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An Italian prospective multicenter study on colonoscopy practice and quality: What has changed in the last 10 years

Open AccessPublished:October 17, 2022DOI:https://doi.org/10.1016/j.dld.2022.09.007

      Abstract

      Background

      A relevant number of adenomas can be missed during colonoscopy.

      Aims

      Assess the current status of colonoscopy procedures in Italian centers.

      Methods

      A prospective observational study involving 17 hospitals (34 endoscopists) included consecutive patients undergoing standard colonoscopy. In the first phase, endoscopists performed consecutive colonoscopies. In the second phase, retraining via an online learning platform was planned, while in the third phase data were collected analogously to phase 1.

      Results

      A total of 3,504 patients were enrolled. Overall, a BBPS score ≥6 was obtained in 95.6% of cases (94.8% and 96.9% in the pre- and post-training phases, respectively). 88.4% of colonoscopies had a withdrawal time ≥6 min (88.2% and 88.7% in the pre- and post-training phases). Median adenoma detection rate (ADR) was 39.1%, with no significant differences between the pre- and post-training phases (40.1% vs 36.9%; P = 0.83). In total, 81% of endoscopists had a ADR performance above the 25% threshold.

      Conclusion

      High colonoscopy quality standards are achieved by the Italian hospitals involved. Quality improvement initiatives and repeated module-based colonoscopy-training have been promoted in Italy during the last decade, which appear to have had a significant impact on quality colonoscopy metrics together with the activation of colorectal cancer screening programs.

      Keywords

      1. Introduction

      Colorectal cancer (CRC) is one of the major causes of death from cancer worldwide. In 2020, up to 43,700 new diagnoses were made in Italy and CRC remains the most frequently diagnosed cancer alongside breast cancer, according to the latest joint report of the Italian Association of Medical Oncology (AIOM) and Italian Tumor Registry (AIRTUM) [

      Associazione Italiana di Oncologia Medica. I numeri del cancro in Italia 2020 [Internet]. 2020 p. 148. Available from: https://www.aiom.it/wp-content/uploads/2020/10/2020_Numeri_Cancro-operatori_web.pdf.

      ]. The 5-year survival rate for colorectal cancer is around 90% if diagnosed early, but decreases dramatically to 13% if diagnosed later [
      • Sawicki T.
      • Ruszkowska M.
      • Danielewicz A.
      • et al.
      A review of colorectal cancer in terms of epidemiology, risk factors, development, symptoms and diagnosis.
      ]. Approximately 95% of CRC cases originate from colon adenomatous polyps [
      • Sawicki T.
      • Ruszkowska M.
      • Danielewicz A.
      • et al.
      A review of colorectal cancer in terms of epidemiology, risk factors, development, symptoms and diagnosis.
      ], and their prompt identification and removal plays a pivotal role in preventing the disease.
      Colonoscopy is considered the gold standard tool for CRC screening, and allows both identification and real-time removal of precancerous lesions. However, colonoscopy is a complex procedure requiring adequate training and experience to achieve optimal results. In order to reach this goal, it is important not only to monitor quality parameters on a daily basis, but also to establish efficient and regular training programs that should include manual and instrumental skills, as well as theoretical aspects. Training programs for both non-expert and expert colonoscopists have also been considered to play a pivotal role in the strategies of several endoscopic societies to achieve and maintain the quality of colonoscopy performance recommended by guidelines [

      The joint advisory group on GI endoscopy. Available at: www.thejag.org.uk/

      ,
      • Gavin D.R.
      • Valori R.M.
      • Anderson J.T.
      • et al.
      The national colonoscopy audit: a nationwide assessment of the quality and safety of colonoscopy in the UK.
      ,
      • May F.P.
      • Shaukat A.
      State of the science on quality indicators for colonoscopy and how to achieve them.
      ].
      Several studies, including back-to-back colonoscopies, have shown that up to 25% of adenomas can be missed during screening colonoscopy [
      • Leufkens A.M.
      • van Oijen M.G.
      • Vleggaar F.P.
      • et al.
      Factors influencing the miss rate of polyps in a back-to-back colonoscopy study.
      ,
      • Rex D.K.
      • Cutler C.S.
      • Lemmel G.T.
      • et al.
      Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies.
      ], highlighting the need to perform high quality colonoscopy with measurable indicators [
      • Rees C.J.
      • Bevan R.
      • Zimmermann-Fraedrich K.
      • et al.
      Expert opinions and scientific evidence for colonoscopy key performance indicators.
      ], since a decrease in quality is associated with an increase in the risk of interval CRC [
      • Corley D.A.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Adenoma detection rate and risk of colorectal cancer and death.
      ,
      • Kaminski M.F.
      • Regula J.
      • Kraszewska E.
      • et al.
      Quality indicators for colonoscopy and the risk of interval cancer.
      ]. The European Society of Gastrointestinal Endoscopy (ESGE) [
      • Rembacken B.
      • Hassan C.
      • Riemann J.F.
      • et al.
      Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE).
      ] has identified and recommended 9 intraprocedural colonoscopy quality indicators to encourage detailed mucosal evaluation during colonoscopy and improve overall colonoscopy performance, as have the American Society of Gastrointestinal Endoscopy (ASGE) together with the American College of Gastroenterology (ACG) [
      • Pedersen L.
      • Bernstein I.
      • Lindorff-Larsen K.
      • et al.
      Improving colonoscopy quality through individualised training programmes.
      ] task force. Among those, bowel preparation quality, cecal intubation rate, withdrawal time of the colonoscope and adenoma detection rate (ADR) are of paramount importance and have been linked to interval (post-colonoscopy) colorectal cancer incidence. Moreover, type of sedation used, severity and recording of pain, and rate of retrieval of removed lesions for histology have also been reported as quality indicators by ESGE recommendations [
      • Kaminski M.F.
      • Thomas-Gibson S.
      • Bugajski M.
      • et al.
      Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative.
      ].
      In order to monitor and improve the quality of colonoscopies in Italy, the Italian Society of Digestive Endoscopy (SIED) and Italian Association of Hospital Gastroenterologists and Endoscopists (AIGO) have conceived a project called INCIPIT (INtegrated Colonoscopy Improvement Program in ITaly), which includes a prospective observational multicenter study. Herein, we present data from the nationwide INCIPIT study to assess the current status of colonoscopy procedures in Italian centers, and to investigate factors linked to the quality of the procedure and possible advantages of a retraining policy.

