Gastroenterology & Hepatology

August 2017 - Volume 13, Issue 8

Approach to Incomplete Colonoscopy: New Techniques and Technologies

Diana L. Franco, MD, Jonathan A. Leighton, MD, and Suryakanth R. Gurudu, MD

Dr Franco is a gastroenterology fellow, Dr Leighton is a professor of medicine, and Dr Gurudu is an associate professor of medicine in the Division of Gastroenterology at the Mayo Clinic Arizona in Scottsdale, Arizona.

Address correspondence to:
Dr Suryakanth R. Gurudu
Mayo Clinic
13400 East Shea Boulevard
Scottsdale, AZ 85259
Tel: 480-301-8000
E-mail: gurudu.suryakanth@mayo.edu

 

Abstract: Colonoscopy is the most widely used screening modality for the detection and removal of colon polyps and for the prevention of colorectal cancer. To identify all colon lesions and reduce the risk of colorectal cancer, it is important to perform a complete colonoscopy. The success of screening colonoscopy depends upon several parameters, including bowel preparation and adenoma detection rate. Incomplete colonoscopy rates vary from 4% to 25% and are associated with higher rates of interval proximal colon cancer. This article reviews the potential causes of and preventive measures for incomplete colonoscopy, as well as techniques and technologies that may improve the rate of complete colonoscopy.

Colonoscopy is the most widely used screening modality for the detection and removal of colon polyps and for the prevention of colorectal cancer (CRC).1 Since the introduction of colonoscopy in the 1960s, the technology associated with this procedure has progressed considerably. The advantages of colonoscopy include complete visualization of the colon, detection and removal of polyps, and tissue sampling of significant lesions. In addition, colonoscopy with polypectomy reduces the incidence of CRC by up to 90%.2-4 The overall success of screening colonoscopy depends upon several parameters such as bowel preparation, cecal intubation rate, withdrawal time, and adenoma detection rate. Cecal intubation is defined as the advancement of the colonoscope tip to a point proximal to the ileocecal valve so that the whole cecal caput, including the medial wall of the cecum, is seen.5 Performing a complete colonoscopy is vital for minimizing polyp miss rates in all segments of the colon, including right-sided lesions. A large, multicenter trial of patients undergoing screening colonoscopy found that 50% of patients had significant dysplastic lesions in the proximal colon.6 Another study found that the risk of proximal cancer increased 2-fold when colonoscopy was not complete.7 Therefore, complete colonoscopy can reduce the rates of interval proximal colon cancer.8 Current guidelines propose targets for successful cecal intubation rates of at least 90% for all colonoscopies and at least 95% for -screening colonoscopies, with the knowledge that the majority of clinicians will exceed these minimal standards.5,9

In certain situations, an endoscopist will encounter difficulty in advancing the colonoscope through the colon, leading to incomplete colonoscopy. Incomplete colonoscopy rates vary from 4% to 25%.10-13 This article reviews the potential factors of an incomplete colonoscopy and the strategies for preventing such a situation. It also highlights the management of incomplete colonoscopy and discusses new techniques and technologies that can be utilized to improve visualization of the entire colon.

Factors Contributing to an Incomplete Colonoscopy

Multiple issues contribute to an incomplete colonoscopy in clinical practice, including patient, technical, and operator factors (Table). Common patient factors include inadequate bowel preparation, discomfort and intolerance, low body mass, female sex, and young age. Technical factors include diverticulosis, tortuosity, adhesions due to previous surgeries, angulation or fixation of bowel loops, and ineffective sedation.14-18 Operator factors may also play a role according to the expertise of the endoscopist or technician. For example, one study showed that colonoscopies performed later in the day had higher rates of incompletion, suggesting operator fatigue to be an important factor.19 The competency of the endoscopist appears to be a significant factor in determining the success of colonoscopy as well; the American Society for Gastrointestinal Endoscopy (ASGE) guidelines state that for trainees, 500 colonoscopies may be required to consistently achieve cecal intubation in 90% of procedures.20

Strategies for Preventing an Incomplete Colonoscopy

It is important to identify and anticipate the risk factors listed in the Table before scheduling a colonoscopy. After the risk factors have been identified, strategies to prevent an incomplete colonoscopy should be implemented. Strategies include customizing the bowel preparation, choosing the appropriate sedation, changing positions and abdominal pressure, ensuring proper endoscopic technique, and considering the use of water techniques, carbon dioxide, and magnetic endoscope imaging.

