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Background: A small percentage of incomplete optical colonoscopies (OCs) are the result of an obstructing tumor. According to current guidelines, CT colonography (CTC) is performed to prevent missing a synchronous tumor. The aim of this study was to evaluate how frequently a synchronous tumor was found on CTC and how often this led to a change in the surgical plan. Methods: In this retrospective study, a total of 267 patients underwent CTC after an incomplete OC as a result of an obstructing colorectal carcinoma (CRC). Among them, 210 patients undergoing surgery met the inclusion criteria and were included in the analysis. The OC report, CTC report and surgical report of these patients were retrospectively evaluated for the presence of synchronous tumors using surgery and post-operative colonoscopy as the gold standard. Results: Six of the 210 patients (2.9%) showed signs of a synchronous CRC proximal to the obstructing tumor on CTC. In three of these patients, a synchronous CRC was conﬁrmed during surgery. All these tumors caused a change in the surgical plan. Three out of the six tumors found on CTC were found to be large, non-malignant polyps. All these polyps were located in the same segment as the obstructing tumor and therefore did not alter the surgical plan. Conclusion: In patients with obstructing CRC, the frequency of synchronous CRCs proximal to this lesion is low. Performing a CTC leads to a change in surgical plan based on the presence of these synchronous tumors in 1.4% of the cases. CTC should be employed as a one-stop shop in patients with an obstructing CRC. Key words: CT colonography; optical colonoscopy; colorectal carcinoma; synchronous tumor; pre-operative evaluation Submitted: 22 November 2017; Revised: 20 December 2017; Accepted: 26 December 2017 V C The Author(s) 2018. Published by Oxford University Press and Sixth Afﬁliated Hospital of Sun Yat-Sen University This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Downloaded from https://academic.oup.com/gastro/article-abstract/6/3/210/4850983 by Ed 'DeepDyve' Gillespie user on 22 August 2018 CT colonography for obstructing colorectal cancer | 211 TM Marker (GI supply). A CRC was considered to be obstructing if Introduction the colonoscope was unable to pass the lesion. If the colono- Worldwide, colorectal carcinoma (CRC) is the third most com- scope was able to pass the lesion but could not reach cecal intu- mon cancer in men and the second in women . Optical (endo- bation, it was also excluded from this study. All colonoscopies scopic) colonoscopy (OC) is currently the gold standard for the were performed by experienced gastroenterologists or special- detection of CRCs. However, 10–13% of all colonoscopies are in- ized nurses supervised by these gastroenterologists. complete [2,3]. These colonoscopies are predominantly incom- plete due to looping of the colon, decreased colon mobility or CTC protocol poor bowel preparation. Only 7% of the incomplete colonosco- pies are the result of an obstructing tumor . In all patients, bowel preparation consisted of a low-fiber diet In patients who have an incomplete OC due to an obstructing for 48 hours, with 150 mL magnesium citrate in the morning CRC, the presence of a synchronous tumor should be excluded. and Bisocadyl 10 mg in the morning as well as in the evening on Large population-based studies show that close to 4% of all CRC the day before CTC was performed. Fecal tagging was performed patients have synchronous colorectal tumors [4,5]. Of these syn- with Barium Sulphate, which was ingested the evening before chronous tumors, 34–46% are located in a different surgical seg- the examination. The CTC was performed by trained techni- ment than the index tumor [4,5]. In general, these synchronous cians on a 64-MDCT (Brilliance 64, Philips Healthcare, Best, The tumors are significantly smaller than solitary tumors and index Netherlands) or on 128 MDCT (Somatom, Siemens, Erlangen, tumors . As a result of the high accuracy of computed tomogra- Germany), imaging in both supine and prone positions. Colonic phy colonography (CTC) for both CRC and large polyps [7–9], the distension was reached by administering 1 mL scopolamine bu- European Society of Gastrointestinal Endoscopy (ESGE) and tyl 20 mg/mL or, when this was contraindicated, 1 mL glucagon European Society of Gastrointestinal and