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Pre- and post-procedural quality indicators for colonoscopy: A nationwide survey

Digestive and Liver Disease, In Press, Corrected Proof, Available online 29 March 2016, Available online 29 March 2016

Abstract

Background

The provision of high-quality colonoscopy can be assessed by evaluating technical aspects of the procedure and, at individual center level, by comparing structural indicators and institutional policies for managing peri-procedural issues with guideline recommendations.

Aim

To assess the colonoscopy quality (CQ) in Italy at center level.

Methods

Gastroenterologists participating in a nationwide colonoscopy education initiative provided information on structural indicators of their centers and on institutional policies by answering 10 multiple-choice clinical scenarios. Practice variation across centers and compliance with guidelines were analyzed.

Results

Data from 282 Italian centers were evaluated. Overall, a significant proportion of centers did not meet CQ standards as concerns endoscopy facilities and equipments (e.g., dedicated recovery room, dirty-to-clean path, reporting software). CQ assurance programs were implemented in only 25% of centers. Concerning peri-procedural issues, main discrepancies with guidelines were recorded in the underuse of split-dose preparation (routinely adopted by 18% of centers), the routine request of coagulation tests prior to colonoscopy (30%), the routine interruption of aspirin for polypectomy (18%), and the adoption of 3-year surveillance for low-risk adenoma (49%).

Conclusions

Present survey shows a significant variation in the CQ of endoscopy centers in Italy on many items of colonoscopy practice that should be targeted for future interventions.

Keywords: Colonoscopy, Practice guidelines, Quality.

1. Introduction

Colonoscopy plays a pivotal role in colorectal cancer (CRC) prevention and diagnosis, but its effectiveness depends on the quality of the examination. High-quality colonoscopy delivers better health outcomes (i.e., lower risk of interval CRC) [1] and [2], better patient experience, and fewer repeated procedures [3]. Although the overall quality of colonoscopy has significantly improved over the last few years, it can still vary considerably across centers and endoscopists.

Despite a set of quality indicators (QI) for the different steps of the colonoscopy procedure (i.e., pre-procedure, intra-procedure, and post-procedure) [4], [5], and [6] has been developed, most studies on colonoscopy quality are focused on few key-performance measures mainly related to the technical aspects of the examination, such as adenoma detection and caecal intubation rate [1], [2], [7], [8], and [9]. Nevertheless, the provision of high-quality colonoscopy is complex and it results from the interaction of a myriad of factors other than technical ones. To this regard, the characteristics and conditions of the healthcare institutions in which digestive endoscopy is delivered (structural indicators; e.g., endoscopy volume and workforce, type of instruments and other endoscopy equipment), and the institutional policies for patient care before (e.g., bowel preparation, management of anti-thrombotic therapy), during (e.g., sedation) and after (e.g., post-polypectomy surveillance) the examination [10] may also influence the overall quality of colonoscopy. For each of these areas (domains) of clinical practice [10], international professional GI societies have issued practice guidelines in order to advise on the best strategies, according to the available evidence, and optimize patient care. In this perspective, the quality of colonoscopy should be assessed not only by measuring individual endoscopist performance, but also, at endoscopy center level, by comparing local institutional policies for each domain to the evidence-based guideline recommendations [11].

The aim of present survey, including a large number of endoscopy units of both academic and non-academic hospitals all over Italy, was to explore the variability of colonoscopy practice across centers as concerns relevant periprocedural issues and to determine the adherence to current guidelines, in order to provide a snapshot of the quality of Italian endoscopy services and identify areas that might benefit from further research.

2. Methods

In 2014, a nationwide colonoscopy education initiative (Bowell.it Educational Tour) was held in Italy. Overall, 480 gastroenterologists and GI endoscopists from 289 different endoscopy centers participated in 14 meetings, aimed at increasing awareness on colonoscopy quality issues and optimizing colonoscopy practice. During these meetings, one endoscopist, representative of each participating center, was invited to take part in the survey by filling in a standard questionnaire. The questonnaire included 13 questions on structural indicators of each endoscopy center (Table 1) and 10 multiple-choice clinical scenarios exploring institutional policies on clinically relevant peri-procedural colonoscopy issues such bowel preparation, sedation practice, management of anti-thrombotic therapy, polyp resection and surveillance. Each endoscopist anonymously completed the questionnaire and returned it to secretary staff in the morning, before the meeting educational session had started.

