activity Index42 PDAI 0–19 Problematic fistula severity assessment
The SES-CD was developed to simplify the CDEIS. The SES-CD lumen [cryptitis and crypt abscesses] and ultimately by erosions and
includes four variables, each considered in five bowel segments [ulcer ulcers.52,53 Histologically, MH is characterised by partial resolution of
size, extent of ulcerated surface, extent of affected surface, and sten- the crypt architectural distortion and of the inflammatory infiltrate,
osis]. Scores range from 0 to 6. The SES-CD correlates highly with although the mucosa may still show some features of sustained dam-
CDEIS. Defining SES-CD cut-offs must take into account endoscop- age, such as a decreased crypt density with branching and shortening
ically meaningful changes.45 However, as the SES-CD do not define of the crypts.56 Ultimately basal plasmacytosis decreases, resulting in
MH, this score is currently not much used in clinical practice. normal cellularity, and remission may result in a complete normalisa-
Rutgeerts et al. developed a score for grading lesions in the tion of the mucosa in approximately 24% of cases.57,58 According to
neo-terminal ileum and anastomosis.46 This score is considered the ECCO-ESP, active inflammation is usually absent in quiescent disease.
gold standard for establishing the prognosis in cases of postopera- There is no consensus on the acceptable number of eosinophils or
tive recurrence; scores of 3 and 4 are validated cut-offs for predict- lymphoid aggregates, nor on residual basal plasmacytosis. Although
ing clinical relapse. The Modified Rutgeerts Score refers to a more endoscopic MH is associated with better outcomes in IBD, less is
refined definition of grade i2, which includes lesions confined to the known about the significance of achieving histological remission.59
ileocolonic anastomosis [i2a] or moderate lesions on the neo-termi- However, recent data suggest that histological remission, defined as

nal ileum [i2b]. minimal residual microscopic disease and absence of epithelial dam-
age, is highly reproducible in multiple UC cohorts. Histological remit-
4.1.3 Capsule endoscopy scores ters are also more likely to achieve endoscopic and clinical response
The Capsule Endoscopy CD Activity Index [CECDAI or Niv Score] or remission and to remain symptom-free at 12 months after a course
was validated in a multicentre prospective study of patients with of corticosteroids. Reduced hospitalisation or colectomy rates60–62
isolated small bowel CD [Supplementary Table 7, available as have also been observed when histological remission is achieved.
Supplementary data at ECCO-JCC online].48 The CECDAI evalu- There is a need for a clear definition of ‘complete’ histological
ates the following three endoscopic parameters: inflammation MH or ‘histological remission’, and to have a reproducible, stand-
[A, 0 to 5 points], extent of disease [B, 0 to 3 points], and stric- ardised, and validated histological scoring system for biopsy evalu-
tures [C, 0 to 3 points], for both the proximal and the distal seg- ation. A histological endpoint is likely to be more relevant in UC
ments of the small bowel, based on the transit time of the capsule than CD, as the diffuse mucosal inflammation in UC is less subject to
[Supplementary Table 7]. biopsy bias than the patchy transmural inflammation of CD.
The Lewis Score assesses villous oedema, ulcers, and stenosis,
and classifies CD activity from mild to severe.49 The small bowel is 4.2.2 Histological scoring systems
first divided into three equal parts [tertiles] based on capsule transit A unique standard system for grading histological activity does not
time from the first duodenal image to the first caecal image. For each exist.63–65 Numerous methods of classification of histological activ-
tertile, a subscore is determined based on the extent and distribution ity have been proposed and some are widely used, with only a few
of oedema and on the number, size, and distribution of ulcers. The validated and proven to be reproducible [Supplementary Tables 9
Lewis Score is the sum of the worst affected tertile plus the stenosis and 10, available as Supplementary data at ECCO-JCC online].
score [Supplementary Table 8, available as Supplementary data at Most the published systems were developed for UC [Supplementary
ECCO-JCC online]. These small bowel capsule endoscopy scoring Table 9]. Bryant et al.59 published the results of a systematic biblio-
systems have been developed only recently, and their usefulness in graphic search that retrieved 22 different histological scoring sys-
clinical trials and clinical practice remains to be seen.47 tems for IBD. The most widely used in UC are the Riley Index66
and the Geboes67 Index. Some [such as the Riley Index] are difficult
4.2 Histological scoring systems in IBD
to reproduce, as the criteria for separating grades are not provided.
The Geboes Index is subjective for chronic inflammation [grade 1]
Statement 4.2. ECCO-ESGAR Diagnostics GL [2018] and eosinophils and neutrophils in the lamina propria [grade 2], but
A validated histological score should be used in clinical acute inflammation is well defined. The Geboes Index also includes
practice for UC [EL3]. There are no scores validated in clini- the requisites to grade architecture and can be modified to include
cal practice for CD [EL5] the evaluation of basal plasmacytosis. The recently published Nancy
Score,55 a three-descriptor histological index, has been validated for
use in clinical practice and clinical trials. The relationship between
The histological examination of endoscopic biopsies is not only the Nancy Score and Geboes Index was assessed with good respon-
a crucial element in the diagnostic workup but also in the evalu- siveness and correlation between them.67 Mosli et al. recently devel-
ation of therapeutic effect and in identification of dysplasia.2,50,51 oped an alternative instrument using some component items of the
The European Society of Pathology [ESP] and the European Geboes Index [Supplementary Table 9].68
Crohn’s and Colitis Organisation [ECCO] published a consensus Few scores were designed specifically for CD [Supplementary
document.52,53 Since the publication of these guidelines, significant Table 10, available as Supplementary data at ECCO-JCC online].
recent literature on histological healing and new histological scor- The Colonic and Ileal Global Histologic Disease Activity Score
ing systems have added to our understanding of the assessment [CGHAS or IGHAS] is probably the most widely used. This system
of disease activity, influencing the paradigms around grading and is subjective and has not been validated, and its role is currently
assessment of disease activity.54,55 undefined [Supplementary Table 10].
4.2.1 Histological remission in IBD 4.2.3 Practice points and future directions
In UC, histological remission should be defined as evidence of There is a clear need for a standard definition of histological MH and
normalisation of the bowel mucosa. Active disease is defined by for a standard and fully validated system of histological disease activ-
the presence of neutrophils within the crypt epithelium and crypt ity. Histology may be more effective in predicting clinical relapses or
278 A. Sturm et al.
in evaluating benefit from therapy.36 Meanwhile, pathologists should Comparative studies using ileocolonoscopy as the reference
use a simple and validated scoring system to complement endoscopic standard have validated both indexes.77,78 Reproducibility is criti-
scores. At present, the Nancy Score and Robarts histopathology [ref- cal to be considered as a useful instrument in practice. Specifically,
erenced in Mosli et al.68] are fully validated; the Geboes Index is only moderate-to-good degrees of interobserver agreement [0.42–0.69]
partially [not formally] validated but is widely used.68 among expert readers has been reported.77
A recent index very similar to MaRIA but using diffusion-
4.3 Cross-sectional imaging scoring systems in IBD weighted imaging [DWI] sequence instead of contrast enhancement
has been recently developed. This index is called the DWI-MaRIA
Statement 4.3. ECCO-ESGAR Diagnostics GL [2018] score or Clermont Score.79 To derive and validate the DWI-MaRIA
score, the same MR enterography [MaRIA] was considered as
Magnetic resonance [MR] enterography-based indexes the reference standard.80 The correlation between the MaRIA and
have high accuracy for assessing luminal CD activity and Clermont scores in the terminal ileum was almost perfect [r = 0.99]
can be used in clinical trials for measuring activity and but was significantly lower in the colon.81
response to pharmacological interventions [EL3]. There The Sailer Index was developed specifically for assessing postop-