Abdominal Radiology 1 mg/mL intravenously and subsequently automated low- (ESGAR) recommend to perform a CTC after an incomplete colo- pressure delivery of carbon dioxide by a colon insufflator noscopy resulting from an obstructing CRC . device (PROTOCO2L, E-Z-EM). Intravenous contrast (120 mL In this study, we examined the added value of performing a Omnipaque 300 mg/mL) was administered, allowing evaluation CTC in patients with an incomplete colonoscopy resulting from of distant metastases. The supine scan was made in portal ve- an obstructing CRC, by calculating the frequency of synchro- nous phase. Imaging data were reviewed by one of four trained nous tumors and by evaluating how frequently performing a radiologists on a dedicated 3D workstation (Extended Brilliance CTC led to a change of the surgical plan. Workspace 3.0 or 4.0, Philips Healthcare; Best, The Netherlands) using a 3D analysis with endoview, filet view and computer- assisted detection (CAD), in addition to the traditional 2D Materials and methods images. This retrospective observational cohort study was performed in VieCuri Medical Centre, Venlo, The Netherlands—a large non- Pre-operative imaging academic hospital. The study was approved by the institutional Patients who had an incomplete OC resulting from an obstruct- ethical committees. ing tumor were preoperatively analysed in the following week. In case the tumor was located in the colon, a chest X-ray and a Patients contrast-enhanced CTC were performed. In case the tumor was Between January 2007 and February 2017, a total of 267 patients located in the rectum, an MRI of the rectum for local staging underwent CTC because they had a histopathologically proven was added. If the gastroenterologist was certain the tumor was obstructing CRC on OC. Fifty-seven patients who did not un- located in the cecum or ascending colon (including hepatic flex- dergo surgical resection were excluded from this study, as it ure), no additional CTC was performed, as it would not change was impossible to confirm or exclude the presence of a synchro- the surgical procedure. If the gastroenterologist was not certain nous tumor in these patients. Most of these patients did not un- whether the tumor was located in the right hemicolon, a CTC dergo surgical resection as a result of present metastases at the was performed preoperatively to verify tumor localization. time of diagnosis. The remaining 210 patients were all included in this study. Statistical analyses If CTC showed a synchronous tumor that was missed on OC as OC protocol a result of an obstructing CRC, either surgery or post-operative Bowel preparation consisted of a low-fiber diet for 72 hours, colonoscopy was performed to confirm the presence of a syn- with Bisocadyl 10 mg in the morning and one sachet of chronous tumor. A change in the primary surgical plan was de- Picoprep (Sodium picosulfate; Magnesium oxide; Citric acid, fined as a surgical procedure other than the one that would Ferring B.V.) in the evening before OC. In addition, the patient have been performed for the obstructing CRC only. Descriptive consumed 2 liters of clear liquid. Another sachet of Picoprep statistics were performed using Statistical Package of Social was taken 4 hours prior to the OC and another 2 liters of clear Sciences version 22.0 (SPSS). liquid was taken 3 hours before the examination. Klean-Prep (Polyethylene Glycol and Electrolytes, Norgine B.V.) was used in- Results stead of Picoprep if the patient had a kreatinine clearance <30 mmol/L. Patients were sedated with Fentanyl 0.1 mg/2 mL or A total of 210 patients met the in- and exclusion criteria. Mean Midazolam 5 mg/1 mL until conscious sedation was reached. age of the patients was 73 years (range, 38–99 years) and 50.0% Colonic distension was obtained by inflating the bowel with car- were male (n ¼ 105). bon dioxide. Once a lesion suspected of being a carcinoma was CTC was unable to evaluate the colon proximal to an ob- identified, biopsies were taken for histopathological examina- structing tumor in 10 cases (4.8%). This resulted mainly from an tion and the lesions were marked with a Spot Endoscopic inability to insufflate the colon proximal to a pinpoint stenosis. Downloaded from https://academic.oup.com/gastro/article-abstract/6/3/210/4850983 by Ed 'DeepDyve' Gillespie user on 22 August 2018 212 | Tom Offermans et al. In 2 of these 10 patients, a right