Adequate Bowel Preparation

Patient education regarding adequate bowel preparation, such as the importance of colon cleansing and specific instructions on how best to prepare for the colonoscopy, is vital. A prospective study evaluating 10,571 colonoscopies found that the completion rate of colonoscopies in patients with satisfactory bowel preparation was 67.5% compared with 36.0% in patients with poor bowel preparation (odds ratio, 3.76; P=.0005).21 A 2016 retrospective study of 28,368 colonoscopies showed that better bowel preparation significantly increased the rate of examination completion, with 99.5% completed colonoscopies from adequate bowel preparation vs 88.4% completed colonoscopies from poor bowel preparation.22 A subsequent study confirmed a high yield of lesions in colonoscopies with better bowel preparation.23

Certain patients are at risk for inadequate bowel preparation, including patients with a history of suboptimal bowel preparation, diabetes, chronic constipation, or abdominal surgery, as well as patients on medications that slow gut motility (eg, tricyclic antidepressants, opiates). In such patients, a 2-day extended preparation, with larger volumes of bowel preparation, can be considered.18 Split-dose bowel preparation has shown to have better colon cleansing in all segments of the colon, and has recently become the standard of care for colon cleansing.24

Appropriate Sedation

Choosing the appropriate sedation method in advance can facilitate procedure completion and improve patient tolerance. Conscious or moderate sedation for screening colonoscopy is well tolerated and cost-effective for most patients. Monitored anesthesia care with propofol should be considered in young women, patients with chronic abdominal pain, long-term opiate users, and patients with a history of abdominal surgery, as these factors are predictors of an inadequate response to moderate sedation.25 One study reported a completion rate of 98% in 119 patients upon repeat colonoscopy with anesthesia assistance.26

Endoscopic Techniques

A comprehensive review of tips for achieving a successful colonoscopy outlined specific techniques for loop reduction and problem-solving in an algorithmic fashion.27 Because the left colon is the most difficult segment of the colon to navigate during insertion, the endoscopist should begin a colonoscopy by anticipating altered sigmoid anatomy and reduce the loops before advancing beyond the splenic flexure. Narrowing and angulations of the sigmoid colon may cause difficulty if an adult colonoscope is inserted; therefore, a pediatric colonoscope or gastroscope may be a better choice, as these devices have a compact arc that can overcome tight turns and allow for easier progress through the sigmoid, and are more flexible compared to standard colonoscopes.27

Abdominal Pressure and Position Changes

The development of looping can cause pain and discomfort to the patient and make advancement of the colonoscope difficult. Abdominal pressure and position changes can be helpful when loops develop. The use of nonspecific abdominal pressure, specific pressure near the tip of the colonoscope, and position changes with the patient are encouraged in a stepwise manner. A study evaluating pressure technique found that nonspecific abdominal pressure was initially more successful on the left side of the colon (78%) than on the right side of the colon (47%; P<.0005), and as the colonoscopy progressed, specific pressure became more useful on the right side.28 If abdominal pressure was not beneficial, changing the position of the patient from left lateral to supine was effective in 68% of patients with difficult colonoscopy.28

Water Techniques

Water techniques, such as water exchange and water immersion, are 2 colonoscopy methods that utilize infusion of water to distend the lumen of the colon. With water exchange, water is suctioned during insertion, whereas with water immersion, water is primarily suctioned during withdrawal. Infused water during the colonoscope insertion weighs down the left colon, straightening the sigmoid and, thus, facilitating advancement. Suctioning the air minimizes angulations, and the colon shortens.29,30 A prospective study of 44 unsedated patients with a history of abdominal surgery compared the use of water immersion to air insufflation.31 Patients who underwent water immersion had a higher rate of cecal intubation (86% vs 50%; P=.0217).31 Water exchange colonoscopy has certain advantages over conventional air insufflation colonoscopy, including less discomfort,32 less or no sedation,33,34 and less need for external abdominal pressure and change in patient position to complete the examinations.35

Carbon Dioxide

Carbon dioxide can be used for colonic insufflation to prevent prolonged colonic distention and discomfort.36 Carbon dioxide is rapidly absorbed through the intestinal mucosa, transported by blood to the lungs, and exhaled. A meta-analysis has shown a significant reduction in abdominal pain during and following the procedure, but no difference was noted in the cecal or ileal intubation rate and time or in the total examination time compared with air insufflation.37 Water methods combined with carbon dioxide have shown significant increase in cecal intubation rate; however, this may be attributed to the water method itself.