are no validated scores for grading luminal activity based erative recurrence at the anastomotic site using MR enteroclysis.82,83
on ultrasound and computed enterography. Scoring of The most frequently used MRI index for perianal disease is the
perianal fistula activity by MR imaging in CD allows evalu- Van Assche Index.84 This score combines both the anatomical and
ation of disease severity and changes after therapy [EL3] complexity of fistula characteristics together with MRI findings
linked to the inflammation observed. Changes in the Van Assche
Cross-sectional imaging has an established role in clinical practice Index have good correlation with clinical response to treatment.84–86
for evaluation of the small and large bowel in patients with CD.69 This index has only been partially validated.87,88 However, certain
Assessments based on cross-sectional imaging may have use in clini- aspects of the index need to be elucidated further, such as the respon-
cal trials, with the added potential for validated indexes as surro- siveness of each individual item of the index and the definition of a
gates for therapeutic response. clinically relevant change in score.89
4.3.1 Cross-sectional index for luminal Crohn’s disease 4.3.2 Bowel damage index
There are no formally validated indexes on luminal activity based on The real potential for acute and chronic inflammation to cause bowel
ultrasonography or CT enterography. Among the different indexes destruction through fibrosis and penetrating disease led the develop-
published based on MR enterography, only a few have been derived ment of scoring systems for bowel damage.90 The Lémann Index was
using valid external reference standards [i.e. endoscopy or histology] designed to measure damage severity in all segments of the digestive
and use descriptors identified in multivariate analyses as independent tract, based on the assessment of stricturing and penetrating lesions
predictors for detecting activity and severity [Supplementary Table 1].70 using MR or CT and endoscopy together with previous surgery
The Magnetic Resonance Index of Activity [MaRIA] is a composite [Supplementary Table 3]. After an initial study,91 further studies dem-
index that takes into account bowel wall thickness, quantifies bowel onstrated that up to 60% of patients had a reduction in score 1 year
enhancement after gadolinium injection, and identifies ulceration and after starting anti-tumour necrosis factor [TNF] therapy.92–94
bowel oedema [Supplementary Table 2]. A subscore is calculated for In conclusion, there are different available indexes for grading
five colonic segments and for the terminal ileum. The global score is luminal disease using MR enterography. MaRIA111–112 is the best-
computed as the sum total of the subscores. The MaRIA score has characterised among these indexes. For perianal disease, there is
good correlation with CDEIS [r = 0.83].71,72 A MaRIA subscore of ≥7 need for an improved validated index for measuring response which
is indicative of bowel segments with active CD, and a subscore of ≥11 overcomes the current limitations.95,96
units identifies segments with severe activity [ulcers at endoscopy].
In a study by Takenaka et al., single-balloon enteroscopy was 4.4 Quality of life scoring systems for IBD
compared with MR enterography in patients with ileal CD.73 The
MaRIA score closely correlated with the SES-CD in the small bowel Statement 4.4. ECCO-ESGAR Diagnostics GL [2018]
[r = 0.808; p < 0.001]. A MaRIA score of ≥11 had high sensitivity,
specificity, and diagnostic accuracy for ulcerative lesions [sensitivity, The Inflammatory Bowel Diseases Questionnaire [IBDQ] is
78.3%; specificity, 98.0%]. Similarly, a MaRIA score of ≥7 had high considered the gold standard for use in clinical trials, but
sensitivity, specificity, and diagnostic accuracy for all mucosal lesions is lengthy and thus impractical in clinical practice [EL3].
[sensitivity, 87.0%; specificity, 86.0%]. At present, there is insufficient evidence to recommend a
The main limitation of the MaRIA index is that it was developed specific quality of life [QoL] score in clinical practice [EL5]
using both oral contrast and active colonic distension with water
enema. It is still uncertain if diagnostic accuracy will remain simi- Due to the wider appreciation that the nature of IBD often has a
lar without colonic distension.71 MaRIA showed high accuracy for negative impact on patients’ lives, emphasis on health-related qual-
detecting ulcer healing [accuracy 0.9] and MH [accuracy 0.83] in ity of life [HRQoL] and its assessment are integral to the holistic
CD patients following medical therapeutic intervention.74,75 care of patients with IBD.97,98 QoL is now a key measure in clinical
The Acute Inflammation Score [AIS] is another MR enterography trials in IBD.99 This corresponds to the WHO statement that ‘health
index and is a composite of two descriptors [mural thickness and mural is not merely an absence of disease’ but rather ‘complete physical,
T2 signal] that are evaluated in a semiquantitative fashion. A cut-off of mental and social well-being’,200 which underpins the importance of
4.1 units defines the presence of active disease with an area under the improving HRQoL as a treatment objective.201
curve [AUC] of 0.77, and demonstrated a moderate degree of correla- HRQoL in IBD may be an indirect indicator of disease activity202,203
tion with histopathological inflammation [Kendall’s tau = 0.40].76 and an outcome measure when assessing the efficacy of treatment.
There is reasonable expectation that effective treatment should gastrointestinal endoscopy, patient experience should be rou-
improve QoL.204 tinely measured and its improvement is crucial for acceptance.129
However, QoL is just one report from patients1 in a continuum with Colonoscopy is an essential tool for diagnosing and monitoring IBD;
general QoL measures at one end,205 disease [IBD]-specific HRQoL biopsy and culture sampling are often needed. Although research on
measurements206 in the centre, and instruments that measure specific the development of different non-invasive surrogates is under way,
variables such as continence,207 sexual dysfunction,208 food-related current therapeutic goals include endoscopically assessed mucosal
QoL,209 fatigue,210 and disability211 at the other end [Supplementary healing [MH]. IBD patients undergo endoscopic procedures [mostly
Table 13, available as Supplementary data at ECCO-JCC online]. for surveillance] more often than the general population.130 Hence,
Some are specific for IBD and others can be used across all medical acceptance of the procedure is crucial for adequate management of
fields [Supplementary Table 14, available as Supplementary data at the disease. Furthermore, endoscopy in IBD can be more demanding
ECCO-JCC online].99 Disease-specific measures may be more sensi- than in the general population; a prospective study on 558 colonos-
tive to variable disease activity,212 whereas generic QoL instruments copies in IBD patients showed a mean procedure time of 21 min.
permit comparison of different patient populations.1,213 These instru- The current European quality initiative established a minimum
ments are not only used in adults and children alike; the process has standard of 6 min and a target standard mean of 10 min of with-