      2. Methods

      2.1 Study design

      This was an observational, prospective, multicenter study conducted over a two-year period (from July 2018 to July 2020) and involved 17 hospitals with 34 endoscopists distributed throughout Italy.
      All patients enrolled in the study gave their informed consent for the procedures, for participation in the study, and for use of data for scientific purposes.
      The study protocol (Supplementary material) was firstly approved on February 2018 by the institutional Ethics Committee of the coordinating center (Register of diagnostic and therapeutic colonoscopies - HSR Reg/Col) and subsequently in all centers involved. The study was registered on Clinical Trials Gov (NCT03661099).
      The study included consecutive patients undergoing standard colonoscopy as per standard protocols in the centers involved, as follows:
      Phase 1: over an estimated 4-month period all endoscopists involved in the study performed consecutive colonoscopies (target: 150–200) and data were prospectively collected through an online electronic case report form (eCRF) and recorded in a database.
      Phase 2: retraining via an online learning platform was planned for all endoscopists. In this learning platform, experts presented and discussed current standards for quality colonoscopy, including technique for colonoscopy and reaching the cecum and other quality parameters recognized by the ESGE and ASGE [
      • Rembacken B.
      • Hassan C.
      • Riemann J.F.
      • et al.
      Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE).
      ,
      • Pedersen L.
      • Bernstein I.
      • Lindorff-Larsen K.
      • et al.
      Improving colonoscopy quality through individualised training programmes.
      ]. Only endoscopists who completed the training modules were admitted to the third phase.
      Phase 3: analogously to phase 1, data referring to all consecutive colonoscopies performed were prospectively collected using an eCRF and recorded in the database.
      The ADR and polyp detection rate (PDR) were calculated for each endoscopist.
      According to current guidelines of the ESGE, quality colonoscopy parameters assessed before and after the training period were: a) colon cleansing defined as score ≥ 6 at Boston bowel preparation scale (BBPS) assessment; b) intraprocedural pain, assessed by nurse-assessed patient comfort score (NAPCOMS); c) cecal intubation rate; d) time of instrument withdrawal; e) intra-procedural use of hyoscine N-butylbromide to distend colonic segments; f) adenoma and polyp detection rate (ADR and PDR); g) number of lesions per patient.
      ADR, PDR, and number of lesions per patient were also analyzed in relation to the number of colonoscopies performed by each endoscopist in the same session (1–5 and >6), whether the colonoscopies were performed in the morning or afternoon, and number of colonoscopies performed the year preceding the study.

      2.2 Inclusion and exclusion criteria

      To ensure a homogeneous population and limit confounding factors, the study included only patients between 50 and 75 years of age, with at least one of the following indications to perform a colonoscopy: screening (due to age or presence of fecal occult blood); post-polypectomy surveillance; presence of symptoms related to the colon but without recent alarm signs/symptoms (anemia, clinically important bowel alteration, weight loss, or asthenia).
      Patients were excluded if they showed the alarm signs or symptoms mentioned above, ASA class ≥3, colic strictures or resections, acute diverticulitis or diverticulitis episodes within the previous 6 weeks, inflammatory bowel disease, a known genetic polyposis syndrome, pregnant or breastfeeding women, severe cardiovascular disease, on anticoagulant therapy, contraindications to sedation or unable to provide informed consent, or colic melanosis.

      2.3 Data collection

      The data collected included sex, age, type of access (outpatient, day hospital, hospitalized), reason for colonoscopy, and whether the colonoscopy was performed for the first time. Data were also collected regarding the endoscopist and the procedure itself, including the above-mentioned quality indicators, complications during or immediately after the procedure, description of polyp morphology using the Paris and Kudo glandular pit pattern classifications, and histological diagnosis of resected/biopsied lesions.

