Clinical practice Guidelines: quality of colonoscopy in colorectal cancer screening

Inhaltsübersicht

Goals of this clinical practice guidline:

1. Collecting the evidence about the quality of colonoscopy screening for colorectal cancer (CRC) in order to serve as a tool for screening programs, endoscopy units and endoscopists that perform screening colonoscopies.

2. Defining and establishing quality indicators and minimum requirements based on available evidence that endoscopy units and endoscopists involved in CRC screening programs should meet.

3. Providing evidence about procedures that may improve the quality of colonoscopy.

Methods

A previously designed strategy was used to do an exhaustive search for the available evidence. First, selection of topics related to the quality of colonoscopy in CRC screening was performed by the working group. Those topics were: quality indicators before colonoscopy, management of anticoagulation and antiplatelet therapy, colonic cleansing, adenoma detection rate, value of endoscopist training and experience, cecal intubation rate, colonoscopy withdrawal time, quality in endoscopic polypectomy, polyps retrieval, complications of colonoscopy and polypectomy, sedation in colonoscopy, procedures after an incomplete colonoscopy, disinfection of endoscopy equipment and quality indicators after colonoscopy. Finally, a list of suggested indicators for monitoring was performed. Search was carried out in MEDLINE, EMBASE and Cochrane Library. Internet addresses for CpG were searched, as well as secondary publications (Bandolier, ACP Journal Club, Clinical Evidence, UpToDate) and Internet searchers TRIP database and SumSearch. Selection of articles and materials of every topic was performed by two people independently. Relevant references from different documents provided by members of the working group were also studied. In a second stage, several studies of every topic in the guideline were included. Search strategies were designed aimed to find the more important studies. Additional articles were identified by manual search of the reference lists of retrieved papers.

Scientific evidence has been classified following the Center for Evidence Based Medicine (CEBM) from Oxford ([Tab.  1]). The working group and external reviewers have evaluated both. Evidence tables were generated for every key question, based on meta-analyses or randomized controlled trials (RCTs) if these were available; otherwise, case–control studies, retrospective analyses, and case series were included.

Table 1 Definitions of categories for recommendation grade and levels of evidence used in this guideline.

Recommendation grade (rec)	Level of evidence (LE)	Source
A	1 a	Systematic review or meta-analysis of randomized clinical trials (RCTs)
	1 b	High quality individual RCT
	1 c	Efficacy demonstrated by practice and not by experimentation
B	2 a	Systematic reviews of cohort studies
	2 b	Individual cohort studies or low quality RCT (< 80 % of follow-up)
	2 c	Investigation of health results
	3 a	Systematic reviews of case-control studies
	3 b	Individual case-control studies
C	4	Case series, or low quality cohort or case-control studies
D	5	Expert opinion

Quality indicators before colonoscopy

• The informed consent must be complete and must comprise a clear explanation of the procedure and the preparation required, with a realistic discussion of discomforts, risks and benefits. Patient and physician performing the colonoscopy must sign the informed consent. (recommendation grade (rec) C, level of evidence (LE) 4).

• This clinical practice guideline recommends that screening colonoscopies should be performed in distinct programs, independent from the diagnostic and therapeutic colonoscopies performed on symptomatic patients (rec D, LE 5).

• Complications of colonoscopy due to a lack of prior assessment should be less than 10 % of recorded complications (rec D, LE 5).

• It is estimated that the average time needed to perform screening colonoscopy should be 60 minutes (rec D, LE 5).

• Delays longer than 6 weeks between notification of a positive FOBT and the performance of colonoscopy should be avoided [1](rec D, LE 5).

Managment of anticoagulation and antiplatelet therapy

• Diagnostic endoscopy, with or without biopsy, is considered a low-risk procedure. Endoscopic polypectomy is considered a high-risk procedure.

• The risk of bleeding after polypectomy does not increase significantly in patients taking aspirin or NSAIDs at standard doses and, therefore, the endoscopic procedure can be performed without removing these drugs [2] [3] [4] (rec B, LE 3b).

• The risk of bleeding after polypectomy does not seem to increase with the isolated use of clopidogrel in polyps smaller than 1 cm. Concomitant use of clopidogrel and aspirin or NSAIDs increases the risk of bleeding [5] [6] (rec B, LE 2b).

• Endoscopic polypectomy should not be performed in patients taking oral anticoagulants [7] [8] (rec B, LE 2b).

Colonic cleansing

• There is no evidence about the superiority of any colon-cleansing product over the others [9] (rec A, LE 1a)

• Effective bowel cleansing is essential for high quality colonoscopy. Good bowel preparation improves the detection of neoplasia, reduces procedure time and complications [10] [11] [12] (rec B, LE 2b).

• This clinical practice guideline recommends that in screening colonoscopies, colonic cleansing should be considered excellent or good in at least 90 % of examinations performed.