also been extended to parents,214–216 families, and carers.102 drawal time.131 A retrospective analysis of 5282 patients who under-
The Inflammatory Bowel Diseases Questionnaire [IBDQ] is went an outpatient colonoscopy associated the previous diagnosis
the foremost106 and the most widely used tool. The IBDQ has up of IBD with higher demand of sedation.132,133 Therefore, endoscopic
to 36 items and has been purported to represent the gold stand- procedures in IBD patients should be performed under deep seda-
ard.217 Short questionnaires may be more appropriate when time tion instead of conscious sedation or no sedation. Propofol-based
for completion is limited. In contrast, in the research setting, the sedation is currently the best option for deep sedation in most cases,
need for more information may necessitate the use of longer ques- and should be administered by an endoscopist, anaesthesiologist, or
tionnaires or even a combination of generic and disease-specific trained nurse according to country-specific regulation.133–136 Besides
questionnaires.99,112,113,118 deep sedation, the use of CO2 has been shown to improve patient
Two recent systematic98,119 analysed IBD-specific tools. Another comfort and satisfaction and should be implemented if possible.137
review has highlighted the fragmented approach to the use of QoL
in this population.113 Some of the limitations are summarised in the 5.1.2 Bowel preparation
Supplementary table 14. Bowel preparation quality is important for the efficacy of colonos-
The Short Health Scale [SHS] deserves a mention as it consists copy and correlates with diagnostic yield and caecal intubation rate.
of only four questions. Developed in Sweden, the SHS showed good Bowel preparation quality should be routinely measured according
reliability, validity, and responsiveness in both patients with UC and to validated scales.14,129,138 Generally, patients with IBD do not have
those with CD.120,121 Some questions exist about its retest reliabil- less successful bowel preparation outcomes but may have decreased
ity.122 English,120 Danish, and Korean versions have been also devel- preparation tolerance, which affects adherence. Regardless of
oped.121 Additionally, the scale has been studied in children with the kind or the volume of the bowel preparation used, split-dose
IBD.123 However, the SHS showed similar properties in patients with administration has demonstrated better quality and acceptance of
irritable bowel syndrome, thus indicating that this scale is a more the preparation in many studies. These results have been validated
generic and not a disease-specific instrument.124 in two meta-analyses. Kilgore et al. included five trials and found
The Short-Form 36 health survey [SF-36] is the generic instru- that split-dose polyethylene glycol [PEG] was associated with sat-
ment for IBD patients125,126 and is used for both clinical and research isfactory bowel cleansing and patient tolerability (odds ratio [OR]
purposes.112 The SF-36 has eight dimensions, which are combined 3.7).139 Martel et al. obtained similar results in an analysis of 47
into two summary scores that reflect physical and mental compo- trials, including split doses of all available preparations [OR 2.5].140
nents. Individual domain scores should be reported, to allow com- Hence, split-dose administration of a low-volume PEG-based pur-
parison across different nationalities.113 gative should be recommended, especially in patients with previous
The EQ-5D is a shorter generic tool that has also been validated preparation intolerance, intestinal hypomotility, or stenosis.138,141–143
in IBD127 but is less frequently used. The EQ-5D has five questions or Patients who have undergone many colonoscopies may have a per-
domains that have the same set of answers and are combined with sonal preference for their bowel preparation, which should be taken
a standardised VAS. into consideration.138 IBD could be considered as a relative contrain-
The CUCQ-8 is a validated IBD-specific and QoL-specific dication for the use of sodium phosphate-based agents, which may
32-item short questionnaire that has the potential to be an efficient also cause mucosal abnormalities that mimic IBD.138,143
tool for assessing the QoL of all IBD patients.128
5.1.3 Technical requirements and training
High-definition technology is preferred over standard colonoscopy,
Chapter 5 General principles and technical especially when performing dysplasia surveillance.14,144 Regardless
aspects of endoscopy including enteroscopy, of diagnostic or therapeutic intent, endoscopy in IBD is technically
capsule endoscopy, ultrasound, CT, MRI, and demanding and a thorough knowledge of the disease is also required.
Moreover, some clinical scenarios [including severely active disease
small bowel enteroclysis/small bowel
or endoscopic dilation] appear to be associated with higher risk of
follow-through [SBE/SBFT]
perforation.14
5.1 Principles of conventional endoscopy To optimise diagnostic yield and impact of clinical management,
5.1.1 Sedation IBD endoscopists should be experienced in both endoscopic and
Colonoscopy is generally perceived as unpleasant by patients. As clinical management of the disease. Therefore, endoscopy in IBD
stated by the European quality improvement initiative for lower should be considered as part of the specific training in IBD.145
280 A. Sturm et al.
Colonoscopic surveillance of chronic colitis patients using meth- 5.2.3 Training