Table 1 Structural indicators, according to the type of centers.

Overall
n = 282
University hospital
n = 39
Community hospital
n = 234
Private practice
n = 9
P-value
Center volume (colonoscopies/year)
 <1000 60 (21.3%) 6 (15.4%) 48 (20.5%) 6 (66.6%) <0.001
 1000–3000 137 (48.5%) 13 (33.3%) 122 (52.1%) 2 (22.3%)
 >3000 85 (30.2%) 20 (51.3%) 64 (27.4%) 1 (11.1%)
Participation in the national screening program 209 (74.1%) 29 (74.3%) 177 (75.6%) 3 (33.3%) 0.017
Dedicated recovery room 182 (64.5%) 26 (66.6%) 150 (64.1%) 6 (66.6%) 0.94
Dirty-to-clean path 190 (67.3%) 22 (56.4%) 160 (68.4%) 8 (88.8%) 0.12
Site of colonoscopy scheduling
 Endoscopy Unit 113 (40.4%) 27 (69.2%) 80 (34.2%) 6 (66.6%) <0.0001
 Centralized Booking Office 169 (59.6%) 12 (30.8%) 154 (65.8%) 3 (33.3%)
Colonoscopy slots
 30 min 139 (49.3%) 19 (48.7%) 120 (51.3%) 0 0.04
 45 min 129 (45.7%) 17 (43.6%) 104 (44.3%) 8 (88.8%)
 60 min 14 (5.0%) 3 (0.7%) 10 (0.4%) 1 (11.2%)
Dedicated reporting software 215 (76.3%) 31 (79.5%) 180 (76.9%) 4 (44.4%) 0.07
Video/images recording system 229 (80.8%) 34 (87.1%) 186 (79.5%) 9 (100.0%) 0.17
Quality indicators recording integrated into the reporting software 101 (35.8%) 20 (68.9%) 79 (33.7%) 2 (22.2%) 0.07
Ongoing colonoscopy quality assurance program 73 (25.5%) 13 (33.3%) 58 (24.8%) 2 (22.2%) 0.51
Electro-surgery unit in any endoscopy room 244 (86.5%) 28 (71.8%) 208 (88.8%) 8 (88.8%) 0.01
High-definition colonoscopes 175 (62.9%) 25 (64.1%) 146 (62.4%) 4 (44.4%) 0.53
Electronic chromo-endoscopy system 151 (53.5%) 22 (56.4%) 126 (53.8%) 3 (33.3%) 0.44

Concerning the 10 clinical scenarios, two authors (SP, FR) reviewed practice guidelines by US and European GI Societies (American Society for Gastrointestinal Endoscopy, ASGE; American College of Gastroenterology, ACG; European Society for Gastrointestinal Endoscopy, ESGE; British Society of Gastroenterology, BSG), in order to determine, whenever possible, the recommended management strategy.

Data from collected questionnaires were gathered and processed. Finally, practice variation across centers and possible discrepancies with recommendations in guideline were analyzed and discussed.

The protocol was approved by the Ethics Committee of the coordinating center (Valduce Hospital).

3. Statistics

Categorical variables were summarized using frequencies and percentages with 95% confidence intervals. Chi-squared (χ2) test was used to compare categorical variables. All statistical tests were two-sided and were considered statistically significant at P < 0.05.

4. Results

Overall, questionnaires from 282 centers were collected, representing the 58.1% of the 485 endoscopy centers in Italy, according to a Italian Society of Digestive Endoscopy (SIED) census spread in year 2014. Information was provided by 146 (51.8%) centers in Northern Italy, 70 (24.8%) from the center and 66 (23.4%) from the South and Islands. Of the participating centers, 234 (83%) were community hospitals, 39 (13.8%) academic hospitals and 9 (3.2%) private practice centers. Structure and organizational indicators, according to the type of centers, are shown in Table 1. All centers were “open access”, so that endoscopy procedures could be scheduled at the request of a referring physician, without a previous clinic consultation [12]. Clinical scenarios exploring institutional policies on peri-procedural colonoscopy issues and responses provided by participants are analyzed below.

(1) What bowel cleansing regimen for colonoscopy is routinely prescribed in your center?