Magnetic Endoscope Imaging

The magnetic endoscope imaging (MEI) system ScopeGuide (Olympus Optical) is a technology that offers real-time visualization of the colonoscope shaft in 3-dimensional views. The system helps to identify difficult anatomy, recognize and overcome loops, and apply specific abdominal pressure in the appropriate location. This technology also allows for training on loop reduction skills. A randomized, controlled, prospective study involving 296 patients compared standard colonoscopy to colonoscopy with MEI performed by either trainees or experienced endoscopists.38 Cecal intubation rates were higher (100% vs 89%) and intubation times were shorter (11.8 vs 15.3 min) in the MEI trainee group compared to the standard colonoscopy trainee group. Additionally, shorter intubation times (8.0 vs 9.3 min) were noted with MEI performed by experienced endoscopists.38 A meta-analysis reviewed approximately 2900 patients who underwent MEI or standard colonoscopy.39 Cecal intubation rates were higher with MEI, but no difference was noted in overall cecal intubation times. These benefits were mostly noted among inexperienced endoscopists.39 Currently, the MEI system is recommended primarily for training; however, the system appears promising for improving colonoscopy completion and loop reduction. There is a learning curve in the use of this technology, even for experienced endoscopists, as it involves additional imaging during the procedure.

Management of Incomplete Colonoscopy

The ASGE and the American College of Gastroenterology recommend a cecal intubation rate of at least 90% for all colonoscopies and at least 95% in screening colonoscopies.5,9 These high rates of colonoscopy completion for effective patient care are quality metrics tied to reimbursement. Management options relate to patient factors, institutional expertise, and available technologies. If a standard colonoscopy is not successful despite the described methods, alternative endoscopic approaches or imaging can be considered. Current options include repeat colonoscopy with or without anesthesia, double-contrast barium enema, computed tomography colonography (CTC), or overtube-assisted colonoscopy. Newer technologies include the colon capsule (PillCam, Medtronic; Figure 1) and the C-Scan Cap imaging system (Check-Cap Ltd; Figure 2).

Repeat Colonoscopy

Repeat colonoscopy can be attempted depending on the reasons for incomplete colonoscopy, and can be performed with different sedation methods, anesthesia assistance, alternate instruments, and different physicians. It is important to customize the bowel preparation and to educate the patient. Of note, deeper sedation means less assistance by the patient. MEI can be considered for repeat colonoscopy.

Imaging

Double-Contrast Barium Enema  With the introduction of other imaging technologies, the role of double-contrast barium enema is restricted due to its low sensitivity for adenoma detection; therefore, its use is discouraged. One study suggests adequate visualization with this method in 77% to 94% of patients after incomplete colonoscopy.40 In a study directly comparing double-contrast barium enema with repeat colonoscopy for completion of colonoscopy, the polyp detection rate was significantly superior with repeat colonoscopy (34.3% vs 3.6%; P<.001).41

Computed Tomography Colonography  CTC produces 2- and 3-dimensional images that allow reconstruction of endoluminal images of the colon. Smaller volumes of bowel preparation, as compared to standard colonoscopies, are needed the day prior to the test. Contrast agents are used for stool and fluid tagging, and iodinated or barium contrast is incorporated into the residual fecal matter to differentiate it from polyps. The colon is then insufflated with air or carbon dioxide. CTC is often performed after incomplete colonoscopy. In 546 patients with incomplete colonoscopy due to redundancy and tortuosity who underwent CTC, 13.2% had additional polyps of at least 6 mm in size.42 Of these patients, 63% underwent repeat colonoscopy, and it is estimated that the positive predictive value per patient undergoing CTC for masses, large polyps, and medium-sized polyps was 91%, 92%, and 65%, respectively.42 The main advantages of CTC are that no sedation is required, a smaller amount of bowel preparation is needed, and it is less invasive than a colonoscopy. CTC also has the benefit of being performed on the same day as the colonoscopy and may be used safely in anticoagulated patients. Disadvantages include lower sensitivity for polyp detection compared to colonoscopy, lack of therapeutic capability, and occasional underdistention of the sigmoid, especially if the endoscopist encounters a difficult sigmoid colon. In experienced hands, and in the appropriate clinical setting, CTC may be a good alternative to conventional colonoscopy and can also provide information on extracolonic findings; however, if the reason for colonoscopy was a positive fecal immunochemical test, then CTC may be inadequate.

Overtube-Assisted Colonoscopy

The concept of overtube-assisted colonoscopy was introduced in the 1980s.43 The overtube helps to straighten the endoscope and the colon upon loop formation and colonic angulations. Several variations have been developed to decrease mucosal injury and perforations. The currently available overtube endoscopes are the single-balloon enteroscopy (SBE) overtube (ST-SB1, Olympus America) and the double-balloon enteroscopy (DBE) overtube (TS-13140, Fujinon). Spiral overtubes are available for pediatric colonoscopes or enteroscopes (eg, Endo-Ease Discovery SB and Endo-Ease Vista, both from Spirus Medical).44

Balloon-assisted enteroscopes initially were created to allow deep insertion of the endoscope into the small bowel. SBE and DBE are used for incomplete colonoscopies and can be used in patients who have risk factors for a difficult colonoscopy. Dedicated colonoscopes using the double-balloon technologies are also available, although their use is limited to availability of these technologies.