ylene blue dye-spray targeted biopsies results in improved dyspla- Capsule endoscopy should be performed by a gastroenterolo-
sia yield compared with conventional random and targeted biopsy gist experienced in conducting, interpreting, and reporting capsule
methods. Accordingly, this technique warrants incorporation into endoscopy procedures.151 Moreover, capsule endoscopy in IBD
clinical practice in this setting and consideration as a standard of patients should be evaluated by gastroenterologists with experience
care for these patients.146,147 in conventional endoscopy in IBD patients.
Statement 5.1.1. ECCO-ESGAR Diagnostics GL [2018] Statement 5.1.2. ECCO-ESGAR Diagnostics GL [2018]
Conventional endoscopy is essential for diagnosis and Capsule endoscopy is appropriate to evaluate small
monitoring of IBD; patient experience and acceptance bowel Crohn’s disease [CD]. The use of bowel preparation
must be considered. Propofol-based deep sedation [EL5] [EL1] and simeticone [EL2] is recommended for capsule
and CO2 insufflation [EL5] should be offered. IBD endos- endoscopy
copy should be performed preferably by an endoscopist

who is experienced in IBD endoscopy and also in IBD 5.3 Enteroscopy
clinical management [EL5]. Bowel preparation with a 5.3.1 Equipment
split-dose polyethylene glycol [PEG]-based purgative is Enteroscopy enables live assessment, treatment, and tissue sampling of
recommended [EL1] the small bowel. Conventional push enteroscopy is intended to access
only the proximal small bowel, but the median insertion typically does
5.2 Capsule endoscopy not exceed 100 cm from the angle of Treitz.154 In patients with IBD, it
Wireless video-capsule endoscopy is a method of endoluminal may be necessary to reach deeper beyond the limits of ileocolonoscopy
mucosal examination of the bowel. This form of endoscopy is based and push enteroscopy. Therefore, in IBD patients undergoing direct
on a pill-sized camera tool that is swallowed by the patient and trav- endoscopic assessment of the small bowel, device-assisted enteroscopy
els through the patients’ luminal digestive tract through its intrinsic should be performed. There are not enough data to recommend any
motor activity. The capsule continuously captures images that are modality of device-assisted deep enteroscopy, either single, double-
wirelessly transmitted to a data recorder worn by the patient. Images balloon, or spiral enteroscopy, or balloon-guided endoscopy.155
are downloaded, processed, and examined by a trained gastroenter-
ologist on a workstation. 5.3.2 Patient preparation and basic technique
Fasting for at least 12 h and avoidance of liquid consumption for
4 h is generally sufficient for patients undergoing oral device-assisted
5.2.1 Equipment
enteroscopy. However, standard colonoscopy preparation is required
All currently available small bowel video capsules are appropri-
for retrograde examination.156
ate for IBD.148 Advances in technology have enabled wireless cap-
Device-assisted enteroscopy is clinically challenging and requires
sule endoscopy systems to examine the colonic mucosa. Despite
deep sedation or general anaesthesia. This procedure seems to be
substantial agreement shown in different endoscopic disease
as safe in IBD patients as in other populations: the general rate of
activity indexes between capsule and conventional colonoscopy,
major complications is estimated at 0.7%. Accordingly, this proce-
there are insufficient data to recommend colon capsule studies in
dure should only be performed if indicated and change of clinical
the evaluation of IBD.148,149 Recently, a new capsule endoscopy
management is intended or expected.155,157 The use of CO2 insuffla-
system has been developed that evaluates both the intestinal and
tion instead of room air is highly recommended in device-assisted
colonic mucosa; however, data regarding its usefulness in IBD
enteroscopy procedures, as it may improve the intubation depth and
remain scarce.150
reduce post-procedural discomfort.158,159
5.2.2 Patient preparation and basic technique