Bowel cleansing regimen Number of centers [%, 95%CI]
4-Liters PEG-ELSa 150 [53.2, 45.0–62.4]
Low-volume bowel preparationsb 103 [36.5, 29.8–44.3]
Sodium phospate 21 [7.4, 4.6–11.4]
Other (e.g., sennosides) 8 [2.9, 1.2–5.6]

a PEG-ELS: polyethylene glycol–electrolyte lavage solution.

b 2L PEG plus ascorbate, 2L PEG plus bysacodyl, sodium picosulphate plus magnesium citrate.

Both US and European guidelines on bowel preparation for colonoscopy consider 4 l polyethylene glycol–electrolyte lavage solution (PEG-ELS) as the ideal agent for bowel cleansing, due to its efficacy and safety profile; low-volume preparations are valid alternatives, in particular for patients with no risk factors for inadequate bowel preparation. Although sodium phosphate (NaP) is effective and well tolerated by most patients, the risk of adverse events makes it unsuitable as a first-line agent; accordingly, current guidelines advise against its routine prescription [13] and [14].

Data from the survey underline a roughly 90% compliance with the above statements, as concerns the choice of the cleansing agent. However, a non-negligible proportion of centers include NaP as routine agent for bowel cleansing. This finding is relevant; taking into account that in “open-access” systems bowel prep instructions are usually delivered by non-health care professionals (i.e., secretary staff) to an unselected population, the routine use of NaP should be proscribed.

(2) How often is split dose regimen for bowel preparation for colonoscopy prescribed in your center?

Adoption of split dose regimen Number of centers [%, 95%CI]
Routinely (more than 80% colonoscopies) 52 [18.4, 13.8–24.2]
Only for late morning or afternoon colonoscopies 83 [29.4, 23.4–36.5]
Occasionally (less than 5% of colonoscopies) 20 [7.1, 4.3–10.9]
Never 127 [45.0, 37.5–53.6]

Both US and European practice guidelines strongly recommend the routine adoption of split-dose regimens for elective morning colonoscopy [13] and [14], due to its superior efficacy and tolerability compared to the traditional regimen of administering the preparation the day before the procedure [15] and [16]. Split dosing has also been demonstrated to increase adenoma detection rate in a screening setting [17].

Although the present survey suggests an increasing trend in the adoption of split-dosing in Italy, as compared to a previous report [18], it clearly documents an unacceptable delay in its implementation and a clinically relevant underuse in the clinical practice.

(3) Is laboratory testing (coagulation tests and platelet count) routinely requested before colonoscopy in your center?

Routine request of laboratory testing Number of centers [%, 95%CI]
Yes 85 [30.1, 24.1–37.3]
No 197 [69.9, 60.4–80.3]

ASGE guidelines advise against routine testing with coagulation studies, chest radiography, electrocardiography, blood typing or screening and chemistry tests before endoscopy, and recommend individualizing them on the basis of patient characteristics and procedural risk factors. Coagulation tests before endoscopy should be restricted only to patients with known or clinically suspected bleeding disorders, medication risk (anticoagulant use), history of abnormal bleeding and conditions associated with acquired coagulopathies [19]. About 30% of centers involved in the present survey routinely still request lab testing before colonoscopy, resulting in unjustified wasting of resources and potential untoward implications (e.g., rescheduling of endoscopic procedures in case of unavailability of blood tests).

(4) Is sedation/analgesia routinely (>80% of the procedures) provided for colonoscopy in your center?

Routine use of sedation and analgesia Number of centers [%, 95%CI]
Yes 234 [83.0, 72.7–94.3]
No 48 [17.0, 12.6–22.6]

Sedation/analgesia during colonoscopy has a key role in enhancing patient comfort, improving acceptability, and reducing procedure duration (4). Observational studies also suggest that sedation improves the overall quality of colonoscopy, by increasing caecal intubation and “polyp/adenoma” detection rates [7] and [8]. Accordingly, in Europe and United States is recommended that sedation and analgesia should be routinely offered for colonoscopy [6], [20], and [21].

In 2007, a nationwide Italian survey, collecting data from 278 centers, reported that sedation/analgesia was used during 55% of colonoscopies [22]. Data from the present survey demonstrate that the use of sedation has been drastically increased over the past decade; this likely reflects a greater attention towards the patient experience and the overall quality of the procedure.

(5) In which cases are oral anticoagulants routinely withheld before colonoscopy in your center?