Double-Balloon Enteroscopy and Colonoscopy  DBE has been available for clinical use since 2003.45 It comprises a 200-cm endoscope and an overtube, each with an inflatable latex balloon near its tip. The overtube and endoscope are advanced in sequence with the help of the balloons to pleat the bowel; thus, looping is minimized and the endoscope can advance deep into the small intestine.

The double-balloon colonoscope, another modality that can be utilized for patients with incomplete colonoscopy, is shorter than the double-balloon enteroscope, at 152 cm. A Japanese multicenter, prospective trial that included 110 patients with incomplete colonoscopies reported a 100% cecal intubation rate and a median intubation time of 12 minutes.46 Subsequently, the same group demonstrated the safety of the double-balloon colonoscope with no reported complications.47 The reasons for incomplete colonoscopies were loop formation, colon angulation, and pain.47 Approximately 50% of the patients had abdominal surgery, and 20% had a history of diverticulosis.47 The yield of double-balloon colonoscopy for clinically significant lesions was 50% in this patient population.47 A smaller study in which 20 patients underwent colonoscopy with the double-balloon enteroscope for prior incomplete colonoscopy reported successful cecal intubation in 95% of the patients, with a mean cecal intubation time of 28 minutes. No complications were reported.48

Single-Balloon Enteroscopy  SBE has been commercially available since 2007.49 SBE uses an endoscope and an overtube with a silicon balloon at the tip, which, when inflated, anchors it into the small bowel. When the balloon is anchored, the endoscopist pulls the endoscope and the overtube together, allowing the bowel to pleat over the endoscope, thereby reducing the loops that have formed. Once reduced, the endoscope is advanced deeply into the bowel until resistance is met, at which point the balloon is deflated and the overtube is advanced over the endoscope until it reaches the tip of the endoscope. The balloon is reinflated, and the cycle is repeated.

The single-balloon system has been shown to be useful in difficult colonoscopies. Reports show a 93% to 100% success rate of reaching the cecum, allowing for endoscopic interventions.50-52 Both single- and double-balloon enteroscopes with overtubes can be considered reasonable alternatives after incomplete conventional colonoscopy, with high success rates. Two studies compared the utility of SBE vs DBE in patients with a history of incomplete colonoscopies, and demonstrated high intubation rates.52,53 This suggests that DBE and SBE have similar effectiveness in reaching the cecum in patients with prior incomplete colonoscopy.

Both techniques are good options in patients with redundant colons, sharp angulations, or severe diverticular disease because redundant colons and loop formations are easily overcome and fixed angulations can be adequately managed.

Integrated Inflated Balloon

G-EYE (SMART Medical Systems) is a new colonoscope with an integrated inflatable balloon at the level of the endoscope bending section, which is reusable and reprocessable. The NaviAid inflation system (SMART Medical Systems) is a balloon device that can be inserted through the colonoscope channel. These balloon systems can be inflated by the endoscopist upon colonoscope withdrawal to carry out balloon-assisted colonoscopy. The inflated balloon applies a mechanical effect over the mucosal folds, flattening and straightening them, which allows the endoscopist to reach challenging segments. A prospective, single-center study of the use of this device in 47 patients reported a 100% cecal intubation rate, with a mean cecal intubation time of 4.3 minutes.54 No major adverse events were reported.54 In a multicenter, randomized, tandem colonoscopy study comparing standard colonoscopy with G-EYE balloon colonoscopy, Shpak and colleagues reported that cecal intubation rates were comparable in 106 subjects who completed back-to-back colonoscopy examinations; however, this study was not intended to evaluate patients with incomplete colonoscopies.55

Spiral Overtubes

The spiral overtube is a 90-cm, disposable, flexible, plastic tube with a 5-mm soft spiral thread at the insertion tip that is placed over a pediatric colonoscope or enteroscope. The insertion phase of spiral endoscopy consists of rotating the device in a clockwise fashion to reach the farthest extent, or until no more pleating of the small bowel over the colonoscope is possible. The device is withdrawn using counterclockwise rotation. One study demonstrated that an overtube (Endo-Ease Vista Retrograde, Spirus Medical), together with a pediatric colonoscope or enteroscope, led to a cecal intubation rate of 92% in patients with a redundant colon.56 No adverse events were reported.56

