Validation of the Computed Assessment of Cleansing Score With

ORIGINAL PAPERS

Validation of the computed assessment of cleansing score with the Mirocam® system Ana Ponte, Rolando Pinho, Adélia Rodrigues, Joana Silva, Jaime Rodrigues and João Carvalho Department of Gastroenterology. Centro Hospitalar Vila Nova de Gaia/Espinho. Gaia, Portugal

ABSTRACT agement of patients with suspected small-bowel diseases, including obscure gastrointestinal bleeding (OGIB), Background and aims: A computed assessment of cleans- Crohn’s disease, small-bowel tumors, polyposis syndromes ing (CAC) score was developed to objectively evaluate small-bowel cleansing in the PillCam capsule endoscopy (CE) system and to and celiac disease (1,7-11). Although previous studies overcome the subjectivity and complexity of previous scoring sys- report a higher diagnostic yield compared with other meth- tems. Our study aimed to adapt the CAC score to the Mirocam® ods including push enteroscopy, radiologic procedures or system, evaluate its reliability with the Mirocam® CE system and angiography, CE has some limitations (5-7,12-16). Two compare it with three validated subjective grading scales. factors which negatively impair the diagnostic yield of CE Patients and methods: Thirty CE were prospectively and independently reviewed by two authors who classified the degree of are the presence of intestinal debris and air bubbles and small-bowel cleanliness according to a quantitative index, a qualita- the failure to complete an entire small-bowel examination tive evaluation and an overall adequacy assessment. The authors (2,11,17,18). The evaluation of the quality of small-bowel were blinded for the CAC score of each CE, which was calculated cleansing is necessary to assess the reliability of the find- as ([mean intensity of the red channel]/[mean intensity of the green channel] - 1) x 10. The mean intensities of the red and green ings in CE (8,17). Moreover, a consensus regarding the channels of the small-bowel segment of the “Map View” bar in the need for intestinal preparation for CE remains to be estab- Miroview Client® were determined using the histogram option of lished (9,15,18). The presence of multiple grading scales two photo-editing software. for small-bowel preparation in CE which are time-con- Results: There was a strong agreement between both CE read- suming and complicated contributes to the difficulty in ers for each of the three subjective scales used. The reproducibility of the CAC score was excellent and identical results were obtained comparing different small-bowel cleansing regimens and with the two photo-editing software. Regarding the comparison to apply them to clinical practice (9,17). Furthermore, between the CAC score and the subjective scales, there was a most of them are not validated and are based on subjective moderate-to-good agreement with the quantitative index, qualitative parameters (9-11,14,17-21). Van Weyenberg et al. devel- evaluation and overall adequacy assessment. oped a computed assessment of the cleansing (CAC) score, Conclusions: CAC score represents an objective and feasible score in the assessment of small-bowel cleansing in the Mirocam® based on objective measurements of color intensities in CE system, and could be used per se or as part of a more com- red and green channels of the tissue color bar in the Rapid prehensive score. Reader® of the PillCam® CE system (PillCam, Medtronic plc. Dublin, Ireland), thus avoiding subjectivity (17). The Key words: Capsule endoscopy. Small-bowel cleansing scales. authors hypothesized that if the tissue color bar, which comprises the summary of all CE images, was converted to the red-green-blue mode (RGB), the ratio between the INTRODUCTION mean intensity of the red and green channels could be used as a measure of enteric cleanliness. Therefore, areas of Capsule endoscopy (CE) was developed in 2001 and adequate mucosal visibility should be associated with high represents a safe and non-invasive diagnostic procedure values of red intensity and low values of green intensity. which allows complete small-bowel mucosal assessment Conversely, areas with high amounts of intestinal debris and guides further diagnostic and therapeutic approach- should be associated with low values of red intensity and es (1-6). Currently, CE has an essential role in the man- high values of green intensity (17). The aims of this study were to adapt the CAC score (17) ® Ana Ponte and Rolando Pinho contributed equally to the manuscript. to the Mirocam system (Mirocam, IntroMedic, Seoul,