Patients should fast for at least 12 h prior to capsule ingestion. The 5.4. Small bowel follow-through and enteroclysis
use of bowel preparation is recommended, as this has been shown 5.4.1 Equipment
to improve the visualisation and the diagnostic yield. Although there Small-bowel follow through [SBFT] and small-bowel enteroclysis
are not enough data to recommend any specific type of preparation, [SBE] are performed using conventional X-ray equipment imaging.
PEG in half dose [1 L], low volume [2 L], or high volume [4 L] has Digital fluoroscope technology is now widely available and allows
been shown to be beneficial.151 As recommended for any other indi- real-time image projection and storage of image ‘loops’. Digital
cation, following capsule ingestion with water, clear liquids may be technology facilitates better radiation dose control in the generally
taken after 2 h and food and medications may be taken after 4 h. young IBD patient population. Equipment to compress, move, and
Appropriate documentation of the procedure and its findings in IBD separate the opacified small bowel should be available. SBFT and
patients undergoing capsule endoscopy should include standardised SBE have high accuracy for mucosal abnormalities [including ulcera-
items. Use of IBD-specific scales such as the Lewis Score and the cap- tions and strictures] and can possibly identify extramural complica-
sule endoscopy Crohn’s Disease Activity Index is encouraged.49,151,152 tions, such as internal fistulas.
On the basis of a recent meta-analysis, the capsule retention rate
in patients with suspected or known IBD is approximately between 5.4.2 Patient preparation and basic technique
4% and 8%. These rates decreased by half in studies that used either For both investigations, patients should have ‘nil by mouth’ for 6 h
a patency capsule or a cross-sectional imaging technique [such as before the procedure. SBFT may be augmented by pneumocolon to
MR enterography or CT enterography] to assess patency before per- produce double-contrast imaging of the distal ileum, which enhances
forming capsule endoscopy.153 the sensitivity for detecting subtle mucosal changes.160 Pneumocolon
requires retrograde insufflation of gas [e.g. room air or CO2] into the 5.4 MRI and CT
terminal ileum via a rectal tube, and requires bowel preparation to 5.5.1 Equipment
remove intraluminal material before the procedure.161 MR enterography and MR enteroclysis should be performed at ≥
SBFT consists of oral administration of 400 mL to 600 mL 1.5T. No evidence supports the superiority of one platform over
barium sulphate suspension, typically 30% to 50% weight/volume another.171,172 Phased-array coils should be used routinely. For peri-
over a specific period of time.162 Ingested volumes should be indi- anal fistula MRI, phased-array surface coils are preferred to endo-
vidualised for each patient. This is followed by serial fluoroscopic coils, given their larger field view and greater patient acceptance.173
interrogation of the small bowel and spot filming at intervals of 20 Due to the propulsive motor action of the gut, CT requires rapid
to 30 min, tracking passage of the contrast agent through the bowel. acquisition of high-resolution images of the bowel. Although there
Targeted compression views of the small bowel are mandatory to are no comparative studies comparing different CT platforms, CT
ensure that the whole small bowel is visualised as far as possible. enterography and CT enteroclysis in general should be performed on
Magnified compression views also facilitate detailed evaluation of scanners with at least 16 slices [ideally 64 or greater].
the small bowel mucosa.
SBE requires placement of a nasojejunal catheter under fluoro- 5.5.2 Patient preparation and basic technique

scopic guidance and insufflating the small bowel with barium and Patient preparation regimens are similar to MR enterography and CT
air or methylcellulose, to create a double-contrast distended view of enterography. Due to insufficient distension of the bowel, there is evi-
the small bowel.163,164 Automated pump infusion is preferred over dence that studies performed without oral contrast preparation have
hand injection. SBE in general provides better distension of the small inferior diagnostic accuracy when compared with those performed after
bowel than SBFT and has been suggested to improve evaluation of administration of oral contrast.174,175 Patients should fast from solids for
the bowel mucosa. However, any diagnostic superiority over SBFT 4–6 h before MR enterography or CT enterography. Liquids should