Colon Capsule Endoscopy

Colon capsule endoscopy (CCE) first generation (CCE-1) was introduced in 2006.57 Second-generation CCE (CCE-2) was instituted later.58 CCE-2 has two 172-degree angle cameras in each end of the capsule, allowing for 344-degree coverage. The frame rate alternates between 4 to 35 images per second. At present, the main indication for CCE is colon imaging following an incomplete colonoscopy due to technical difficulties beyond poor bowel preparation. A prospective study of 34 patients undergoing CCE due to incomplete colonoscopy demonstrated that CCE passed the most proximal point reached by conventional colonoscopy in 85.3% of patients; this led to a change in clinical decision-making in 58.8% of the patients.59 Of relevance, 40% of the procedures were unsatisfactory due to poor bowel preparation.59 In another prospective study, Rex and colleagues measured the accuracy of CCE for detecting polyps at least 6 mm in size in an average-risk population.60 A total of 884 patients underwent CCE followed by conventional colonoscopy. After adjusting for poor bowel preparation, CCE identified polyps at least 6 mm in size with 81% sensitivity and 93% specificity, and identified conventional adenomas at least 6 mm in size with 88% sensitivity and 82% specificity.60 The false-negative findings from capsule analysis were attributed to sessile serrated polyps and hyperplastic polyps in 26% and 37% of patients, respectively.60

A prospective, multicenter study utilizing CCE-2 included 96 patients with incomplete colonoscopy.61 Complete visualization was reached in 69 patients (71.9%). In the 20 patients out of the 27 in whom CCE-2 did not reach the rectum, the capsule passed the colonic segment that was explored in the previous colonoscopy, leading to complete visualization of the colonic mucosa in 92.7% of the patients.61 A recent meta-analysis of 14 studies evaluated the accuracy of CCE-1 vs CCE-2, with 7 studies in each arm.62 The analysis showed a sensitivity of 58% and 54% for polyps larger than 6 mm and 10 mm, respectively, for CCE-1, and a sensitivity of 86% and 87% for polyps larger than 6 mm and 10 mm, respectively, for CCE-2.62 These results translate into a clinically relevant improvement of the capsule.

Advantages of CCE include lack of exposure to radiation and discomfort of bowel distension from air insufflation. However, for successful CCE, adequate bowel preparation is an important factor and remains intensive. In one study, patients needed 4 liters of polyethylene glycol prior to the ingestion of the capsule as well as the use of additional laxatives and prokinetics at various times.60 In addition, the optimal training and learning curve associated with CCE have yet to be defined. Another significant limitation is missed polyps.

C-Scan Cap Imaging System

The C-Scan Cap imaging system consists of an ingestible capsule that emits and detects ultra low–dose radiation. The patient ingests the capsule along with a small amount of a radio-opaque contrast agent without needing a bowel preparation while continuing with his or her daily activities. The capsule generates a 3-dimensional reconstruction of the colonic lumen for detection of polyps. Preclinical and clinical testing in healthy volunteers has demonstrated safety and feasibility with a mean radiation dose estimated at 0.04 mSv.63 Projected sensitivity is 80% for cancer and 50% for large polyps.64 However, the diagnostic performance of this system is still uncertain. Additionally, several imaging reconstruction–related features, such as measurement of polyp size and colon diameter, still need refinement and validation.

Robotic Colonoscopes

Endotics (Era Endoscopy s.r.l.) is a self-propelled robotic colonoscope consisting of a disposable probe and a console maneuvered from a workstation. The disposable probe has a head with light, water, and air systems, as well as a flexible body with clamps that allow advancement similar to a worm. The endoscopist manages the workstation and can steer 180 degrees in any direction. A study by Tumino and colleagues assessed cecal intubation in 102 patients with previous incomplete colonoscopy and found that cecal intubation was successful in 93.1% of cases.65 No adverse events were noted. No other clinical studies have been performed, as this is a fairly new technology that requires clinical validation.

Summary

Complete colonoscopy is essential to ensure a high-quality examination of the colon. Cecal intubation rates greater than or equal to 90% are recommended as a quality benchmark for colonoscopy.5,9 In approaching this issue, it is important to first anticipate when a colonoscopy may be difficult. Focusing on bowel preparation techniques prior to the procedure and using appropriate sedation and adjunct techniques such as water immersion, abdominal pressure, and patient positioning during the procedure can overcome many challenges of colonoscopy. If standard colonoscopy is unsuccessful, leading to incomplete colonoscopy, then endoscopic alternatives such as DBE and other overtube technologies have reported good -success for colonoscopy completion. Imaging modalities are also available and can be performed on the same day as colonoscopy. Newer technologies in the form of capsules and robotics may be alternative options in the future; further clinical studies are needed to assess their efficacy and success rates.