      2.4 Statistical analysis

      Data were summarized using the appropriate descriptive statistics. Medians (with interquartile ranges, IQR) and percentages were used for continuous and categorical data, respectively. Multivariable logistic regression was performed to identify factors that were significantly associated with (i) the number of patients with at least one adenoma detected and (ii) proper cleansing of the right colon. Odds ratio (OR) estimates and 95% Wald confidence intervals (CI) were calculated. Analyses were performed using SAS software.

      3. Results

      All but one endoscopist initiating participating had performed >1000 colonoscopies lifelong and >150 colonoscopies per year. All endoscopists were invited to complete the training and proceed with the last phase; however, due to organizational issues within their individual centers or because some no longer practiced in the same center, only 21 completed all phases of the study. They performed a median of 622 (IQR: 400–925) coloscopies in the previous year and had a median of 10 (IQR: 5–11) years of experience. Eleven (52%) had a specialization in gastroenterology and digestive endoscopy, 7 (33%) in gastroenterology, 2 (10%) in general surgery, and 1 (5%) was a resident in gastroenterology. A total of 3504 patients met inclusion criteria and were enrolled in the study, 2314 in the first phase and 1190 in the second phase. The 4-month of duration of planned recruitment referred to single investigators (there were differences regarding the actual starting period due to different timings to receive ethics committee approvals and activate the centers). Among the 21 investigators who completed both phases, 14 begun the post-training recruitment only in January 2020. Due to the outbreak of COVID-19 in Italy, the recruitment rate dropped to near zero starting in March 2020. Since heavy difficulties in recruitment persisted even until July, we decided to complete the study despite the differences in number of patients in the first and second phase. Characteristics, access type, and indications for colonoscopy are reported in Table 1.
      Table 1Characteristics of patients.
      CharacteristicOverall N = 3504n (%)Pre-training N = 2314n (%)Post-training N = 1190n (%)
      Sex, n (%)
      • -
        Male
      • -
        Female


      1822 (52.0)

      1682 (48.0)


      1197 (51.7)

      1117 (48.3)


      625 (52.5)

      565 (47.5)
      Age (years), n (%)
      • -
        <55
      • -
        55 – 59
      • -
        60 – 64
      • -
        65 – 69
      • -
        ≥70


      690 (19.7)

      761 (21.7)

      673 (19.2)

      722 (20.6)

      658 (18.8)


      468 (20.2)

      494 (21.3)

      438 (18.9)

      471 (20.4)

      443 (19.1)


      222 (18.7)

      267 (22.4)

      235 (19.7)

      251 (21.1)

      215 (18.1)
      Access type, n (%)
      • -
        Outpatient
      • -
        Day hospital
      • -
        Hospitalized


      3446 (98.3)

      37 (1.1)

      21 (0.6)


      2268 (98.0)

      34 (1.5)

      12 (0.5)


      1178 (99.0)

      3 (0.3)

      9 (0.8)
      ASA risk, n (%)
      • -
        I: healthy patient
      • -
        II: patient with mild systemic disease but without functional limitation


      1852 (52.9)

      1652 (47.1)


      1229 (53.1)

      1085 (46.9)


      623 (52.4)

      567 (47.6)
      Patient first colonoscopy, n (%)1779 (50.8)1213 (52.4)566 (47.6)
      Colonoscopy indication
      • -
        Presence of symptoms (without alarm signs/symptoms)
      • -
        Positive for occult blood
      • -
        Opportunistic screening/spontaneous presentation
      • -
        Post-polypectomy surveillance


      893 (25.5)

      1077 (30.7)

      573 (16.4)

      961 (27.4)


      572 (24.7)

      722 (31.2)

      375 (16.2)

      645 (27.9)


      321 (27.0)

      355 (29.8)

      198 (16.6)