Anticoagulant management Number of centers [%, 95%CI]
Never withheld 60 [21.3, 16.2–27.4]
Withheld in patients at higher risk of polyps (i.e., positive FIT, post-polypectomy surveillance) 63 [22.3, 17.2–28.6]
Routinely withheld 159 [56.4, 48.0–65.9]

Current guidelines clearly recommend to continue anticoagulation for diagnostic procedures, and to withhold it in case of operative colonoscopy (polypectomy) [23] and [24]. However the key issue, neglected by the current guidelines, is how to manage anticoagulation before colonoscopy, when the presence of significant polyps is unpredictable. The only evidence from the literature, coming from a decision analysis study, suggest that temporary warfarin cessation before colonoscopy is cost-effective when the probability of polypectomy is higher than 35% [25]. Accordingly, the strategy of temporary withholding anticoagulants upon clinical indications, applied in 22% of the participating centers, is likely the most appropriate approach.

(6) What is the maximum size of non-pedunculated polyps (provided that no clear features of submucosal invasion are present) that are concomitantly resected during the index colonoscopy in the routine practice in your center?

Polypectomy during index colonoscopy Number of centers [%, 95%CI]
Never 0
Only for polyps up to 10 mm 64 [22.7, 17.5–29.0]
Only for polyps up to 20 mm 54 [19.1, 14.4–24.9]
Always 164 [58.2, 49.6–67.8]

The majority of colonic and rectal superficial lesions can be effectively removed in a curative way by standard polypectomy and/or by endoscopic mucosal resection (EMR) [26]. While most neoplastic lesions <20 mm should be readily resected by endoscopists with appropriate basic training, the resection of larger lesions is usually more technically demanding, time-consuming, and associated with a higher complication rate. Accordingly, recent BSG guidelines advise to defer resection of non-pedunculated lesions larger than 20 mm unless appropriate patient consent, time slots and endoscopist expertise allow it [27]. The data presented in our survey show that one out of five centers routinely defers resection for polyps >10 mm, which might lead to an unjustified rescheduling of a significant number of colonoscopies. On the other hand, the routine resection of any polyp, regardless of size, by about 60% of centers clashes with the abovementioned recommendations and deserves a critical evaluation.

(7) Is polypectomy routinely performed, with or without prophylactic haemostatic procedures, in case of ongoing aspirin treatment in your center?

Polypectomy on aspirin Number of centers [%, 95%CI]
Never 50 [17.7, 13.2–23.4]
Only for polyps up to 10 mm 119 [42.2, 35.0–50.5]
Only for polyps up to 20 mm 49 [17.4, 12.9–23.0]
Always 64 [22.7, 17.5–29.0]

Several observational studies support the safety of continued aspirin administration in the peri-endoscopic period, even after high-risk endoscopic procedures. Accordingly, both US and European guidelines recommend that aspirin should not discontinued before resection, irrespective of polyp size [23], [24], and [28]. Aspirin discontinuation should be considered on an individual basis, depending on the risks of thrombosis vs hemorrhage, only in the context of endoscopic submucosal dissection (ESD) or large (>20 mm) colonic EMR. The present survey shows poor adherence to the abovementioned guidelines, with only 20% centers complying with the recommendations of aspirin continuation. Due to the burden of primary and secondary cardiovascular prevention in the general population, it appears important to underlines the importance of aspirin continuation, to avoid an inappropriate rescheduling of a large number of colonoscopies and to prevent patients from an unacceptable thrombotic risk.

(8) Is polypectomy routinely performed, with or without prophylactic haemostatic procedures, in case of ongoing thienopyridines (clopidogrel or ticlopidine) treatment in your center?

Polypectomy on thienopyridines Number of centers [%, 95%CI]
Never 170 [60.3, 51.6–70.1]
Only for polyps up to 10 mm 96 [34.0, 27.6–41.6]
Only for polyps up to 20 mm 11 [3.9, 1.9–7.0]
Always 5 [1.8, 0.6–4.1]

Dimensional criteria are relevant in patients taking thienopyridines. The resection of small polyps (≤1 cm), followed by endoclip placement (either routinely or in cases of excessive intra-procedural bleeding), has been reported to be relatively safe, provided that pure-cutting current is not applied [28] and [29]. Conversely, for polyps >1 cm, current guidelines call for caution and recommend to withdraw thienopyridines, provided that the patient is not at high risk for thrombotic events. However, when polyps must be resected in patients who cannot discontinue thienopyridines, preventive measures should be readily available. In patients with large polyps who are receiving thienopyridines, polypectomy deferral should be considered [28].