remains unproven. Furthermore, conscious sedation is sometimes also be restricted, although water is permissible. There are ranges of
necessary due to the discomfort the procedure can cause. suitable oral agents available to distend the small bowel, usually with
hyperosmolar properties.176 These include mannitol, PEG, sorbitol, or
5.4.3 Technical parameters
combinations thereof.177–182 There is currently no evidence that favours
During SBE, infusion rates of should be constantly adjusted to obtain
one preparation over another. Although use is not widespread, negative-
uniform distention of the entire small intestine, without overwhelming
contrast agents containing paramagnetic iron reduce luminal signal on
peristaltic capacity. All accessible segments of the small bowel should
both T1-weighted and T2-weighted images.183 Oral contrast agents
be manually or mechanically compressed during the course of infusion.
should be ingested 45 min before the examination.184 Volumes over
This includes using rotation and palpation and special manoeuvres used
1000 mL may give better distension,179 although it is possible to acquire
to isolate pelvic small bowel loops.162 Large-format images should be
diagnostically acceptable images with ingested volumes of 450 mL.185
obtained when the entire small bowel is adequately filled and distended.
Patients should be warned that they might experience cramping and
Similarly, segments of the small bowel should be manually or mechani-
diarrhoea after ingesting hyperosmolar oral contrast agents.
cally compressed to ensure adequate visualisation during SBFT.
Enteroclysis is more invasive than enterography and is less well
Barium sulphate is non-toxic and is normally passed in stool. SBE
tolerated by patients,186 but may provide superior distension of
is inherently more invasive, with tube placement under fluoroscopic
the proximal small bowel in particular.187 MR enteroclysis and CT
guidance resulting in a higher radiation exposure than that from
enteroclysis should be performed with similar distension agents as
SBFT.165 Although the radiation exposure for barium studies is lower
MR enterography and CT enterography, which should be infused via
than for CT, it is nevertheless a significant exposure for adults166 and
an 8F or 10F nasojejunal tube placed under fluoroscopic guidance.
children,167 particularly when repeated examinations are performed.
Automated pump infusion [at a rate of 80–120 mL/min] is preferred
Moreover, excessive fluoroscopy time and frequent abdominal radio-
over hand injection, although both are acceptable. On-table moni-
graphs can result in doses that are equivalent to CT.167
toring of small bowel distension should be performed during both
MR enteroclysis and CT enteroclysis, and infused volumes should be
5.4.4 Training individualised for each patient.170
SBFT and SBE are highly operator-dependent, and patient radiation Diagnostic accuracy for colonic inflammation is improved with
doses are influenced by the radiologist’s technique.168,169 Consequently, colonic filling, either by prolonged oral contrast administration188,189
dedicated gastrointestinal radiologists who are experienced in con- or via a rectal liquid enema.190 However, additional colonic prepara-
ducting and interpreting them should perform both procedures. tion is not required for routine MR enterography or CT enterog-
raphy. Superior bowel distension may be achieved by placing the
patient prone, but there is no evidence that this translates into supe-
Statement 5.2.1. ECCO-ESGAR Diagnostics GL [2018] rior diagnostic accuracy compared with the supine position.191
Small-bowel follow through [SBFT] and small-bowel enter-
oclysis [SBE] have a diminishing role and are largely now 5.5.4 Technical parameters
replaced by cross-sectional techniques. However, they CT images should be acquired following intravenous contrast
may have a role in specific clinical circumstances [EL5] agent administration in the enteric or portal venous phase only.192
Iodinated contrast administration facilitates assessment of the bowel
wall enhancement pattern and mesenteric vascularity. The use of
5.5 Cross-sectional imaging techniques multiplanar reformats is mandatory during CT evaluation, and these
Reference should be made to the ESGAR/ESPR guidelines for the should be reconstructed at 3 mm or less.193
technical performance of cross-sectional small-bowel and colonic Radiation exposure is the major limiting factor for the use of CT
imaging.170 in IBD.194,195 Exposure to high radiation doses can occur [primarily
282 A. Sturm et al.
due to repeated CT] and particularly in those with young age of