Received: 11-04-2016 Accepted: 18-07-2016 Ponte A, Pinho R, Rodrigues A, Silva J, Rodrigues J, Carvalho J. Validation Correspondence: Ana Ponte. Department of Gastroenterology. Centro Hos- of the computed assessment of cleansing score with the Mirocam® system. pitalar Vila Nova de Gaia/Espinho. Rua Conceiçao Fernandes. 4434-502 Rev Esp Enferm Dig 2016;108(11):709-715. Gaia, Portugal DOI: 10.17235/reed.2016.4366/2016 e-mail: [email protected] 710 A. PONTE ET AL. Rev Esp Enferm Dig

Korea), to evaluate its reliability with the Mirocam® CE images recorded by the CE. Although this bar can be zoomed, without system and to compare this automated scale with three zoom the bar is similar to the tissue color bar in the Rapid Reader® in previously validated subjective grading scales (8). the PillCam® CE system (PillCam, Medtronic plc. Dublin, Ireland). The small-bowel in the Map View bar is automatically circumscribed by a blue line according to the images previously marked as the first PATIENTS AND METHODS duodenal and cecal images. An image of the Map View bar was created using free open source software (ShareX®, available at http:// Capsule endoscopies getsharex.com) (Fig. 1A). The resulting image was imported into 2 photo editing software (proprietary software, Photoshop® [Photoshop CS2, version 9.0.2, Adobe Systems Inc., San Jose, California, USA], Capsule endoscopies were included in the study if the patients and free open source software, GIMP®, [GNU Image Manipulation were above 18 years old and the capsule reached the cecum within Program, available at https://www.gimp.org/]). The images were the recording time. Patients with diabetes mellitus, thyroid patholo- cropped using both softwares to include only the segment corre- gy or taking drugs known to interfere with gastrointestinal motility sponding to the small-bowel. The histogram function of Photoshop® were excluded from the study. Furthermore, patients with active and GIMP® was then used to measure the mean intensity value of the bleeding confirmed during CE were also excluded from this study. green and red channels (Fig. 1B). These values were entered into the All patients gave informed consent for the CE examination. Thirty database and the computer scores were determined according to the capsule endoscopies fulfilling the inclusion and exclusion criteria, formula published by Weyenberg et al. (17): ([mean intensity of the performed between November 2014 and June 2015, were selected red channel]/[mean intensity of the green channel] - 1) x 10 for both consecutively. Photoshop® (P-CAC) and GIMP® (G-CAC). All CE were performed at the same center using the Mirocam® CE system (Mirocam, IntroMedic, Seoul, Korea). This CE records images at a rate of 3 frames per second (fps) that are transmitted through human body communication technology to an external Statistical analysis recorder. The CE protocol consists of capsule ingestion with a glass Descriptive results are presented as percentages, means and stan- of water at 8 a.m. after an overnight fast without prior bowel prepa- dard deviation of the mean. The correlation between the computer ration, real-time views at 1 h and 2 h post-ingestion, administration scores obtained with Photoshop® and GIMP® and between the com- of 10 mg metoclopramide if the capsule remains in the stomach after puter scores and the 10 points QI was performed using Spearman’s 2 h, light diet 4h after capsule ingestion, and normal daily activities correlation coefficient. The computer scores and the 4 grades QE on an outpatient basis during the day; the recorder is removed 12 h were compared using the intra-class correlation coefficient (ICC). after capsule ingestion (or earlier, if real-time viewing confirms that The computer scores were compared according to the OAA using the capsule has already reached the colon). Student’s t test. All CE were reviewed by two authors (AP, RP) who confirmed The level of agreement between both readers was evaluated using the first duodenal image and the first cecal image. All remaining the ICC for the QI and the QE and the unweighted kappa test for findings were deleted from the CE videos. The resulting video files the OAA. were saved and numbered with sequential numbers ranging from 1 to 30. A dedicated database including the number of the CE, age and sex of the patient, the indication for CE and fields for the subjective scales and the computer scores was created.

A Subjective scales

All CE videos were reviewed independently by two authors (AP, RP) at a fixed rate of 40 fps, in Single View (Miroview Client®), with the purpose of grading the level of cleanliness according to 3 subjective grading scales previously described (8): a) quantitative index (QI), which grades the level of cleanliness with a score ranging from 0 to 10; b) qualitative evaluation (QE), which grades the degree of cleanliness as excellent, good, fair and poor; and c) overall adequacy assessment (OAA), which is simply graded as adequate or inadequate. Both readers were blinded to the results of the CAC score.