• Polyetilenglicol (PEG) preparations are faster, more effective and better tolerated than a restrictive diet combined with laxatives, high-volume enema or mannitol [13] [14] (rec A, LE 1a).

• The addition of ascorbic acid to PEG-3350 improves the taste, induces diarrhoea, inhibits bacterial reproduction and gas generation and seems as effective as the standard preparation of PEG [15] (rec A, LE 1a).

• Preparations of sodium phosphate, low-volume hyperosmolar solutions, should not be used in patients with electrolyte disorders [16] (rec A, LE 1a).

• The combination of magnesium citrate and sodium picosulfate shows a similar efficacy to traditional preparations of PEG and sodium phosphate [17] (rec C, LE 4).

• Regardless the type of preparation, splitting the volume between the day before the test and the day of the examination allows the detection of more polyps and improves tolerance and security [18] [19] [20] [21] (rec B, LE 2b).

• Time between the last dose and the start of the examination should be lower than 6 hours and greater than 2 hours [19] [22] [23] (rec A, LE 1a).

• Endoscopy reports should contain details of what type of bowel cleansing has been used and should state the degree of colonic cleansing achieved. Any of the validated classifications can be used for this purpose [24] [25] [26] (rec B, LE 2b).

Adenoma detection rate

• The Adenoma Detection Rate (ADR) may be defined as the number of colonoscopies at which one or more histologically confirmed adenomas are founded divided by the total number of colonoscopies performed.

• ADR appears as a direct parameter of quality, reliable and easy to obtain, that assesses the skill of the endoscopist involved in CRC screening program [27] [28] [29] (LE 2b).

• ADR is an independent factor predicting the risk of interval cancer after a screening colonoscopy [30] (LE 1b).

• Expected ADR in western populations when colonoscopy is used as the initial strategy of CRC screening should be at least 20 % [30] (rec A, LE 1b).

• Expected ADR in western populations when the initial strategy of screening is the immunological FOBT should be higher than 40 % [31] [32] [33] [34] (rec A, LE 1c).

Value of endoscopist training and experience

• The endoscopist experience in screening colonoscopy is directly related to many aspects of quality such are cecal intubation rate, ADR or the complications rate. Therefore, it is recommended that endoscopists performing screening colonoscopies meet minimum standards for life-time experience and annual number of procedures [35] [36] [37] (rec B, LE 2b).

• Screening colonoscopies performed by non-gastroenterologists are more often related to the appearance of interval CRC [38] [39] (rec B, LE 2b).

• This clinical practice guideline recommends a minimum experience in colonoscopy (at least 200 colonoscopies and 200 supervised colonoscopies as a specialist) and a continuous dedication (at least 200 colonoscopies per year) for performing CRC screening colonoscopy.

• Endoscopists especially dedicated to the implementation of CRC screening colonoscopies have better detection rates of adenomas [40] (rec B, LE 2b).

• Nurses experience performing colonoscopy also influences the rate of colonoscopy complications, the exploration time and the cecal intubation rate [41] [42] (rec A, LE 1b).

Cecal intubation rate

• Cecal intubation is defined as the insertion of the endoscope tip to a point proximal to the ileocecal valve so that the entire cecal pole, including the medial wall (located between the ileocecal valve and appendicular orifice) is visualized and explored.

• Photographic documentation is recommended in every endoscopic procedure as a quality parameter [43] (rec B, LE 2b).

• Cecal intubation rate must be greater than or equal to 95 % when the indication for colonoscopy is CRC screening in healthy adults [43] [44] [45] (rec B, LE 2b).

• Incomplete procedures due to poor preparation or severe colitis and colonoscopies performed for a therapeutic purpose should be excluded to determine the cecal intubation rate. All other procedures should be included.

• Female gender, advanced age and history of abdominal-pelvic surgery, especially hysterectomy, have been associated with lower cecal intubation rates [46] [47] [48] (LE 1b).

• The use of small calibre endoscopes (pediatric endoscope) and variable stiffness endoscope can facilitate intubation of the cecum when there is a difficult sigmoid colon [49] (rec D, LE 5).

• Instillation of water into the sigmoid colon instead of air can facilitate the passage of the endoscope [50] [51] (rec C, LE 4).

• Straightening maneuvers, change of body position and abdominal pressure can help to complete the exploration when cecal intubation is difficult due to a redundant colon [40] [52] (rec D, LE 5).

Colonoscopy withdrawal time

• Colonoscopy withdrawal time was calculated as the time from cecal intubation to the extraction of the colonoscope through the anus.

• The longer is the colonoscopy withdrawal time, the higher ADR can be achieved [43] (LE 2b).

• Mean colonoscopy withdrawal time should be longer than 6 minutes [53] (rec B, LE 2b).