      316 (26.6)
      ASA= American Society of Anesthesiologists; n/a= not available.
      Low-volume PEG preparations were used in 60.1% of patients and a split-dose regimen was adopted in 71.1% of cases. Overall, a BBPS score ≥6 was obtained in 95.6% of cases (94.8% and 96.9% in the pre- and post-training phases, respectively). The mean BBPS score was 7.69 ± 1.53 (7.60 ± 1.58 and 7.85 ± 1.40 in the pre- and post-training phases, respectively). Multivariable logistic regression analysis on proper cleansing of the colon (all three BBPS segment scores ≥2) highlighted the positive effect of the use of a 1 L PEG preparation and split-dose regimens (Table 2). In the subgroup of patients treated with low-volume preparations, the fractional intake of the preparation, with the last dose taken 3–5 h before the examination, was significantly associated with better cleansing of the colon compared to administration the day before (OR 3.0, 2.0–4.8 95% CI).
      Table 2Factors associated with the cleansing of the colon (all three BBPS segment scores ≥2).
      FactorOR95% Wald CIs
      Bowel preparation (vs high volume preparation)
      1 L PEG preparation (Plenvu)4.011*1.738 - 9.254
      2 L PEG preparation + ASC (Moviprep)1.1340.827 - 1.554
      2 L PEG preparation + Bisacodyl1.5800.882 - 2.832
      2 L PEG preparation + simethicone (Clensia)1.7630.841 - 3.696
      Other0.5780.300 - 1.116
      Period of administration (vs day before exam)
      Split-dose regimen, < 3 h since last dose2.231*1.061 - 4.691
      Split-dose regimen, 3–5 h since last dose2.595*1.903 - 3.539
      Split-dose regimen, ≥ 6 h since last dose1.726*1.67- 2.792
      BBPS= Boston bowel preparation scale; OR= odds ratio; CI= confidence interval; *significant association,.
      Overall, sedation and analgesia were offered to 3038/3504 patients (86.7%), in 85.5% and 89.1% of case prior and after training. Intraprocedural pain was reported as absent or mild in 89.0% of cases and moderate to severe in 11.0% of cases. In the pre- and post-training phases, intraprocedural pain was absent and mild in 88.6% and 89.7%, respectively (Table 3).
      Table 3Distribution by severity of intra-procedural pain.
      Pain severityOverall N = 3504n (%)Pre-training N = 2314n (%)Post-training N = 1190n (%)
      None or minimal1810 (51.7)1226 (53.0)584 (49.1)
      Mild1308 (37.3)825 (35.7)483 (40.6)
      Moderate332 (9.5)223 (9.6)109 (9.2)
      Severe54 (1.5)40 (1.7)14 (1.2)
      Whether or not the cecum was reached was reported in all 3504 colonoscopies. Overall, cecal intubation was achieved in 98.0% of procedures (97.9% and 98.2% in the pre- and post-training phases, respectively).
      Withdrawal time was reported for 3433 colonoscopies. The overall rate of colonoscopies in whom the withdrawal time was ≥6 min was 88.4% (88.2% and 88.7% in the pre- and post-training phases).
      Intra-procedural hyoscine N-butylbromide was used to distend colon segments in 1.9% of patients before training and in 8.3% of patients after training (p<0.001). Curiously, stratifying by insufflation method, the change was significant only among the operators adopting CO2 insufflation (Table 4; p<0.001). Air and CO2 were used in 67.5% (2366) and 32.5% (1138) colonoscopies. The rate did not substantially change after training. CO2 usage appear to be significantly associated to both higher hyoscine N-butylbromide administration (9.9% vs 1.1%, p<0.001) and reduced pain severity (Table 4; p<0.001). Only 7 adverse events were observed (0.19%), 5 bleedings during or after polyp removal and 2 hypotensive events.
      Table 4Distribution of intra-procedural use of hyoscine N-butylbromide and pain severity according to air or CO2 insufflation method.
      CharacteristicAir insufflation N = 2366n (%)CO2 insufflation N = 1138n (%)P value
      Intra-procedural use of hyoscine N-butylbromide26 (1.1%)113 (9.9%)<0.001
       Pre-training (Air: N = 1571: CO2: N = 742)22 (1.4%)18 (2.4%)
       Post-training (Air: N = 795: CO2: N = 396)4 (0.5%)95 (24%)
      Pain severity
       None or minimal1241569 (50.0)<0.001
       Mild(52.5)478 (42.0)
       Moderate830 (35.1)80 (7.0)
       Severe252 (10.7)11 (1.0)
      43 (1.8)
      Note: The association between variables has been evaluated with Chi-squared tests.
      † Pre- and post-training differences among subgroups: P = 0.16 for air insufflation, P<0.001 for CO2 insufflation.
      Lesions were found in 49.9% of colonoscopies (50.9% and 47.9% in the pre- and post-training phases). The mean number of lesions per colonoscopy was 2.11±1.65 (2.15±1.73 and 2.02±1.49 in the pre- and post-training phases). The characteristics of lesions found are reported in Table 5.
      Table 5Characteristics of lesions in the 3504 patients.
      Characteristic
      Total lesions found, n (%)3684
      Patients with ≥1 lesion - PDR, n (%)1748 (49.9)
      Lesions per patient, median (interquartile range)2 (1 – 3)
      Adenomas found, n2576
      Patients with ≥1 adenomas, n (%)1376 (39.3)
      Adenomas per patient (in those with ≥1 adenomas), median (interquartile range)1 (1 – 2)
      Lesion location, n (%)
      • -
        Right colon - Cecum
      • -
        Right colon - Ascending
      • -
        Transverse colon - Hepatic flexure
      • -
        Transverse colon - Transverse
      • -
        Transverse colon - Splenic flexure
      • -
        Left colon - Descending
      • -
        Left colon - Sigma
      • -
        Left colon - Rectum


      447 (12.1)

      859 (23.3)

      168 (4.6)

      649 (17.6)

      54 (1.5)

      399 (10.8)

      726 (19.7)

      382 (10.4)
      Lesion size, n (%)
      • -
        <5 mm
      • -
        6–10 mm
      • -
        11–20 mm
      • -
        >20 mm


      2559 (69.5)

      805 (21.9)

      245 (6.7)