Computed assessment of cleansing score B

Besides Single View, Dual View and Quad View, the Mirocam® Fig 1. A. Image depicting the print screen of the entire tissue color bar reading software (Miroview Client®) has another function named of the Map View. B. Histogram function of GIMP® used to measure the Map View which displays a bar containing a representation of all mean intensity value of the green and red channels of the small bowel segment of the tissue color bar.

Rev Esp Enferm Dig 2016;108(11):709-715 2016, Vol. 108, N.º 11 VALIDATION OF THE COMPUTED ASSESSMENT OF CLEANSING SCORE WITH THE MIROCAM® SYSTEM 711

Results were considered to be significant when p < 0.05. The Quantitative index Statistical Package for Social Sciences version 20.0 (IBM Corp., Armonk, New York, USA) was used for data entry and data anal- The mean grade for the QI was 7.47 (±1.74) for read- ysis. er 1 and 7.9 (±1.67) for reader 2 (Table II). An excellent inter-reader reliability with an ICC of 0.92 (CI 95% = 0.84- 0.96) was found. RESULTS A good correlation between the QI and the computed scores was found with a Spearman’s Rho of 0.5, p = 0.005 The 30 CE videos referred to 30 patients, 66.7% males for reader 1; 0.48, p = 0.008 for reader 2; and 0.49, p = with a mean age of 49.3 (± 17) years old. The main indi- 0.006 for the mean of both readers using P-CAC, and 0.49, cations for CE were OGIB and suspected Crohn’s disease p = 0.006 for reader 1; 0.47, p = 0.009 for reader 2 and (Table I). The mean small-bowel transit time was 272.2 0.49, p = 0.007 for the mean of both readers using G-CAC (±71.3) minutes. (Fig. 2).

CAC scores Qualitative evaluation

The mean value of the CAC score was 4.93 (±1.36) The scores obtained with the QE scale are detailed in using Photoshop® and 4.95 (±1.36) using GIMP®. An table III. An excellent concordance between both readers excellent correlation between the 2 scores was found with with an ICC of 0.83 (CI 95% = 0.68-0.91) was found. a Spearman’s Rho of 1.00, p < 0.001. A fair correlation between QE and the computed scores was found with an ICC of 0.43 (CI 95% = 0.089-0.68, p = 0.008) for reader 1 and 0.45 (CI 95% = 0.11-0.70, p = 0.006) for reader 2 using P-CAC and 0.43 (CI 95% = Table I. Demographic data of patients and indications 0.088-0.68, p = 0.008) and 0.45 (CI95% = 0.11-0.69, p = for capsule endoscopy performance 0.008), respectively, using G-CAC. Demographic data No. (%) Male/Female 20 (66.7)/10 (33.3) Overall adequacy assessment Mean age +/- S.D. (years) 49.3 +/- 17 Indication for CE No. (%) The degree of cleanliness was considered as adequate in OOGIB - Anemia 14 (46.7) 86.7% of cases by reader 1 and 90% of cases by reader 2. An excellent inter-reader reliability was found, with an Suspected Crohn’s disease 13 (43.3) unweighted kappa of 0.84. The mean values of P-CAC for Abdominal pain 2 (6.7) adequate/inadequate levels of cleanliness were 5.16/3.45 OOGIB - positive FOBT 1 (3.3) (p = 0.02) for reader 1 and 5.07/3.66 for reader 2 (p = 0.09); the mean values for G-CAC were 5.18/3.47 (p = CE: Capsule endoscopy; OOGIB: Occult obscure gastrointestinal bleeding; FOBT: fecal occult blood test. 0.02) and 5.09/3.68 (p = 0.09), respectively (Fig. 3).