• An appropriate withdrawal technique, looking carefully into the proximal side of the haustra, folds and valves, cleaning and aspirating liquid stools and with adequate colonic distension, improves ADR.

Quality in endoscopic polypectomy

• Polyps should be classified according to their macroscopic aspect (Paris classification) and size [54].

• All the detected polyps must be resected, even diminutive rectal polyps, except if they are obviously non neoplastic [55] [56] (rec A, LE 1c).

• It is not necessary to make routine blood test before colonoscopy and/or polypectomy [57] (rec B, LE 2b).

• Guillotine resection with cold snare seems more appropriate than extirpation with biopsy forceps for polyps smaller than 5 – 7 mm in order to avoid incomplete resections. [58] [59] (rec C, LE 4).

• Hot biopsy forceps technique could be used for polyps up to 5 mm in diameter and must be performed cautiously. This technique should be avoided in the right colon, especially in the cecum. [58] [60] (rec C, LE 4).

• 10 % glycerine solution allows better and longer polyp elevation than saline, allowing higher in bloc resection rate in large flat lesions [61] (rec C, LE 4).

• Adrenaline injection in the polyp base has shown a prophylactic effect for immediate bleeding, but not for late bleeding. [62] [63] (rec A, LE 1b).

• Treatment with argon gas after piecemeal resection in flat or sessile large polyps reduces recurrence rate [64] (rec A, LE 1b).

• Endoscopists should be able to resect any pedunculated polyp and flat or sessile polyps up to 2 cm in diameter.

Polyp retrieval

• Retrieval of polyps must be reflected in the endoscopy report.

• Roth’s basket has shown its efficacy for the retrieval of medium and large size polyps, especially in the right colon. [65]. (rec B, LE 2b).

• Small size polyps could be retrieved by aspiration through the endoscope working channel [66] [67] (rec C, LE 4).

• These clinical practice guidelines recommend a polyp retrieval rate higher than 80 % for polyps smaller than 10 mm and 95 % for polyps of 10 mm or larger.

Colonoscopy and polypectomy complications

• Colonoscopy perforation rate should be lower than 1 / 1,000 procedures [68] [69] (rec D, LE 5).

• Women seem to have a higher frequency of minor complications such as pain or abdominal distension [70] [71] (LE 1b).

• Advanced age, comorbidity, obesity, diverticulosis, history of abdominal surgery, or low experienced endoscopist are associated with a higher perforation rate [72] [73] (LE 2b).

• Significant post-polypectomy bleeding should be lower than 1 / 200 endoscopic polypectomies [69] (rec D, LE 5).

• The main risk factors for bleeding are: age over 65, concomitant cardiovascular or renal disease, anticoagulant therapy, polyp size larger than 1 cm, right-sided polyps, polyps with thick pedicle or lateral extension, poor bowel cleansing, use of cutting current or unnoticed cut of the polyp before applying current [74] [75] (LE 2b).

• The experience of the endoscopist is related to the post-polypectomy bleeding rate. [76] [77] (LE 2b).

• Prophylactic injection of epinephrine diminishes the risk of immediate post-polypectomy bleeding [78] [79] [80] [81] [82] (rec A, LE 1b).

• The use of epinephrine or endoloops significantly reduces the risk of bleeding when compared with no prophylaxis, but there are no differences between both procedures [62] (rec A, LE 1b).

• The use of combined techniques diminishes the risk of bleeding in large pedunculated polyps [83] (rec A, LE 1b).

• The risk of perforation and thermal injury is reduced when using cutting current, but it produces a lower grade of hemostasis with a higher risk of hemorrhage. Coagulation current is associated with an increased risk of delayed lesions and must be avoided in the right colon and with flat polyps [75] [84] [85] [86] (rec B, LE 2b).

Sedation in endoscopy

• This guideline recommends that the endoscopy units involved in CRC screening must perform their colonoscopies under sedation in at least 90 % of the patients.

• Sedation in colonoscopy is associated with a higher level of patient satisfaction [87] [88] (LE 1b).

• The use of sedation requires a specific informed consent (rec D, LE 5).

• Literature data available on effectiveness, recovering issues and complications seem to favour the use of propofol over benzodiazepines. [89] (rec B; LE 2b).

• Oxygen saturation and heart frequency must be monitored along the procedure. In patients with heart diseases it is recommendable to obtain a continuous electrocardiography registry [90] (rec B, LE 2b).

• Safety of colonoscopy with propofol sedation when administered by a non-anesthesiologist is high and similar to the risk of sedation with benzodiazepines, regarding to hypoxia, hypotension and bradycardia [91] (rec A, LE 1a ).

• Assistance from an anesthesiologist when using propofol in healthy people (ASA I-II) is very expensive and it has not shown any improvement in the patient safety or in the procedure outcome [91] (LE 2c).

• Personnel in charge of monitoring the vital signs and sedation of the patient must be trained in advanced cardiopulmonary resuscitation (rec D, LE 5).