Data from our survey, showing that two thirds of the centers never perform polypectomy on thienopyridines, seem to be overly defensive. This approach tends to emphasize the risk of bleeding, which, albeit slightly increased by thienopyridines, can be successfully managed by endoscopy in most cases [29] and [30]. Conversely, it underestimates the thrombotic risk associated with drug interruption that is usually associated with worse patient outcomes.

(9) After the evaluation of polyp histology, how is post-polypectomy surveillance recommended in your center?

Post-polypectomy surveillance recommendation Number of centers [%, 95%CI]
Written always 197 [69.9, 60.4–80.3]
Written for high-risk adenomas only 25 [8.9, 5.7–13.1]
Orally 54 [19.1, 14.4–25.0]
Never 6 [2.1, 0.8–4.6]

Both US and European guidelines recommend that the endoscopist should specify and document the pathology-based follow-up for any colonoscopy with polypectomy [5], [20], and [31]. The rationale for this statement is that the endoscopist is better suited to anyone else to evaluate the appropriate surveillance interval, being aware of the quality of the baseline examination (e.g., quality of bowel preparation) [13]. Besides, written information likely improves patient's compliance.

Our survey shows suboptimal adherence to the guidelines, with about 30% of centers not providing written indications on post-polypectomy surveillance intervals.

(10) What kind of surveillance interval is recommended in your center to an average-risk subject participating in the Fecal Immunochemical Test (FIT)-based organized CRC screening program after the resection of a 8 mm tubular, low-grade dysplasia adenoma?

Recommended surveillance for low risk adenoma in a screening setting Number of centers [%, 95%CI]
FIT after 5 years 30 [10.6, 7.2–15.2]
Colonoscopy at 10 years 100 [35.5, 28.9–43.1]
Colonoscopy at 5 years 13 [4.6, 2.4–7.9]
Colonoscopy at 3 years 139 [49.3, 41.4–58.2]

ESGE and European guidelines on colorectal cancer screening recommend that patients with less than 3 small (<10 mm) adenomas and no advanced histology simply return to screening. According to this recommendation, in a FIT-based screening program, low-risk patients should repeat FIT in 5 years [31]. Conversely, in the same scenario, US guidelines suggest colonoscopy in 5–10 years [32].

Regardless of the guidelines adopted in the center, our data are disappointing as almost 50% of centers recommend to repeat colonoscopy at 3 years, showing a significant overuse of surveillance colonoscopy in low-risk patients.

5. Discussion

Data from the present survey show that there is a large variability across centers as concerns multiple colonoscopy domains and an overall scarce compliance with available guideline recommendations. This may negatively impact on safety, costs and patient experience, with related risks of suboptimal care and poor health outcomes.

Despite some structural indicators are essential prerequisites of any endoscopy center, the present survey shows significant shortcoming in facilities (e.g., lack of dedicated recovery rooms, and/or dirty to clean path) in many centers; moreover, there is no evidence of improvement when present data are compared with a nationwide survey performed more than 6 years ago [22]. Current data also outline deficiencies in technology, such as lack of last generation high-definition scopes, and of endoscopy reporting systems (with automatically generated collection of quality indicators). Their availability has been shown to be associated with colonoscopy quality [33] and it remains essential for quality assessment. Interestingly, most relevant structural indicators did not significantly differ according to the type of centers. The persistence of these structural inadequacies and technology deficiencies over time likely reflects the lack of accreditation programs for centers and the difficulty to find financial resources that are needed to implement quality programs. However, the presence of an ongoing quality assurance program in only about one out of four centers, regardless the type of centers again, may disclose a scarce attention to a “culture of quality” in the majority of endoscopy units.

The overall limited adherence to current guidelines as concerns the management of many peri-procedural issues may be associated with clinically relevant implications. As far as patient safety is concerned, the routine adoption of NaP for bowel cleansing in an open-access setting can expose patients to the risk of irreversible kidney injury (acute phosphate nephropathy) [34]. Besides, the underuse of split dosing may significantly decrease adenoma detection, resulting in an increased miss rate of significant neoplastic lesions [17]. Last but not least, the indiscriminate interruption of anticoagulants or antiplatelet agents before colonoscopy, to minimize procedural bleeding, may increase the risk of serious thrombotic events [35].