disease onset and complicated disease.196 It is therefore imperative Statement 5.3.1.2. ECCO-ESGAR Diagnostics GL [2018]
that dose exposure is minimised by optimising tube voltage and cur- A suitable oral contrast agent should be administered
rent.197,198 The use of automated tube current modulation reduces 45 min before MRI and CT enterography or infused via
dose while maintaining image quality.199 Furthermore, there are nasojejunal tube before MR enteroclysis or CT enterocly-
good data demonstrating that iterative reconstruction techniques sis [EL2]
significantly reduce dose while producing diagnostically acceptable
images200–204; these techniques should be applied routinely when
available. It is good practice to maintain a log of radiation exposure
Statement 5.3.1.3. ECCO-ESGAR Diagnostics GL [2018]
for patients with IBD undergoing repeat medical imaging.170 Due to
the risks from repeated radiation exposure, given the chronic nature Dedicated colonic preparation is not part of routine proto-
of the disease and need for repeated imaging, MRI is generally the cols but can be achieved either by prolonged oral contrast
preferred modality in IBD patients. or administration of a liquid rectal enema [EL2]
Although diagnostically acceptable MR enterography images

can be acquired without use of spasmolytic agents,205 administra-
tion of these agents improves bowel distension199 and use is cur- Statement 5.3.1.4. ECCO-ESGAR Diagnostics GL [2018]
rently recommended.170 Hyoscine butylbromide [butylscopolamine]
is the spasmolytic agent of choice, although glucagon is an accept- Radiation exposure is a limitation of CT and should only be
able alternative.206 High-quality MR enterography and MR entero- used if MRI or ultrasound is not available. Dose exposure
clysis require fast breath-hold sequences to minimise breathing and must be minimised by optimising acquisition parameters,
peristaltic artefacts. A typical protocol should include a combination use of tube current modulation, and iterative reconstruc-
of T2-weighted and steady-state free precession gradient echo [SSFP tion techniques when available [EL2]. Cumulative radia-
GE] sequences. T1-weighted images acquired in the enteric or portal tion exposure of IBD patients should be monitored [EL5]
venous phase following intravenous gadolinium contrast adminis-
tration facilitate assessment of the bowel wall enhancement pattern
and mesenteric vascularity, with some evidence that they increase Statement 5.3.1.5. ECCO-ESGAR Diagnostics GL [2018]
diagnostic accuracy.207,208 However, recent studies have reported long-
term retention of gadolinium in the brain of exposed patients,209–212 MR enterography and MR enteroclysis should be per-
and protocols omitting gadolinium contrast may have similar diag- formed with fast breath-hold sequences to minimise
nostic accuracy.213,214 Administration of gadolinium should therefore breathing and peristaltic artefacts [EL2]. Consideration
be considered on a case-by-case basis. There are increasing data sup- should be precede the routine use of intravenous gado-
porting the use of diffusion-weighted imaging214–217 and cine motil- linium in all patients, weighing the risks and benefits [EL4]
ity sequences,218–221 in both disease detection and activity assessment.
Pending further research, these sequences are currently considered
optional.170 Statement 5.3.1.6. ECCO-ESGAR Diagnostics GL [2018]
Sequence selection in perianal fistula imaging should include
Radiologists interpreting cross-sectional imaging in IBD
high-resolution T2-weighted images with and without fat saturation
require appropriate training, with initial evidence suggest-
angled to the plane of the anal canal. Short T1 inversion recovery
ing that radiologists should review at least 100 cases [EL2]
[STIR] sequences are an alternative to fat-saturated T2-weighted
sequences.222,223 The use of gadolinium enhancement on T1-weighted
imaging is useful for differentiating granulation tissue from fluid, for 5.6 Ultrasonography
gauging fistula activity,85 and may increase staging accuracy.224
5.6.1 Equipment
Modern ultrasound devices have sufficient quality and screen resolu-
5.5.5 Training tion to delineate the structure of the gastrointestinal wall. The reso-
There is evidence of a learning curve in the interpretation of MR lution of an ultrasound transducer is dependent on the frequency,
enterograpy. Initial data suggest that feedback on 100 cases is the speed of sound in tissue, and the number of cycles in the ultra-
required to achieve diagnostic accuracy equivalent to that of expe- sound pulse. Since the thickness of the bowel wall layer is usually <
rienced radiologists.225 However, once trained, radiologists tend to 3 mm,231 the frequency of the transducer must be at least 5 MHz for
maintain their interpretation skills long term.226 Moderate-to-good wall layers to be well discriminated. No head-to-head studies have
interobserver agreement has been reported for MR enterogra- been published comparing the diagnostic performance of regular
phy77,226,227 and CT enterography,228 with one study suggesting higher low-frequency, mid-frequency, or high-frequency probes for detec-
reader agreement for CT enterography over MR enterography.229 tion of the normal small bowel and pathological findings. Harmonic
There are also data that confirmed a learning curve in the interpreta- imaging should be activated when available, as this may improve
tion of MRI perianal fistula imaging, with improvement in accuracy delineation of the bowel wall.232
after dedicated training.230 Doppler ultrasound can assess both blood flow in the visceral
vessels that supply the gastrointestinal tract and the smaller vessels
of the intestinal wall. Doppler ultrasound cannot detect capillary
CT enterography and CT enteroclysis should be performed flow. Colour Doppler or power Doppler can both be used to evaluate
on CT scanners with at least 16 slices. MR enterography bowel wall vascularity.233 Flow parameters should be optimised to
and MR enteroclysis can be performed at 1.5T or 3T [EL2] maximise the sensitivity for the detection of vessels with low-veloc-
ity flow in the bowel wall. The information obtained from colour
Doppler images is semi-quantitative. It is recommended to measure the operator. Colonic preparation or liquid enemas are also not
bowel wall vascularity according to the number of vessels detected required. As noted above, use of colour Doppler should be routine.
per square centimetre.234–236 Although both CEUS and elastography are highly promising evolving
Increased vascularity of the diseased bowel wall is a marker of techniques, they are not yet routinely used outside specialist centres.
disease activity. To improve the sensitivity of Doppler ultrasound,
intravenous ultrasound contrast agents have been introduced. For 5.6.6 Training
example, the second-generation echo-signal enhancer SonoVue is The interobserver agreement between operators with various degrees
injected as a bolus in units of 1.2–4.5 mL into an antecubital vein, of experience in bowel ultrasound and its learning curve needs to be
immediately followed by injection of 10 mL of normal saline solu- investigated further. Dedicated training in bowel ultrasound is neces-
tion [0.9% NaCl] flush. For each examination, a recording is ini- sary and should preferably be performed following training in gen-
tiated a few seconds before the intravenous administration of the eral abdominal ultrasound.254,255 Preliminary data suggest that signs
agent, and continuous imaging is performed for 40 s.237 There are of CD in bowel ultrasound can be standardized and have shown fair-
several ways of interpreting contrast enhancement in the bowel wall. to-good reproducibility. In particular, bowel wall thickness shows
These include pattern of enhancement,238,239 contrast quantification excellent reproducibility.256

at peak intensity,240 and dynamic contrast-enhanced ultrasound
where intensity changes over time are analysed.241
5.6.2 Contrast-enhanced ultrasound
For a complete examination of the bowel with ultrasound,
Contrast-enhanced ultrasound [CEUS] can be used to quantify vas-
low-resolution and high-resolution probes should be used
cularity242 but can also be used to separate vascular from avascu-
[EL5]
lar tissue, which is particularly useful when trying to differentiate a
phlegmon from an abscess.243