• Sedation in colonoscopy increases the rate of cecal intubation and polyp detection. Deep sedation in screening colonoscopy favors the detection of more adenomatous polyps than moderate sedation [92] (LE 3).

Procedures after an incomplete colonoscopy

• The reasons for an incomplete colonoscopy must be evaluated again. In the setting of intolerance or inexperienced endoscopist, a new test under deep sedation and with more experienced personnel must be scheduled (rec A, LE 1c).

• Several endoscopic techniques, such are the use of variable stiffness endoscopes, upper gastrointestinal endoscope or enteroscope may complete the study of the colon. [93] (LE 4).

• CT colonography is better than barium enema in the detection of colonic lesions, yielding better sensitivity and specificity. Therefore, this technique is preferred in the setting of incomplete screening colonoscopy [94] [95] [96] (rec B, LE 2a).

• CT colonography has shown a detection rate for polyps ≥ 10 mm and advanced neoplasia similar to the obtained with the colonoscopy. However, both sensitivity and specificity are lower than the obtained with the colonoscopy for lesions < 10 mm [97] [98] [99] (LE 1a).

• The results with MR colonography are similar to those obtained with CT colonography, although its use is not widespread [100] [101] [102] (LE 2a).

Disinfection of endoscopy equipment

• Gastrointestinal endoscopy is an invasive procedure which may facilitate the transmission of viral or bacterial infections [103] (LE 1c).

• Endoscope reprocessing must be done by qualified personnel, with specific training and experience [104] (rec A, LE 1c).

• Proper manual cleaning alone eliminates 99 % of infective agents and is the most important step in the reduction of the microbial load [105] (LE 1c).

• Automatic endoscope reprocessors provide a high-level disinfection, similar to the manual system, but with the advantage that the whole procedure is standardized and can be validated in every step [106] [107] (LE 1b).

• Reusable ancillary devices must be cleaned mechanically and then sterilized [104] (rec A, LE 1a).

• Ancillary devices must be single-use when possible [108] (rec A, LE 1c).

• Endoscope reprocessing must be done in a separate facility, specifically aimed to this function. This facility must be equipped with and adequate air cleaning and gas extraction system. [109] (rec A, LE 1c).

• It is advisable to obtain culture samples periodically from the endoscopes and ancillary devices in order to detect contamination. A three-month periodicity may be adequate [110] (rec B, LE 2b ).

Quality indicators after colonoscopy

• Recovery after colonoscopy will take place in a specific area, separated from the endoscopy room and fully equipped to provide postanesthetic care. [111] [112] (rec A, LE 1b).

• Before being discharged from the endoscopy unit, the patient must be conscious and oriented, with normal vital signs and with at least 9 points on the Modified Aldrete’s Scoring System 8112,113] (rec A, LE 1b).

• Fulfilment of a satisfaction questionnaire is recommended. [114] [115] (rec C, LE 4).

• It is advisable to provide the patient with a contact phone, available at least 12 hours a day, to communicate any colonoscopy-related complication [116] (rec C, LE 5).

Quality indicators and auditable outcomes

A quality indicator is an outcome supported by enough evidence to be strongly recommended as a quality standard. An auditable outcome is a result that should be measured, but there is not enough evidence yet for recommending it as a quality standard. Quality indicators and auditable outcomes can be seen in [Table 2], with their suggested acceptable levels for endoscopy units and endoscopists participating in CRC screening programmes.

Table 2 Quality indicators and auditable outcomes for quality monitoring in colorectal cancer screening colonoscopy.