Table II. Results of the 10-point quantitative scale for the evaluation of the small bowel cleansing according to reader 1 and reader 2 Reader 1 (No. [%]) 3 4 5 6 7 8 9 10 Total 4 1 0 0 0 0 0 0 0 1 (3.3) 5 0 1 0 1 0 0 0 0 2 (6.7) 6 0 0 2 0 1 0 0 0 3 (10) 7 0 0 0 2 2 1 0 0 5 (16.7) Reader 2 (No. [%]) 8 0 0 0 0 3 4 0 0 7 (23.3) 9 0 0 0 0 0 5 1 0 6 (20) 10 0 0 0 0 0 0 2 4 6 (20) Total 1 (3.3) 1 (3.3) 2 (6.7) 3 (10) 6 (20) 10 (33.3) 3 (10) 4 (13.3) 30

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Fig 2. Correlation between computed assessment of cleansing (Y-axis) score using Photoshop® (P-CAC) and GIMP® (G-CAC) and the quantitative index (QI) for reader 1, reader 2 and the mean of both readers (x-axis). The outer lines correspond to the 95% confidence interval.

Table III. Scores obtained for qualitative evaluation for each reader Reader 1 (No. [%]) Poor Fair Good Excellent Total Poor 2 1 0 0 3 (10) Fair 0 5 2 0 7 (23.3) Reader 2 (No. [%]) Good 0 2 12 0 14 (46.7) Excellent 0 0 2 4 6 (20) Total 2 (6.7) 8 (26.7) 16 (53.3) 4 (13.3) 30

DISCUSSION order to prevent missing lesions and the need to repeat CE, which may occur in up to 33% of the cases (8,10,20,22). CE is a safe, non-invasive and extremely valuable tool Currently, the bowel preparation method recommend- in the diagnosis of small-bowel pathologies (9). Neverthe- ed for CE consists of a clear liquids diet and a 12-hour less, the quality of mucosal visualization and the diagnostic fast (2,7,8,10,11,13,14,19,24,25). This recommendation yield of CE may be impaired due to incomplete exam- probably resulted from the experience with push enteros- ination and poor intestinal preparation with air bubbles, copy, which evaluates the proximal small-bowel usually bile, intraluminal fluid and debris (2,7,9,15,19,21,22). 80-120 cm beyond the ligament of Treitz (7,26). Nev- Moreover, CE is time consuming and expensive and has ertheless, using this approach, the quality of CE images inherent limitations including uncontrolled movements, is affected in up to 30% of cases with residual intestinal unidirectional field of view, incapability of air inflation, contents, mainly in the distal part of the small-bowel, thus fluid suction or washing of the small-bowel mucosa limiting mucosal visualization and possibly the diagnos- (3,8,10,14,20-23). Therefore, it is essential to optimize tic yield (5,11,13,14,21,25). As an adequate preparation intestinal preparation to improve mucosal assessment in improves adequacy of mucosal assessment, many stud-

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Fig 3. Box plot graphics showing the relation between the computed assessment of cleansing score (y-axis) using Photoshop® (P-CAC) and GIMP® (G-CAC) and the overall adequacy assessment (OAA) for readers 1 and 2 (x-axis). ies have focused on the ideal approach to clean the small lack of consensus regarding the optimal small bowel intestine before CE (5,7,10-15,18,19,21,25). Several bow- cleansing method (9). Currently, a validated scale that el preparation methods have been described, namely the is universally accepted for grading small-bowel cleans- use of purgatives including polyethylene glycol, sodium ing is lacking. Moreover, most of them are based on phosphate, magnesium citrate or mannitol; simethicone; subjective parameters (9,10,11,14,17-21). Weyenberg or prokinetics (8,9,15,17,27). Due to the heterogeneity developed and validated a computed quantitative score of protocols regarding the type of preparation, dosage for the PillCam® CE system, based on objective mea- and time of administration, results are conflicting and surements of color intensities in red and green channels a consensus regarding the efficacy, tolerability and best of the tissue color bar of CE, therefore avoiding subjec- approach for intestinal cleansing before CE is lacking tivity (17). Furthermore, the authors suggested that the (7,9,10,12,14,15,18,19,21). Nevertheless, small-bowel incorporation of this score into the CE reading software preparation before CE seems to improve the quality of would result in a fully automated score, as the manual visualization of the mucosa and the diagnostic yield, with- selection of the tissue color bar segments and analysis in out any difference regarding CE completion rate, gastric a photo-editing software would be redundant (17). This transit time and small-bowel transit time (2,27). aspect would overcome all the disadvantages of the pre- The absence of a standardized grading scale for vious scoring systems, namely subjectivity, complexity small-bowel preparation in CE also contributes to the and lengthiness. Taking into account all the advantages

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