      75 (2.0)
      Lesion morphology, n (%)
      • -
        0-Ip pedunculated
      • -
        0-Isp semi-pedunculated
      • -
        0-Is sessile
      • -
        0-IIa slightly detected
      • -
        0-IIb flat
      • -
        0-IIc depressed
      • -
        0-IIa + 0-IIc depressed area in slightly raised lesion
      • -
        0-IIc + 0-IIa slightly raised area in depressed lesion
      • -
        0-III slightly excavated


      268 (7.3)

      140 (3.8)

      2490 (67.6)

      701 (19.0)

      48 (1.3)

      10 (0.3)

      16 (0.4)

      6 (0.2)

      5 (0.1)
      Laterally spreading tumor (Ø >10 mm, LST), n (%)LST subtype
      • -
        Granular, Uniform (0-IIa)
      • -
        Granular, Nodular mixed (0-IIa; 0-Is + IIa; 0-IIa + Is)
      • -
        Non-Granular Mildly Detected (0-IIa)
      • -
        Non-Granular Pseudodepressed (0-IIa + 0-IIc; 0-IIc + IIa)
      95 (2.6)

      47 (49.5)

      17 (17.9)

      17 (17.9)

      14 (14.7)
      Removed and recovered lesions, n (%)3545 (96.2)
      Dysplasia, n (% of recovered lesions)
      • -
        Absent
      • -
        Low grade
      • -
        High grade
      • -
        Indefinite


      950 (26.8)

      2363 (66.7)

      145 (4.1)

      87 (2.5)
      Typology, n (%)
      • -
        Tubular adenoma
      • -
        Villous adenoma
      • -
        Tubular-villous adenoma
      • -
        Hyperplastic
      • -
        Traditional serrated adenoma (TSA)
      • -
        Adenoma/Serrated sexile polyp (SSA/P)
      • -
        Carcinoma
      • -
        Inflammatory
      • -
        Normal mucosa
      • -
        Submucosal leiomyoma
      • -
        Adenoma (not otherwise specified)
      • -
        n/a


      2056 (58.0)

      32 (0.9)

      247 (7.0)

      625 (17.6)

      34 (1.0)

      210 (5.9)

      38 (1.1)

      28 (0.8)

      249 (7.0)

      1 (<0.1)

      1 (<0.1)

      24 (0.7)
      PDR= polyp detection rate; n/a= not available; Ø= diameter; LST= laterally spreading tumor; TSA= traditional serrated adenoma; SSA= serrated sexile adenoma.
      Overall, the median ADR was 39.1%, ranging from a minimum of 21.1% to a maximum 59.3% (IQR 31.6–43.7%). No significant differences were observed between the pre- and post-training phases (40.1% vs 36.9%; P = 0.83). Considering the ADR threshold of 30% for males and 20% for females [
      • Rex D.K.
      • Petrini J.L.
      • Baron T.H.
      • et al.
      Quality indicators for colonoscopy.
      ], 71.4% of endoscopists exceeded the thresholds. The mean number of adenomas detected per patient was 1.87±1.43 (1.90±1.46 and 1.80±1.36 in the pre- and post-training phases). In total, 80.95% (17 of 21) of endoscopists had a ADR performance above the 25% threshold identified by ESGE and ASGE guidelines. The median PDR was 47.4%, ranging from 26.3% to 73.7%. The mean number of polyps detected per patient was 2.11±1.65 (2.15±1.73 and 2.02±1.49 in the pre- and post-training phase). Removed lesions were retrieved in 96.1% of colonoscopies (96.6% and 95.1% in the pre- and post-training phases).
      The results of multivariable logistic regression analysis for the number of patients with at least one adenoma detected is reported in Table 6. The single most impactful factor was cecal intubation (OR 14.2).
      Table 6Factors associated with the number of patients with at least one adenoma detected.
      FactorOR95% Wald CIs
      Patient female sex (vs male sex)0.639*0.554 – 0.737
      Age (years) (vs <55)
      55 - 591.475*1.175 – 1.851
      60 - 641.474*1.165 – 1.865
      65 - 691.950*1.549 – 2.455
      ≥702.313*1.822 – 2.937
      No. exams (vs 1–5)
      6–101.1280.943 – 1.349
      >101.1300.718 – 1.780
      Exam done in the morning (vs in the afternoon)1.0530.869 – 1.277
      No. colonoscopies in the last year (vs 1–500)
      >5001.652*1.422 −1.919
      n/a0.8620.610 – 1.218
      No antidote used (vs antidote used)2.059*1.484 – 2.857
      Patient first colonoscopy (vs not the first colonoscopy)1.440*1.192 – 1.739
      Colonoscopy indication (vs symptoms without alarm signs)
      Positive for occult blood1.757*1.440 – 2.142
      Opportunistic screening/spontaneous presentation1.2340.974 – 1.564
      Post-polypectomy surveillance2.203*1.745 – 2.782
      Use of HD endoscope (vs non-HD endoscope)1.372*1.094 – 1.720
      Cecal intubation (vs no cecal intubation)14.184*4.427 – 45.448
      OR= odds ratio; CI= confidence interval; *significant association.