hemicolectomy was performed because the obstructing tumor was located in the right hemico- lon. In four of these patients, post-operative colonoscopy did not show signs of a tumor proximal to the anastomosis. The other four patients did not receive post-operative colonoscopy because the patient was diagnosed with distant metastases, be- cause the patient deceased or because of non-adherence. In 49 out of 210 cases (23.3%), CTC was able to evaluate the colon proximal to an obstructing tumor but CTC quality was suboptimal. This was caused by inadequate bowel distension (n ¼ 20), fecal contamination (n ¼ 19) or a combination of both (n ¼ 10). Twenty-two of the 49 patients did not undergo a post- operative colonoscopy, mainly because, in these patients, the tumor had already metastasized. In 27 of these 49 cases, a post- operative colonoscopy was performed. In one of these cases, a tumor proximal to the obstructing lesion was found on post-op- erative OC that pre-operative CTC did not locate. This patient had an obstructing sigmoid tumor (pT4N0). As CTC could not lo- cate the synchronous tumor preoperatively in this patient, a sigmoidectomy was performed. At post-operative colonoscopy (9 months later), a second tumor in the ascending colon (pT3N0) was found. Based on this finding, a subtotal colectomy was performed. In 151 of the 210 patients (71.9%), CTC quality was optimal. In 88 of these 151 cases, a post-operative colonoscopy was per- formed. None of these patients had a synchronous tumor that Figure 1. A patient who underwent optical colonoscopy was found to have an was not located on CTC. Sixty-three patients did not undergo obstructing T4 tumor in the sigmoid colon. A CT colonography that was per- post-operative colonoscopy. This occurred mainly because the formed to rule out synchronous tumors proximal to the obstructing tumor patient was diagnosed with metastases, because the patient de- showed a synchronous tumor in the hepatic ﬂexure. Based on this information, ceased or because the follow-up time after surgery was less a subtotal colectomy was performed. Surgery conﬁrmed the presence of a syn- than 12 months. chronous tumor in the hepatic ﬂexure. According to surgery, the obstructing tumors were located in the rectum (n ¼ 21), sigmoid colon (including rectosigmoid junc- tion) (n¼106), descending colon (including splenic flexure) 1.4% of the cases. Although the prevalence of synchronous tu- (n¼25), transverse colon (n¼12), ascending colon (including he- mors proximal to an obstructing tumor is low, pre-operative de- patic flexure) and cecum (n¼46). There were 14 synchronous tection of synchronous tumors is essential, as it prevents CRCs present in these 210 patients (6.7%). CTC located all but secondary surgery and simultaneously might prevent develop- one of these synchronous tumors. Ten out of these 14 CRCs ment to an advanced stage of the synchronous tumor. In the were distal to the obstructing CRC and were also shown on OC. Netherlands, the number of newly diagnosed patients with co- Six patients (2.9%) showed signs of a synchronous CRC prox- lorectal cancer was 15 273 in 2016 . Approximately 16% of imal to the obstructing tumor on CTC. In three of these patients these tumors are obstructing . If we extrapolate our findings, (1.4%), a synchronous CRC was confirmed during surgery. These secondary surgery could have been prevented in 34 patients CRCs were located in a different surgical segment as the ob- during that year. Furthermore, CTC could delay the post-opera- structing carcinoma, and thus changed the surgical plan tive interval of performing an OC. Current guidelines recom- (Figure 1). In three out of six tumors found on CTC (1.4%), the tu- mend performing a post-operative OC 3 months after resection mors turned out to be large non-malignant polyps of respec- to exclude the presence of synchronous tumors . In our tively 2, 2 and 3 cm instead of CRCs. These polyps were located study, the colon was already optimally visualized proximal to in the same surgical segment as the obstructing CRC and did the obstructing tumor in 71.9% of the cases. In these cases, due not alter the surgical plan. A summary of the characteristics of to the high negative predictive value of CTC for synchronous ad- all synchronous tumors proximal to an obstructing CRCs can be vanced neoplasia , performing an OC could be delayed to 12 found in Table 1. months after