The authors have no relevant conflicts of interest to disclose.

References

1. Zauber AG, Lansdorp-Vogelaar I, Knudsen AB, Wilschut J, van Ballegooijen M, Kuntz KM. Evaluating test strategies for colorectal cancer screening: a decision analysis for the US Preventive Services Task Force. Ann Intern Med. 2008;149(9):659-669.

2. Winawer SJ, Zauber AG, Ho MN, et al; The National Polyp Study Workgroup. Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med. 1993;329(27):1977-1981.

3. Citarda F, Tomaselli G, Capocaccia R, Barcherini S, Crespi M; Italian Multicentre Study Group. Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence. Gut. 2001;48(6):812-815.

4. Thiis-Evensen E, Hoff GS, Sauar J, Langmark F, Majak BM, Vatn MH. Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer. Telemark Polyp Study I. Scand J Gastroenterol. 1999;34(4):414-420.

5. Rex DK, Schoenfeld PS, Cohen J, et al. Quality indicators for colonoscopy. Am J Gastroenterol. 2015;110(1):72-90.

6. Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000;343(3):169-174.

7. Brenner H, Chang-Claude J, Jansen L, Seiler CM, Hoffmeister M. Role of colonoscopy and polyp characteristics in colorectal cancer after colonoscopic polyp detection: a population-based case-control study. Ann Intern Med. 2012;157(4):225-232.

8. Baxter NN, Sutradhar R, Forbes SS, Paszat LF, Saskin R, Rabeneck L. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology. 2011;140(1):65-72.

9. Rex DK, Schoenfeld PS, Cohen J, et al. Quality indicators for colonoscopy. Gastrointest Endosc. 2015;81(1):31-53.

10. Bowles CJ, Leicester R, Romaya C, Swarbrick E, Williams CB, Epstein O. A prospective study of colonoscopy practice in the UK today: are we adequately prepared for national colorectal cancer screening tomorrow? Gut. 2004;53(2):277-283.

11. Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med. 2000;343(3):162-168.

12. Marshall JB, Barthel JS. The frequency of total colonoscopy and terminal ileal intubation in the 1990s. Gastrointest Endosc. 1993;39(4):518-520.

13. Ridolfi TJ, Valente MA, Church JM. Achieving a complete colonic evaluation in patients with incomplete colonoscopy is worth the effort. Dis Colon Rectum. 2014;57(3):383-387.

14. Witte TN, Enns R. The difficult colonoscopy. Can J Gastroenterol. 2007;21(8):487-490.

15. Saunders BP, Fukumoto M, Halligan S, et al. Why is colonoscopy more difficult in women? Gastrointest Endosc. 1996;43(2 Pt 1):124-126.

16. Anderson JC, Gonzalez JD, Messina CR, Pollack BJ. Factors that predict incomplete colonoscopy: thinner is not always better. Am J Gastroenterol. 2000;95(10):2784-2787.

17. Waye JD. Completing colonoscopy. Am J Gastroenterol. 2000;95(10):2681-2682.

18. Dik VK, Moons LM, Hüyük M, et al; Colonoscopy Quality Initiative. Predicting inadequate bowel preparation for colonoscopy in participants receiving split-dose bowel preparation: development and validation of a prediction score. Gastrointest Endosc. 2015;81(3):665-672.

19. Sanaka MR, Shah N, Mullen KD, Ferguson DR, Thomas C, McCullough AJ. Afternoon colonoscopies have higher failure rates than morning colonoscopies. Am J Gastroenterol. 2006;101(12):2726-2730.

20. Faulx AL, Lightdale JR, Acosta RD, et al; ASGE Standards of Practice Committee. Guidelines for privileging, credentialing, and proctoring to perform GI endoscopy. Gastrointest Endosc. 2017;85(2):273-281.

21. Hendry PO, Jenkins JT, Diament RH. The impact of poor bowel preparation on colonoscopy: a prospective single centre study of 10,571 colonoscopies. Colorectal Dis. 2007;9(8):745-748.

22. Martin D, Walayat S, Ahmed Z, et al. Impact of bowel preparation type on the quality of colonoscopy: a multicenter community-based study. J Community Hosp Intern Med Perspect. 2016;6(2):31074.

23. Bick BL, Vemulapalli KC, Rex DK. Regional center for complex colonoscopy: yield of neoplasia in patients with prior incomplete colonoscopy. Gastrointest Endosc. 2016;83(6):1239-1244.