      4. Discussion

      The ESGE has identified pre-, intra-, and post-procedural colonoscopy quality indicators to improve mucosal evaluation during colonoscopy and the overall quality of colonoscopy performance. Among the intra-procedural indicators, bowel preparation quality, cecal intubation rate, withdrawal time of colonoscope, and ADR are of paramount importance and have been significantly linked to interval colorectal cancer [
      • Corley D.A.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Adenoma detection rate and risk of colorectal cancer and death.
      ,
      • Kaminski M.F.
      • Regula J.
      • Kraszewska E.
      • et al.
      Quality indicators for colonoscopy and the risk of interval cancer.
      ]. Nonetheless, how to measure and apply these colonoscopy quality indicators in daily clinical practice still remains a challenge for endoscopists. Indeed, nationwide training programs and monitoring colonoscopists’ performance is still scarce.
      The aim of the present study was to assess quality performance in colonoscopy practice in Italy, among expert endoscopists, and whether a training period could further improve performance. To the best of our knowledge, this is the largest multicenter observational study on colonoscopy diagnostic yields and quality indicators performed in Italy [
      • Frazzoni L.
      • La Marca M.
      • Radaelli F.
      • et al.
      Systematic review with meta-analysis: the appropriateness of colonoscopy increases the probability of relevant findings and cancer while reducing unnecessary exams.
      ,
      • Frazzoni L.
      • Radaelli F.
      • Spada C.
      • et al.
      The diagnostic yield of colonoscopy in hospitalized patients. An observational multicenter prospective study.
      ]. The data can be compared to those reported in a similar multicenter prospective observational study carried out in 2010 by the SIED in 28 Italian endoscopy centers including 3150 consecutive colonoscopies [
      • Ricci E.
      • Hassan C.
      • Petruzziello L.
      • et al.
      Inter-centre variability of the adenoma detection rate: a prospective, multicentre study.
      ], and to that reported in a previous Italian survey published in 2008 [
      • Radaelli F.
      • Meucci G.
      • Minoli G.
      • et al.
      Colonoscopy practice in Italy: a prospective survey on behalf of the Italian Association of Hospital Gastroenterologists.
      ].
      Inadequate bowel preparations limit colon visualization and are associated with an adenoma miss rate of up to 47.9% [
      • Chokshi R.V.
      • Hovis C.E.
      • Hollander T.
      • et al.
      Prevalence of missed adenomas in patients with inadequate bowel preparation on screening colonoscopy.
      ]. Poor quality of cleansing also leads to repeat procedures, with increased costs for the healthcare system. The BBPS is the most widely used in clinical practice due to its reliability and ease of use [
      • Heron V.
      • Parmar R.
      • Menard C.
      • et al.
      Validating bowel preparation scales.
      ]. Over 85% of colonoscopies for all indications and approximately 90% of screening colonoscopies should be rated as at least adequate (BBPS ≥6) to meet the ESGE-ASGE/ACG quality indicator goals. In two meta-analyses, split-dose bowel preparations and same-day preparations were reported to improve bowel preparation outcomes [
      • Bucci C.
      • Zingone F.
      • Schettino P.
      • et al.
      Same-day regimen as an alternative to split preparation for colonoscopy: a systematic review with meta-analysis.
      ,
      • Guo X.
      • Yang Z.
      • Zhao L.
      • et al.
      Enhanced instructions improve the quality of bowel preparation for colonoscopy: a meta-analysis of randomized controlled trials.
      ].
      Herein, adequate bowel preparation (BBPS ≥6) was reported in 95.6% of cases, with a 22% increase compared to the 78% reported 10 years ago [
      • Ricci E.
      • Hassan C.
      • Petruzziello L.
      • et al.
      Inter-centre variability of the adenoma detection rate: a prospective, multicentre study.
      ]. The current percentage of adequate bowel cleansing was above the recommended ESGE/ASGE-ACG threshold. The use of low-volume preparations (1 L) allowed for significantly better cleansing of the colon compared to high volume preparations (OR 4.0). This is in agreement with another study from Italy [
      • Maida M.
      • Sinagra E.
      • Morreale G.C.
      • et al.
      Effectiveness of very low-volume preparation for colonoscopy: a prospective, multicenter observational study.
      ]. While using low-volume preparations, the split-dose intake of the preparation (with the last dose taken 3–5 h before examination) was also associated with significantly better cleansing and was adopted in 71.1% of cases. In an Italian survey on quality indicators for colonoscopy carried out in 2016, a split-dose was routinely adopted in only 18% of centers [
      • Paggi S.
      • Amato A.
      • Anderloni A.
      • et al.
      Pre- and post-procedural quality indicators for colonoscopy: a nationwide survey.
      ]. In a comparable study which was carried out in Poland, adequate bowel preparation was seen on 91.3% of cases, which ranged from 79.2 to 99.2% among individual centers [
      • Bugajski M.
      • Rupinski M.
      • Wieszczy P.
      • et al.
      Key performance measures for colonoscopy in the Polish Colonoscopy Screening Program.
      ].
      Increased rates of adequate bowel preparation, including the adoption of a split-dose, likely reflects an increased awareness of adequate cleansing that in turn leads to better patient education about the importance of cleansing [