5.6.3 Small intestine contrast ultrasonography
In recent years, the use of oral contrast agents [such as PEG solution] The use of intraluminal orally administered contrast
has been introduced to distend the bowel for better characterisation agents improves the overall accuracy in diagnosing small-
of the bowel wall and increased disease detection. The use of an bowel CD [EL2]
oral contrast agent does not alter the procedure greatly; the same
equipment is used with the addition of 375–800 mL of oral contrast
fluid. However, the procedure duration increases, ranging from 25 to Statement 5.3.2.3. ECCO-ESGAR Diagnostics GL [2018]
60 min.244 The accuracy for assessing lesions in the proximal small
bowel and for defining the extent of diseased ileal walls can be signif- Contrast-enhanced ultrasound [CEUS] of the bowel can
icantly improved using small intestine contrast ultrasonography.245 be used to differentiate vascular from avascular intestinal
or peri-intestinal lesions, including abscesses [EL3]
5.6.4 Ultrasound elastography
Gut fibrosis develops in up to 50% of Crohn’s disease [CD] patients
and is a major challenge.246 Clinically suspected fibrostenotic dis- Statement 5.3.2.4. ECCO-ESGAR Diagnostics GL [2018]
ease is currently mainly investigated by contrast-enhanced CT,247
A standard ultrasound examination of the intestine does
or MR247,248 enterography, or MR enteroclysis, or native ultrasound
not require specific patient preparation, although fasting
and CEUS [see above]. Novel MRI sequences [such as magnetisation
is recommended before the examination [EL4]
transfer] also show promise,249,250 although detection and characteri-
sation of fibrotic disease by imaging remains suboptimal. Whereas
MR elastography is being studied for staging several diseases [such
as liver fibrosis], it has not been studied in fibrotic bowel disease.
Ultrasound elasticity imaging based on strain under deformation Dedicated training in bowel ultrasound is necessary
and elastic modulus251 is an evolving technique. Recent studies sug- and should be performed following training in general
gest that ultrasound elastography can differentiate between fibrotic abdominal ultrasound [EL5]
and inflammatory stenosis independent of wall thickness and blood
flow in CD.252,253
Conflict of Interest
5.6.5 Patient preparation and basic technique
Abdominal ultrasound is most successful in non-obese patients, due ECCO and ESGAR have diligently maintained a disclosure policy of potential
to its basic technical principles as discussed above. The small bowel conflicts of interests [CoI]. The conflict of interest declaration is based on a
form used by the International Committee of Medical Journal Editors [ICMJE].
and colon should be carefully and systematically interrogated, using
The CoI statement is not only stored at the ECCO Office and the editorial
gentle graded compression. No patient preparation is needed to per-
office of JCC, but also is open to public scrutiny on the ECCO website [https://
form bowel ultrasound. However, to reduce the amount of food and
www.ecco-ibd.eu/about-ecco/ecco-disclosures.html] providing a comprehen-
bowel gas, a fasting period of at least 4–6 hours is recommended, sive overview of potential conflicts of interest of authors. The ECCO-ESGAR
although there are no rigorous studies confirming this approach.254 Consensus Guidelines are based on an international consensus process. Any
Administration of a spasmolytic agent is not required and indeed treatment decisions are a matter for the individual clinician and should not be
may interfere with the real-time assessment of bowel peristalsis by based exclusively on the content of the ECCO-ESGAR Consensus Guidelines.
284 A. Sturm et al.
The European Crohn´s and Colitis Organisation, the European Society of • Greece: Ioannis Koutroubakis, Charikleia Triantopoulou
Gastrointestinal and Abdominal Radiology, and/or any of its staff members, • Ireland: Garret Cullen
and/or any consensus contributor may not be held liable for any information • Israel: Matti Waterman
published in good faith in the ECCO-ESGAR Consensus Guidelines. • Italy: Ennio Biscaldi
• Lithuania: Gediminas Kiudelis
• Moldova: Svetlana Turcan
Acknowledgements • Poland: Maria Klopocka, Małgorzata Sładek
• Portugal: Paula Ministro dos Santos
Guidelines Panel:
• Romania: Mihai Mircea Diculescu
Chairs: Andreas Sturm, Christian Maaser, and Jaap Stoker
• Russia: Alexander Potapov
Consultant Pathologist Expert: Paula Borralho Nunes
• Spain: Javier Gisbert, Rosa Bouzas
Working Group [WG]1: Initial diagnosis [or suspecting IBD], Imaging tech-
• Sweden: Ann-Sofie Backman, Michael Eberhardson
niques in regard to location: Upper Gastrointestinal [GI] tract, Mid GI tract,
• Switzerland: Dominik Weishaupt
Lower GI tract, Perianal disease, Extraintestinal manifestation
• Trinidad & Tobago: Alexander Sinanan
Leader – Stephan Vavricka
• UK: Barney Hawthorne
Member – Pierre Ellul
Additional reviewers who participated in the 2nd Voting Round:

Member – Fabiana Castiglione
• Almer, Sven
Y-ECCO – Bram Verstockt
• Biancone, Livia
ESGAR – Damian Tolan
• Bonifacio, Cristiana
WG2: Imaging techniques in regard to clinical situations: Monitoring thera-
• Civitelli, Fortunata
peutic success [inclusive calpro], Monitoring clinically asymptomatic patients,
• Eder, Piotr
Monitoring clinically symptomatic patients, Imaging after surgery including
• Fernandes, Carlos
ileoanal pouch
• Lopetuso, Loris
Leader – Torsten Kucharzik
• Luglio, Gaetano
Member – Patrick van Rheenen
• Portela, Francisco
Member – Uri Kopylov
• Rizzello, Fernando
Y-ECCO – Hannah Gordon
• Sahnan, Kapil
ESGAR – Andrea Laghi
• Sieczkowska, Joanna
WG3: Detecting [suspected] complications [stricture, fistula, abscess, anas-
Reviewers, on behalf of GuiCom: Tim Raine, Glen Doherty
tomotic insufficiency, toxic megacolon, perforation]: Endoscopic and non-
medical, non-surgical interventions [stricture, abscess, bleeding], Cancer
surveillance, Imaging during pregnancy
Leader – Gionata Fiorino
Supplementary Data
Member – Florian Rieder Supplementary data are available at ECCO-JCC online.
Member – Paulo Kotze
Member – Abraham Eliakim
Y-ECCO – Dominik Bettenworth
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Journal of Crohn's and Colitis, 2018, 273–290

ECCO Guideline/Consensus Paper

ECCO-ESGAR Guideline for Diagnostic

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Statement 4.1.1. ECCO-ESGAR Diagnostics GL [2018]

Table 2. Mayo score for ulcerative colitis.6

Mayo Score [Index] 0 1 2 3

Stool frequency Normal 1–2/day >normal 3–4/day >normal 5/day >normal

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Score Endoscopic Strengths Weaknesses Proposed

Truelove and Witts11 No endoscopic descriptor definitions ----- ----- -----

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Table 5. Non-endoscopic Crohn’s disease activity indexes in clinical practice.

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Colonoscopic surveillance of chronic colitis patients using meth- 5.2.3 Training

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5.2.2 Patient preparation and basic technique

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due to repeated CT] and particularly in those with young age of

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Statement 5.3.2.2. ECCO-ESGAR Diagnostics GL [2018]

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