24. Gurudu SR, Ramirez FC, Harrison ME, Leighton JA, Crowell MD. Increased adenoma detection rate with system-wide implementation of a split-dose preparation for colonoscopy. Gastrointest Endosc. 2012;76(3):603-608.e1.

25. Lichtenstein DR, Jagannath S, Baron TH, et al; Standards of Practice Committee. Sedation and anesthesia in GI endoscopy. Gastrointest Endosc. 2008;68(2):205-216.

26. Rex DK, Chen SC, Overhiser AJ. Colonoscopy technique in consecutive patients referred for prior incomplete colonoscopy. Clin Gastroenterol Hepatol. 2007;5(7):879-883.

27. Bourke MJ, Rex DK. Tips for better colonoscopy from two experts. Am J Gastroenterol. 2012;107(10):1467-1472.

28. Waye JD, Yessayan SA, Lewis BS, Fabry TL. The technique of abdominal pressure in total colonoscopy. Gastrointest Endosc. 1991;37(2):147-151.

29. Falchuk ZM, Griffin PH. A technique to facilitate colonoscopy in areas of severe diverticular disease. N Engl J Med. 1984;310(9):598.

30. Baumann UA. Water intubation of the sigmoid colon: water instillation speeds up left-sided colonoscopy. Endoscopy. 1999;31(4):314-317.

31. Leung FW, Mann SK, Leung JW, Siao-Salera RM, Guy J. The water method is effective in difficult colonoscopy—it enhances cecal intubation in unsedated patients with a history of abdominal surgery. J Interv Gastroenterol. 2011;1(4):172-176.

32. Hsieh YH, Lin HJ, Tseng KC. Limited water infusion decreases pain during minimally sedated colonoscopy. World J Gastroenterol. 2011;17(17):2236-2240.

33. Hsieh YH, Tseng KC, Hsieh JJ, Tseng CW, Hung TH, Leung FW. Feasibility of colonoscopy with water infusion in minimally sedated patients in an Asian community setting. J Interv Gastroenterol. 2011;1(4):185-190.

34. Radaelli F, Paggi S, Amato A, Terruzzi V. Warm water infusion versus air insufflation for unsedated colonoscopy: a randomized, controlled trial. Gastrointest Endosc. 2010;72(4):701-709.

35. Cadoni S, Liggi M, Falt P, et al. Evidence to suggest adoption of water exchange deserves broader consideration: its pain alleviating impact occurs in 90% of investigators. World J Gastrointest Endosc. 2016;8(2):113-121.

36. Cadoni S, Falt P, Gallittu P, Liggi M, Smajstrla V, Leung FW. Impact of carbon dioxide insufflation and water exchange on postcolonoscopy outcomes in patients receiving on-demand sedation: a randomized controlled trial. Gastrointest Endosc. 2017;85(1):210-218.e1.

37. Memon MA, Memon B, Yunus RM, Khan S. Carbon dioxide versus air insufflation for elective colonoscopy: a meta-analysis and systematic review of randomized controlled trials. Surg Laparosc Endosc Percutan Tech. 2016;26(2):102-116.

38. Shah SG, Brooker JC, Williams CB, Thapar C, Saunders BP. Effect of magnetic endoscope imaging on colonoscopy performance: a randomised controlled trial. Lancet. 2000;356(9243):1718-1722.

39. Chen Y, Duan YT, Xie Q, et al. Magnetic endoscopic imaging vs standard colonoscopy: meta-analysis of randomized controlled trials. World J Gastroenterol. 2013;19(41):7197-7204.

40. Chong A, Shah JN, Levine MS, et al. Diagnostic yield of barium enema examination after incomplete colonoscopy. Radiology. 2002;223(3):620-624.

41. Winawer SJ, Stewart ET, Zauber AG, et al; National Polyp Study Work Group. A comparison of colonoscopy and double-contrast barium enema for surveillance after polypectomy. N Engl J Med. 2000;342(24):1766-1772.

42. Copel L, Sosna J, Kruskal JB, Raptopoulos V, Farrell RJ, Morrin MM. CT colonography in 546 patients with incomplete colonoscopy. Radiology. 2007;244(2):471-478.

43. Rogers BHG. Sigmoid straightening. In: Sivak MV, Petrini JL, eds. Gastrointestinal Endoscopy: Old Problems, New Techniques. Westport, CT: Greenwood Publishing Group; 1986:112-114.

44. Moreels TG, Macken EJ, Pelckmans PA. Renewed attention for overtube-assisted colonoscopy to prevent incomplete endoscopic examination of the colon. Dis Colon Rectum. 2013;56(8):1013-1018.