Indicator	Definition	Indicator type	Acceptable level	Recommendation grade and level of evidence	Subject
Adenoma detection rate	Proportion of colonoscopies performed in asymptomatic individuals over 50 in which at least one adenoma has been detected.	Quality indicator	> 20 %	A; 1b	Endoscopist
Adenoma detection rate after positive FOBT	Proportion of colonoscopies performed in individuals after a positive FOBT in which at least one adenoma has been detected.	Quality indicator	> 40 %	A; 1c	Endoscopist
Colonoscopy withdrawal time	Mean time from cecal intubation to colonoscopy extraction through the anus.	Quality indicator	> 6 minutes	B; 2b	Endoscopist
Endoscopist experience	Number of colonoscopies performed during the endoscopist career (previous) and during the last year (annual).	Quality indicator	Previous: 400 Annual: 200	D; 5	Endoscopist
Cecal intubation rate	Proportion of procedures in which cecal intubation is achieved.	Quality indicator	> 95 %	B; 2b	Endoscopist
Waiting time from positive FOBT to colonoscopy	Time from communication of positive FOBT result to follow-up colonoscopy.	Quality indicator	< 6 weeks	D; 5	Endoscopy Unit
Use of sedation	Proportion of colonoscopies performed under sedation.	Auditable Outcome	> 90 %		Endoscopist
Appropriate bowel cleansing	Proportion of procedures in which colon cleansing is considered excellent or good.	Auditable Outcome	> 90 %		Endoscopy Unit
Colon perforation rate	Proportion of procedures in which a colon perforation is direct consequence of the procedure.	Quality indicator	< 1 / 1000 colonoscopies	D; 5	Endoscopist
Post-polypectomy bleeding rate	Proportion of individuals who have a significant bleeding requiring hospitalization as a consequence of an endoscopic polypectomy.	Quality indicator	< 1 / 200 polipectomies	D; 5	Endoscopist
Description of polyp characteristics	Appropriate description of polyps in shape, size, location and type following the Paris classification.	Auditable Outcome	100 %		Endoscopist
Staff, infrastructures, and endoscopy unit equipment		Auditable Outcome	At least 2 endoscopists fulfil acceptable level		Endoscopy Unit
Independent screening colonoscopy program	Screening colonoscopies are performed in independent programs, separated from diagnostic or therapeutic procedures performed in symptomatic patients.	Auditable Outcome	100 %		Endoscopy Unit
Record of complications	Existence of an active record of the complications arising in screening colonoscopies.	Auditable Outcome	100 %		Endoscopy Unit
Endoscopic resection of pedunculated polyps and sessile/flat polyps	All pedunculated polyps and sessile or flat polyps smaller than 2 cm are endoscopically resected.	Auditable Outcome	Attempt: 100 % Extirpation > 95 %		Endoscopist
Retrieval rate of resected polyps	Proportion of resected polyps that are retrieved for pathological study.	Auditable Outcome	> 95 % polyps > 10 mm > 80 % polyps < 10 mm		Endoscopist
Information and consent	Existence of an information sheet and a consent document signed by all the persons before the colonoscopy.	Quality indicator	100 %	C; 4	Endoscopy Unit
Colonoscopy complications due to lack of previous assessment	Colonoscopy complications related to the lack of knowledge of patient history or use of antiplatelet or anticoagulant therapy.	Auditable Outcome	< 10 %		Endoscopy Unit
Decontamination indicators	Appropriate control of endoscopy disinfection measures.	Quality indicator	Every 3 months	B; 2c	Endoscopy Unit
Existence of a program of quality improvement	Endoscopy unit is following an appropriate quality control program.	Auditable Outcome	Yearly		Endoscopy Unit
*FOBT: fecal occult blood test.