      • Kastenberg D.
      • Bertiger G.
      • Brogadir S.
      Bowel preparation quality scales for colonoscopy.
      ].
      High cecal intubation rates have been proven to be associated with high ADR and a lower incidence of interval cancers, providing protection from right-sided colon cancer [
      • Chaptini L.
      • Laine L.
      Can I improve my adenoma detection rate?.
      ]. The performance target reported in guidelines is at least 90% for all colonoscopies and 95% for screening colonoscopies. The reported cecal intubation rate (98%) was above the guideline threshold required for all and screening colonoscopies (≥90% and ≥95%, respectively); 10 years ago, the 93% cecal intubation rate was above the guideline threshold for all colonoscopies, too, but below that for screenings. In the 2008 survey, the cecal intubation rate was 80.7%, with a threshold of ≥90% reached in only 22.1% of colonoscopies [
      • Radaelli F.
      • Meucci G.
      • Minoli G.
      • et al.
      Colonoscopy practice in Italy: a prospective survey on behalf of the Italian Association of Hospital Gastroenterologists.
      ].
      A withdrawal time ≥6 min for diagnostic colonoscopies has been found associated with a higher detection of lesions during colonoscopy and a lower risk of interval cancers [
      • Barclay R.L.
      • Vicari J.J.
      • Doughty A.S.
      • et al.
      Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.
      ,
      • Lee A.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Endoscopist fatigue estimates and colonoscopic adenoma detection in a large community-based setting.
      ,
      • Shaukat A.
      • Rector T.S.
      • Church T.R.
      • et al.
      Longer withdrawal time is associated with a reduced incidence of interval cancer after screening colonoscopy.
      ]. In the study by Barclay et al., there was a wide difference (from 9.4% to 32.7%) in ADR depending on the duration of withdrawal (which ranged from 3.1 to 16.8 min) [
      • Barclay R.L.
      • Vicari J.J.
      • Doughty A.S.
      • et al.
      Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.
      ]. Colonoscopists with withdrawal times >6 min had higher detection of any neoplasia (28.3% vs. 11.8%). The detection of advanced neoplasia was also significantly different (6.4% vs. 2.6%). The English screening program data published in 2011 showed that withdrawal times of 10 min were associated with the best ADR [
      • Lee T.J.W.
      • Blanks R.G.
      • Rees C.J.
      Colonoscopy withdrawal time and adenoma detection rate in screening colonoscopy: the optimum average withdrawal time is 10min.
      ]; Shaukat et al. [
      • Shaukat A.
      • Rector T.S.
      • Church T.R.
      • et al.
      Longer withdrawal time is associated with a reduced incidence of interval cancer after screening colonoscopy.
      ] suggested that in presence of high ADR rates (25%) the withdrawal time rather than ADR could be a more sensitive marker of colonoscopy quality. The percentage of colonoscopies with withdrawal time ≥6 min herein was slightly inferior (88% compared with at least 90% recommended for purely diagnostic examinations).
      ADR is considered as a pivotal measure of the quality of colonoscopy performance since it correlates with interval colorectal cancer risk [
      • Kaminski M.F.
      • Regula J.
      • Kraszewska E.
      • et al.
      Quality indicators for colonoscopy and the risk of interval cancer.
      ]. The current benchmarks are 20% for women and 30% for men 50 years and older, with a blended rate of 25% [
      • Rex D.K.
      • Petrini J.L.
      • Baron T.H.
      • et al.
      Quality indicators for colonoscopy.
      ], but the ADR rate remains highly variable among endoscopists. Since ADR does not include other polypoid non-adenomatous lesions (mainly serrated ones), other parameters have been proposed to measure the quality of colonoscopy performance such as the polyp detection rate and the number of adenomas/polyps detected per colonoscopy, which have been associated with a low adenoma miss rate [
      • Zhao S.
      • Wang S.
      • Pan P.
      • et al.
      Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systematic review and meta-analysis.
      ]. However, ADR, PDR, and number of adenomas detected per colonoscopy depend on other quality parameters such as colon cleanliness, rate of cecal intubation, and withdrawal time.
      Focused training interventions have been associated with a strong trend toward increased ADRs, also among certified endoscopists. Three training studies, including 119 endoscopists, showed an improvement of ADRs (odds ratio 1.16 and 1.17 in all and screening colonoscopies), PDRs, adenocarcinoma detection, and withdrawal times after training. However, a high level of heterogeneity was reported in this systematic review [
      • Lim S.
      • Hammond S.
      • Park J.
      • et al.
      Training interventions to improve adenoma detection rates during colonoscopy: a systematic review and meta-analysis.
      ].
      In the present study the majority of endoscopists (81%) had an ADR performance above the ESGE/ASGE-ACG thresholds, with a median rate of 39.1%; in the previous multicenter Italian study carried out in 2013 [
      • Ricci E.
      • Hassan C.
      • Petruzziello L.
      • et al.
      Inter-centre variability of the adenoma detection rate: a prospective, multicentre study.
      ], the median ADR was 22% and only 64.3% of endoscopists met the ESGE/ASGE-ACG thresholds (≥25%). At that time a similar mean ADR (24.2% ± SD 11.6%) was reported by the Austrian nationwide quality control program for screening colonoscopy [