resection. Fifteen out of 210 patients had 23 advanced polyps (polyps We found that, in 1.4% of the cases, CTC caused a change in >10 mm) proximal to the obstructing tumor on CTC. Nine out of the primary surgical plan as a result of the presence of a syn- these 15 patients underwent post-operative surveillance colo- chronous carcinoma proximal to the obstructing tumor, com- noscopy (60%). The mean time between surgery and postsurgi- pared to 1.9–6.7% found in previous studies [14–16]. This cal colonoscopy was 7 months (range 1–12 months). None of relatively low percentage compared to other studies can be ex- these polyps was found to be malignant during post-operative plained by variance due to the low prevalence of synchronous colonoscopy or following surgical resection. All of the polyps tumors combined with the small sample sizes in all studies. could be endoscopically removed. Furthermore, in our study, 45 patients with an obstructing tu- mor in the cecum and ascending colon were included. Finding a synchronous tumor proximal to this obstructing tumor would Discussion never lead to a change in the surgical plan based on this finding, In our study, the pre-operative identification of synchronous as a right hemicolectomy would be performed either way. CRCs by CTC caused a change in the primary surgical plan in These patients underwent CTC because tumor localization of Downloaded from https://academic.oup.com/gastro/article-abstract/6/3/210/4850983 by Ed 'DeepDyve' Gillespie user on 22 August 2018 CT colonography for obstructing colorectal cancer | 213 Table 1. Characteristics of synchronous tumors found on CT colonography Tumor Localization of Localization of TNM stage of TNM stage of Modification Type of surgery number obstructing synchronous obstructing synchronous of surgical performed tumor tumor tumor tumor plan #1 Sigmoid colon Cecum T3N0 T1N0 Yes Sigmoid resection and ileocecal resection #2 Sigmoid colon Hepatic ﬂexure T4N1 T2N0 Yes Subtotal colectomy #3 Sigmoid colon Descending colon T4N1 T2N1 Yes Extended left-sided hemi colectomy #4 Rectum Sigmoid colon T3N0 Advanced adenoma 2 cm No Low anterior resection #5 Hepatic ﬂexure Cecum T3N0 Advanced adenoma 3 cm No Right-sided hemi colectomy #6 Rectum Sigmoid colon T3N0 Advanced adenoma 2 cm No Low anterior resection the obstructing tumor was uncertain on OC, which is a known synchronous tumors in 1.4% of the cases. The added clinical flaw of OC . value of performing CTC preoperatively, however, does not only Three patients in our study were found to have a large lesion lie within the ability of CTC to find a synchronous tumor; pre- at CTC, which was interpreted as malignancy but turned out to operative evaluation of the colon also grants the surgeon the be a large non-malignant adenoma instead. CTC has a limited ability to evaluate the length and quality of the colon and the capability in differentiating advanced adenomas from CRCs . ability to better localize the tumor(s) preoperatively. For these In addition, the sensitivity and specificity of CTC might be lower reasons, CTC should be employed as a one-stop shop in patients in obstructing CRC due to inadequate bowel distension and fe- with obstructing CRC. cal contamination (in our study, 28.1% of the CTCs had subopti- mal or poor quality) . This might lead to unnecessary Conflict of interest statement: none declared. resections, as most polyps can be endoscopically removed [18,19]. On the other hand, when a polyp cannot be removed en- References doscopically, secondary surgery is needed . If there is any 1. GLOBACAN 2012: Estimated Cancer Incidence, Mortality and doubt on CTC whether a lesion is a CRC or a large polyp, an in- Prevalence Worldwide in 2012. http://globocan.iarc.fr (21 tra-operative OC can be performed. April 2017, date last accessed). When a CRC is detected, a contrast-enhanced CT abdomen 2. Shah HA, Paszat LF, Saskin R et al. Factors associated with in- is usually performed to exclude metastases. Huisman et al. complete colonoscopy: a population-based study. found in their study that two out of three synchronous tumors Gastroenterology 2007;132:2297–303. found on CTC were also visible on conventional staging CT ab- 3. Aslinia F, Uradomo L, Steele A et al. Quality assessment of domen . 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Gastroenterology Report – Oxford University Press
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