References

• 1 Paterson W G, Depew W T, Pare P et al. Canadian consensus on medically acceptable wait times for digestive health care.  Can J Gastroenterol. 2006;  20(6) 411-423
• 2 Hui A J, Wong R M, Ching J Y et al. Risk of colonoscopic polypectomy bleeding with anticoagulants and antiplatelet agents: analysis of 1657 cases.  Gastrointest Endosc. 2004;  59(1) 44-48
• 3 Shiffman M L, Farrel M T, Yee Y S. Risk of bleeding after endoscopic biopsy or polypectomy in patients taking aspirin or other NSAIDS.  Gastrointest Endosc. 1994;  40(4) 458-462
• 4 Yousfi M, Gostout C J, Baron T H et al. Postpolypectomy lower gastrointestinal bleeding: potential role of aspirin.  Am J Gastroenterol. 2004;  99(9) 1785-1789
• 5 Friedland S, Soetikno R. Colonoscopy with polypectomy in anticoagulated patients.  Gastrointest Endosc. 2006;  64(1) 98-100
• 6 Singh M, Mehta N, Murthy U K et al. Postpolypectomy bleeding in patients undergoing colonoscopy on uninterrupted clopidogrel therapy.  Gastrointest Endosc. 2010;  71(6) 998-1005
• 7 Kim H S, Kim T I, Kim W H et al. Risk factors for immediate postpolypectomy bleeding of the colon: a multicenter study.  Am J Gastroenterol. 2006;  101(6) 1333-1341
• 8 Sawhney M S, Salfiti N, Nelson D B et al. Risk factors for severe delayed postpolypectomy bleeding.  Endoscopy. 2008;  40(2) 115-119
• 9 Belsey J, Epstein O, Heresbach D. Systematic review: oral bowel preparation for colonoscopy.  Aliment Pharmacol Ther. 2007;  25(4) 373-384
• 10 Froehlich F, Wietlisbach V, Gonvers J J et al. Impact of colonic cleansing on quality and diagnostic yield of colonoscopy: the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study.  Gastrointest Endosc. 2005;  61(3) 378-384
• 11 Harewood G C, Sharma V K, de Garmo P. Impact of colonoscopy preparation quality on detection of suspected colonic neoplasia.  Gastrointest Endosc. 2003;  58(1) 76-79
• 12 Rex D K, Imperiale T F, Latinovich D R, Bratcher L L. Impact of bowel preparation on efficiency and cost of colonoscopy.  Am J Gastroenterol. 2002;  97(7) 1696-1700
• 13 Adler M, Quenon M, Even-Adin D et al. Whole gut lavage for colonoscopy--a comparison between two solutions.  Gastrointest Endosc. 1984;  30(2) 65-67
• 14 DiPalma J A, Brady C E, III , Stewart D L et al. Comparison of colon cleansing methods in preparation for colonoscopy.  Gastroenterology. 1984;  86(5 Pt 1) 856-860
• 15 Ell C, Fischbach W, Bronisch H J et al. Randomized trial of low-volume PEG solution versus standard PEG + electrolytes for bowel cleansing before colonoscopy.  Am J Gastroenterol. 2008;  103(4) 883-893
• 16 Marschall H U, Bartels F. Life-threatening complications of nasogastric administration of polyethylene glycol-electrolyte solutions (Golytely) for bowel cleansing.  Gastrointest Endosc. 1998;  47(5) 408-410
• 17 Love J, Bernard E J, Cockeram A et al. A multicentre, observational study of sodium picosulfate and magnesium citrate as a precolonoscopy bowel preparation.  Can J Gastroenterol. 2009;  23(10) 706-710
• 18 Aoun E, Abdul-Baki H, Azar C et al. A randomized single-blind trial of split-dose PEG-electrolyte solution without dietary restriction compared with whole dose PEG-electrolyte solution with dietary restriction for colonoscopy preparation.  Gastrointest Endosc. 2005;  62(2) 213-218
• 19 Parra-Blanco A, Nicolas-Perez D, Gimeno-Garcia A et al. The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study.  World J Gastroenterol. 2006;  12(38) 6161-6166
• 20 Rostom A, Jolicoeur E, Dube C et al. A randomized prospective trial comparing different regimens of oral sodium phosphate and polyethylene glycol-based lavage solution in the preparation of patients for colonoscopy.  Gastrointest Endosc. 2006;  64(4) 544-552
• 21 Sabri M, di Lorenzo C, Henderson W et al. Colon cleansing with oral sodium phosphate in adolescents: dose, efficacy, acceptability, and safety.  Am J Gastroenterol. 2008;  103(6) 1533-1539
• 22 Church J M. Effectiveness of polyethylene glycol antegrade gut lavage bowel preparation for colonoscopy--timing is the key!.  Dis Colon Rectum. 1998;  41(10) 1223-1225
• 23 Poon C M, Lee D W, Mak S K et al. Two liters of polyethylene glycol-electrolyte lavage solution versus sodium phosphate as bowel cleansing regimen for colonoscopy: a prospective randomized controlled trial.  Endoscopy. 2002;  34(7) 560-563
• 24 Aronchick C A. Bowel preparation scale.  Gastrointest Endosc. 2004;  60(6) 1037-1038
• 25 Lai E J, Calderwood A H, Doros G et al. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research.  Gastrointest Endosc. 2009;  69(3 Pt 2) 620-625
• 26 Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality.  Gastrointest Endosc. 2004;  59(4) 482-486
• 27 Bretagne J F, Ponchon T. Do we need to embrace adenoma detection rate as the main quality control parameter during colonoscopy?.  Endoscopy. 2008;  40(6) 523-528