      • Waldmann E.
      • Gessl I.
      • Sallinger D.
      • et al.
      Trends in quality of screening colonoscopy in Austria.
      ].
      Over a 10-year period, the median ADR calculated for endoscopists and the percentage of endoscopists who met the ≥25% threshold increased by approximately 78% and 26%, respectively. Similarly, the current median PDR was 47.4%, with a 34% increasing rate compared to 35% median PDR reported in the previous multicenter Italian study (Fig. 1). Consistent with previous multivariable analyses [
      • Frazzoni L.
      • La Marca M.
      • Radaelli F.
      • et al.
      Systematic review with meta-analysis: the appropriateness of colonoscopy increases the probability of relevant findings and cancer while reducing unnecessary exams.
      ,
      • Frazzoni L.
      • Radaelli F.
      • Spada C.
      • et al.
      The diagnostic yield of colonoscopy in hospitalized patients. An observational multicenter prospective study.
      ,
      • Chaptini L.
      • Laine L.
      Can I improve my adenoma detection rate?.
      ], we found that older age, male gender, use of HD endoscopes, and cecal intubation are associated with an increased ADR.
      Fig. 1
      Fig. 1Comparison of adenoma detection rate (ADR), polyp detection rate (PDR), and endoscopists above the ADR 25% threshold here and in the study by Ricci et al. from 2013. Error bars represents ADR and PDR ranges among endoscopists.
      Similar improvement in the ADR has been reported by the Polish Colonoscopy Screening Program which analyzed database records for 43,277 colonoscopies, reporting a cecal intubation rate of 97.4% (range: 93.4% - 99.4%) and an ADR of 29.8% (range: 19.1% - 39.1%) [
      • Bugajski M.
      • Rupinski M.
      • Wieszczy P.
      • et al.
      Key performance measures for colonoscopy in the Polish Colonoscopy Screening Program.
      ].
      We also evaluated the potential influence of the number of exams performed during the day and the periods of the day on ADR to explore whether the endoscopist fatigue could impact the quality of the procedure. One study found that an increase in the number of hours during which endoscopies were performed before the index colonoscopy negatively affects ADR [
      • Almadi M.A.
      • Sewitch M.
      • Barkun A.N.
      • et al.
      Adenoma detection rates decline with increasing procedural hours in an endoscopist's workload.
      ], while another did not find any evidence that time of day or number of procedures performed before the colonoscopy may decrease ADR [
      • Lee A.
      • Jensen C.D.
      • Marks A.R.
      • et al.
      Endoscopist fatigue estimates and colonoscopic adenoma detection in a large community-based setting.
      ]. In our study, we found an association between increased ADR and more than 500 colonoscopies performed in the previous year, but with no effect of the time of day or number of exams performed in the day. However, confidence intervals were too broad to draw any meaningful conclusions, and more studies with larger sample sizes are needed.
      We cannot compare other parameters such as intra-procedural pain assessment, withdrawal time, use of hyoscine N-butylbromide, and percentage of removed lesions retrieved for histology with previous Italian multicenter studies because these were not previously assessed.
      Although there is general agreement that retraining has a favorable impact on ADR and other metrics in colonoscopy practice, even among expert endoscopists [
      • Pedersen L.
      • Bernstein I.
      • Lindorff-Larsen K.
      • et al.
      Improving colonoscopy quality through individualised training programmes.
      ,
      • Kaminski M.F.
      • Anderson J.
      • Valori R.
      • et al.
      Leadership training to improve adenoma detection rate in screening colonoscopy: a randomised trial.
      ,
      • Khan R.
      • Zheng E.
      • Wani S.B.
      • et al.
      Colonoscopy competence assessment tools: a systematic review of validity evidence.
      ], considered the planned training period between the two phases of the study only use of hyoscine N-butylbromide showed a significant increase. This could be explained by the high colonoscopy quality standards that are already achieved by the Italian hospitals involved in this study. Among those below the 30% ADR threshold, on the other hand, 4 of 5 investigators improved after training, although the difference was not statistically significant. Quality improvement initiatives and repeated module-based colonoscopy-training developed for junior and certified endoscopists have been promoted in Italy during the last decade, stimulated by the activation of colorectal cancer screening programs, which appear to have had a significant impact on quality colonoscopy metrics and allowed achieving almost all quality parameters recommended by the ESGE, ASGE, and ACG. Awareness of quality metrics among individual and endoscopy practices and patients very likely played a pivotal role in this improvement.

      Declaration of Competing Interest

      None to declare.

      Funding

      The study was promoted by the Italian Society of Digestive Endoscopy (SIED) and the Italian Association of Hospital Gastroenterologists and Endoscopists (AIGO) and was unconditionally supported by Norgine Italia Srl.

      Acknowledgments

      The authors thank Matteo Mucchetti of Health Publishing & Services Srl for project coordination and Patrick Moore who provided medical writing assistance on behalf of Health Publishing & Services Srl. This unconditional support was provided by Norgine Italia Srl.

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