Many of the discrepancies with guideline recommendations identified in the present survey may also lead to a substantial unaffordable increase of colonoscopy repetition. For instance, the underuse of split dosing may result in surveillance colonoscopies at shorter intervals, due to suboptimal bowel cleansing. Likewise, the compulsory request of pre-colonoscopy laboratory testing or the systematic deferral of polypectomy for polyps larger than 10 mm or in patients on anti-thrombotic therapy, may lead to repeat a large number of examinations. All these issues increase endoscopy workload, lengthen waiting lists, and eventually boost colonoscopy costs. The need for colonoscopy repetition also negatively impacts on patient experience and further increases risks.

Interestingly, if interventions aimed at modifying structure indicators are difficult and require resources, interventions to “bridge the gap” between guidelines recommendations and everyday clinical practice seem to be more realistic even in budget-constrained health system. Indeed, interventions in these domain may be easy and cheap; as an example, it has already been demonstrated that the availability of charts in the endoscopy suites or pocket-size cards was useful to improve the adequacy of prescriptions, as concerns post-polypectomy surveillance interval [36]. However, as demonstrated by previous studies, the dissemination and the implementation of guidelines into practice are slow and difficult processes. The lack of knowledge about the guidance, resistances to behavior changes, the low strength of evidence for many recommendations, and, last but not least, organizational constraints are well known barriers against the implementation of guidelines into practice [37].

The main strength of our study is that we used of a standardized protocol to collect data from a large number of centers, both academic and non-academic, distributed all over the country. As more than a half of the endoscopy units in Italy were included in the survey, it provides a reliable snapshot of the nationwide quality of the endoscopy services. Nonetheless, we acknowledge certain limitations, which are in part intrinsically related to the study design. Data were collected at the center level; although each participating endoscopist (one for each center) was asked to answer the questions according to the management strategy routinely adopted in the center, we cannot definitely exclude that the answers could have been influenced by the physician's own attitude, rather than the institutional policy. Besides, any survey is based on self-reported answers to hypothetical scenarios, and do not necessarily reflect what it is really done in real clinical practice. Last but not least, the rigid structure of a multiple-choice questionnaire might be too simplistic to reliably represent the complexity of the everyday clinical practice.

Despite these limitations, data from the present survey clearly show that in Italy there is still a clinically significant variation in the quality of endoscopy services, with regards to many areas of colonoscopy practice, potentially resulting in suboptimal care, increased costs and poor health outcomes. Many areas of colonoscopy, other than the technical performance of the examination, are actually an essential backbone for procedure improvement, and must be targeted by interventions to improve overall colonoscopy quality.

Conflict of interest

None declared.

Acknowledgements

The authors would like to thank Dr. Anastasios Koulaouzidis MD, FACG (Endoscopy Unit, The Royal Infirmary of Edinburgh) for manuscript content and language revision.

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Footnotes

a Division of Gastroenterology, Valduce Hospital, Como, Italy

b Istituto Clinico Humanitas, Gastroenterology and Endoscopy Unit, Milano, Italy

c Gastroenterology Unit, A.O. Universitaria Careggi, Firenze, Italy

d Endoscopy Service, Department of Diagnostic and Therapeutic Services, IRCCS – ISMETT (Istituto Mediterraneo per i Trapianti e Terapie ad alta specializzazione), Palermo, Italy

e Department of Oncological Gastrointestinal Surgery, Division of Gastroenterology, S. Maria del Prato Hospital, Feltre, Italy

f Endoscopy Unit, Fondazione Poliambulanza, Brescia, Italy

g Digestive Endoscopy Unit, Azienda Ospedaliera Sant’Andrea di Roma, Italy

h Endoscopy Unit, A.O.U. Policlinico G. Martino, Messina, Italy

i Unit of Gastroenterology and Digestive Endoscopy, AUSL Bologna Bellaria-Maggiore Hospital, Italy

j Endoscopy Unit, Istituto Europeo di Oncologia, Milano, Italy

k Department of Clinical Medicine, S. Orsola-Malpighi Hospital, University of Bologna, Italy

l Digestive Endoscopy Unit, AUSL Modena Northern Area, Carpi-Mirandola Hospital, Italy

m Division of Gastroenterology, AOU Città della Salute e della Scienza, Torino, Italy

n Gastroenterology Unit, Nuovo Regina Margherita Hospital, Rome, Italy

o Humanitas University, Milano, Italy

Corresponding author at: Division of Gastroenterology, Valduce Hospital, Via Dante 11, 22100 Como, Italy. Tel.: +39 031324145; fax: +39 031324150.