• 28 Pinsky P F, Schoen R E, Weissfeld J L et al. Variability in flexible sigmoidoscopy performance among examiners in a screening trial.  Clin Gastroenterol Hepatol. 2005;  3(8) 792-797
• 29 Rex D K. Maximizing detection of adenomas and cancers during colonoscopy.  Am J Gastroenterol. 2006;  101(12) 2866-2877
• 30 Kaminski M F, Regula J, Kraszewska E et al. Quality indicators for colonoscopy and the risk of interval cancer.  N Engl J Med. 2010;  362(19) 1795-1803
• 31 Faivre J, Dancourt V, Lejeune C et al. Reduction in colorectal cancer mortality by fecal occult blood screening in a French controlled study.  Gastroenterology. 2004;  126(7) 1674-1680
• 32 Kronborg O, Fenger C, Olsen J et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test.  Lancet. 1996;  348(9040) 1467-1471
• 33 Manfredi S, Piette C, Durand G et al. Colonoscopy results of a French regional FOBT-based colorectal cancer screening program with high compliance.  Endoscopy. 2008;  40(5) 422-427
• 34 Steele R J, McClements P L, Libby G et al. Results from the first three rounds of the Scottish demonstration pilot of FOBT screening for colorectal cancer.  Gut. 2009;  58(4) 530-535
• 35 Harewood G C. Relationship of colonoscopy completion rates and endoscopist features.  Dig Dis Sci. 2005;  50(1) 47-51
• 36 Radaelli F, Meucci G, Sgroi G, Minoli G. Technical performance of colonoscopy: the key role of sedation/analgesia and other quality indicators.  Am J Gastroenterol. 2008;  103(5) 1122-1130
• 37 Wexner S D, Garbus J E, Singh J J. A prospective analysis of 13,580 colonoscopies. Reevaluation of credentialing guidelines.  Surg Endosc. 2001;  15(3) 251-261
• 38 Bressler B, Paszat L F, Chen Z et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis.  Gastroenterology. 2007;  132(1) 96-102
• 39 Rabeneck L, Paszat L F, Saskin R. Endoscopist specialty is associated with incident colorectal cancer after a negative colonoscopy.  Clin Gastroenterol Hepatol. 2010;  8(3) 275-279
• 40 Fracchia M, Senore C, Armaroli P et al. Assessment of the multiple components of the variability in the adenoma detection rate in sigmoidoscopy screening, and lessons for training.  Endoscopy. 2010;  42(6) 448-155
• 41 Dellon E S, Lippmann Q K, Galanko J A et al. Effect of GI endoscopy nurse experience on screening colonoscopy outcomes.  Gastrointest Endosc. 2009;  70(2) 331-343
• 42 van Putten P G, van Leerdam M E, Kuipers E J. The views of gastroenterologists about the role of nurse endoscopists, especially in colorectal cancer screening.  Aliment Pharmacol Ther. 2009;  29(8) 892-897
• 43 Rex D K, Petrini J L, Baron T H et al. Quality indicators for colonoscopy.  Gastrointest Endosc. 2006;  63(4) 16-28
• 44 Johnson D A, Gurney M S, Volpe R J et al. A prospective study of the prevalence of colonic neoplasms in asymptomatic patients with an age-related risk.  Am J Gastroenterol. 1990;  85(8) 969-74
• 45 Marshall J B, Barthel J S. The frequency of total colonoscopy and terminal ileal intubation in the 1990 s.  Gastrointest Endosc. 1993;  39(4) 518-520
• 46 Anderson J C, Messina C R, Cohn W et al. Factors predictive of difficult colonoscopy.  Gastrointest Endosc. 2001;  54(5) 558-562
• 47 Kim W H, Cho Y J, Park J Y et al. Factors affecting insertion time and patient discomfort during colonoscopy.  Gastrointest Endosc. 2000;  52(5) 600-605
• 48 Shah H A, Paszat L F, Saskin R et al. Factors associated with incomplete colonoscopy: a population-based study.  Gastroenterology. 2007;  132(7) 2297-2303
• 49 Rex D K. Achieving cecal intubation in the very difficult colon.  Gastrointest Endosc. 2008;  67(6) 938-944
• 50 Baumann U A. Water intubation of the sigmoid colon: water instillation speeds up left-sided colonoscopy.  Endoscopy. 1999;  31(4) 314-317
• 51 Leung F W, Aharonian H S, Leung J W et al. Impact of a novel water method on scheduled unsedated colonoscopy in U.S. veterans.  Gastrointest Endosc. 2009;  69(3 Pt 1) 546-550
• 52 Witte T N, Enns R. The difficult colonoscopy.  Can J Gastroenterol. 2007;  21(8) 487-490
• 53 Barclay R L, Vicari J J, Doughty A S et al. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy.  N Engl J Med. 2006;  355(24) 2533-2541
• 54 The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002.  Gastrointest Endosc. 2003;  58(6 Suppl) 3-43
• 55 Riley S. Colonoscopic polypectomy and endoscopic mucosal resection: a practical guide. http://www bsg org uk/pdf_word_docs/polypectomy_08 pdf 2008
• 56 Moran S S, Torrella E, Esteban D P et al. Colonoscopy quality assessment.  Rev Esp Enferm Dig. 2009;  101(2) 107-6
• 57 Levy M J, Anderson M A, Baron T H et al. Position statement on routine laboratory testing before endoscopic procedures.  Gastrointest Endosc. 2008;  68(5) 827-832