45. Yamamoto H. Double-balloon endoscopy. Clin Gastroenterol Hepatol. 2005;3(7)(suppl 1):S27-S29.

46. Hotta K, Katsuki S, Ohata K, et al. A multicenter, prospective trial of total colonoscopy using a short double-balloon endoscope in patients with previous incomplete colonoscopy. Gastrointest Endosc. 2012;75(4):813-818.

47. Hotta K, Katsuki S, Ohata K, et al. Efficacy and safety of endoscopic interventions using the short double-balloon endoscope in patients after incomplete colonoscopy. Dig Endosc. 2015;27(1):95-98.

48. Kaltenbach T, Soetikno R, Friedland S. Use of a double balloon enteroscope facilitates caecal intubation after incomplete colonoscopy with a standard colonoscope. Dig Liver Dis. 2006;38(12):921-925.

49. Kawamura T, Yasuda K, Tanaka K, et al. Clinical evaluation of a newly developed single-balloon enteroscope. Gastrointest Endosc. 2008;68(6):1112-1116.

50. May A, Nachbar L, Ell C. Push-and-pull enteroscopy using a single-balloon technique for difficult colonoscopy. Endoscopy. 2006;38(4):395-398.

51. Teshima CW, Aktas H, Haringsma J, Kuipers EJ, Mensink PB. Single-balloon-assisted colonoscopy in patients with previously failed colonoscopy. Gastrointest Endosc. 2010;71(7):1319-1323.

52. Dzeletovic I, Harrison ME, Pasha SF, et al. Comparison of single- versus double-balloon assisted-colonoscopy for colon examination after previous incomplete standard colonoscopy. Dig Dis Sci. 2012;57(10):2680-2686.

53. Yamada A, Watabe H, Takano N, et al. Utility of single and double balloon endoscopy in patients with difficult colonoscopy: a randomized controlled trial. World J Gastroenterol. 2013;19(29):4732-4736.

54. Hasan N, Gross SA, Gralnek IM, Pochapin M, Kiesslich R, Halpern Z. A novel balloon colonoscope detects significantly more simulated polyps than a standard colonoscope in a colon model. Gastrointest Endosc. 2014;80(6):1135-1140.

55. Shpak B, Halpern Z, Kiesslich R, Moshkowitz M, Santo E, Hoffman A. A novel balloon-colonoscope for increased polyp detection rate—intermediate results of a randomized tandem study. United Eur Gastroenterol J. 2013;1(suppl 1):A87.

56. Schembre DB, Ross AS, Gluck MN, Brandabur JJ, McCormick SE, Lin OS. Spiral overtube-assisted colonoscopy after incomplete colonoscopy in the redundant colon. Gastrointest Endosc. 2011;73(3):515-519.

57. Eliakim R, Fireman Z, Gralnek IM, et al. Evaluation of the PillCam Colon capsule in the detection of colonic pathology: results of the first multicenter, prospective, comparative study. Endoscopy. 2006;38(10):963-970.

58. Spada C, Hassan C, Costamagna G. Colon capsule endoscopy. Gastrointest Endosc Clin N Am. 2015;25(2):387-401.

59. Alarcón-Fernández O, Ramos L, Adrián-de-Ganzo Z, et al. Effects of colon capsule endoscopy on medical decision making in patients with incomplete colonoscopies. Clin Gastroenterol Hepatol. 2013;11(5):534-540.e1.

60. Rex DK, Adler SN, Aisenberg J, et al. Accuracy of capsule colonoscopy in detecting colorectal polyps in a screening population. Gastroenterology. 2015;148(5):948-957.e2.

61. Nogales Ó, García-Lledó J, Luján M, et al. Therapeutic impact of colon capsule endoscopy with PillCam COLON 2 after incomplete standard colonoscopy: a Spanish multicenter study. Rev Esp Enferm Dig. 2017;109(5):322-327.

62. Spada C, Pasha SF, Gross SA, et al. Accuracy of first- and second-generation colon capsules in endoscopic detection of colorectal polyps: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2016;14(11):1533-1543.e8.

63. Kimchy Y, Lifshitz R, Lewkowitz S, et al. Radiographic capsule-based system for non-cathartic colorectal cancer screening. Abdom Radiol (NY). 2017;42(5):1291-1297.

64. Chatrath H, Rex DK. Potential screening benefit of a colorectal imaging capsule that does not require bowel preparation. J Clin Gastroenterol. 2014;48(1):52-54.

65. Tumino E, Parisi G, Bertoni M, et al. Use of robotic colonoscopy in patients with previous incomplete colonoscopy. Eur Rev Med Pharmacol Sci. 2017;21(4):819-826.

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