• 58 Carpenter S, Petersen B T, Chuttani R et al. Polypectomy devices.  Gastrointest Endosc. 2007;  65(6) 741-749
• 59 Chino A, Karasawa T, Uragami N et al. A comparison of depth of tissue injury caused by different modes of electrosurgical current in a pig colon model.  Gastrointest Endosc. 2004;  59(3) 374-379
• 60 Mann N S, Mann S K, Alam I. The safety of hot biopsy forceps in the removal of small colonic polyps.  Digestion. 1999;  74-6 Ref Type: Generic
• 61 Uraoka T, Fujii T, Saito Y et al. Effectiveness of glycerol as a submucosal injection for EMR.  Gastrointest Endosc. 2005;  61(6) 736-740
• 62 di Giorgio P, de Luca L, Calcagno G. Detachable snare versus epinephrine injection in the prevention of postpolypectomy bleeding: a randomized and controlled study.  Endoscopy. 2004;  860-863 Ref Type: Generic
• 63 Paspatis G A, Paraskeva K, Theodoropoulou A et al. A prospective, randomized comparison of adrenaline injection in combination with detachable snare versus adrenaline injection alone in the prevention of postpolypectomy bleeding in large colonic polyps.  Am J Gastroenterol. 2006;  101(12) 2805
• 64 Brooker J C, Saunders B P, Shah S G et al. Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations.  Gastrointest Endosc. 2002;  55(3) 371-375
• 65 Miller K, Waye J D. Polyp retrieval after colonoscopic polypectomy: use of the Roth Retrieval Net.  Gastrointest Endosc. 2001;  54(4) 505-507
• 66 Banez A V, Bozek S A, Simon R F. A double endoscope method for multiple colonic polypectomy.  Gastrointest Endosc. 1987;  33(1) 30-32
• 67 Waye J. It ain't over til it's over: retrieval of polyps after colonoscopic polypectomy.  Gastrointest Endosc. 2005;  62(2) 257-259
• 68 Rex D K, Bond J H, Winawer S et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer.  Am J Gastroenterol. 2002;  97(6) 1296-1308
• 69 Patnick J, Segnan N, von Karsa L. European Guidelines for Quality Assurance in Colorectal Cancer Screening 2010. 
• 70 Ko C W, Riffle S, Michaels L et al. Serious complications within 30 days of screening and surveillance colonoscopy are uncommon.  Clin Gastroenterol Hepatol. 2010;  8(2) 166-173
• 71 Rathgaber S W, Wick T M. Colonoscopy completion and complication rates in a community gastroenterology practice.  Gastrointest Endosc. 2006;  64(4) 556-562
• 72 Arora G, Mannalithara A, Singh G et al. Risk of perforation from a colonoscopy in adults: a large population-based study.  Gastrointest Endosc. 2009;  69(3 Pt 2) 654-664
• 73 Park D I, Kim H J, Park J H et al. Factors affecting abdominal pain during colonoscopy.  Eur J Gastroenterol Hepatol. 2007;  19(8) 695-699
• 74 Dobrowolski S, Dobosz M, Babicki A et al. Blood supply of colorectal polyps correlates with risk of bleeding after colonoscopic polypectomy.  Gastrointest Endosc. 2006;  63(7) 1004-1009
• 75 Heldwein W, Dollhopf M, Rosch T et al. The Munich Polypectomy Study (MUPS): prospective analysis of complications and risk factors in 4000 colonic snare polypectomies.  Endoscopy. 2005;  37(11) 1116-1122
• 76 Lorenzo-Zuniga V, Moreno de Vega V, Domenech E et al. Endoscopist experience as a risk factor for colonoscopic complications.  Colorectal Dis. 2010;  12 273-277
• 77 Rabeneck L, Paszat L F, Hilsden R J et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice.  Gastroenterology. 2008;  135(6) 1899-906,1906
• 78 Dobrowolski S, Dobosz M, Babicki A et al. Prophylactic submucosal saline-adrenaline injection in colonoscopic polypectomy: prospective randomized study.  Surg Endosc. 2004;  18(6) 990-993
• 79 Folwaczny C, Heldwein W, Obermaier G et al. Influence of prophylactic local administration of epinephrine on bleeding complications after polypectomy.  Endoscopy. 1997;  29(1) 31-33
• 80 Hsieh Y H, Lin H J, Tseng G Y et al. Is submucosal epinephrine injection necessary before polypectomy? A prospective, comparative study.  Hepatogastroenterology. 2001;  48(41) 1379-1382
• 81 Lee S H, Lee K S, Park Y S et al. Submucosal saline-epinephrine injection in colon polypectomy: appropriate indication.  Hepatogastroenterology. 2008;  55(86 – 87) 1589-1593
• 82 Shirai M, Nakamura T, Matsuura A et al. Safer colonoscopic polypectomy with local submucosal injection of hypertonic saline-epinephrine solution.  Am J Gastroenterol. 1994;  89(3) 334-338
• 83 Kouklakis G, Mpoumponaris A, Gatopoulou A et al. Endoscopic resection of large pedunculated colonic polyps and risk of postpolypectomy bleeding with adrenaline injection versus endoloop and hemoclip: a prospective, randomized study.  Surg Endosc. 2009;  23 2732-2737
• 84 Dominitz J A, Eisen G M, Baron T H et al. Complications of colonoscopy.  Gastrointest Endosc. 2003;  57(4) 441-445
• 85 Morris M L, Tucker R D, Baron T H. Electrosurgery in gastrointestinal endoscopy: principles to practice.  Am J Gastroenterol. 2009;  104(6) 1563-1574
• 86 Waye J D, Lewis B S, Yessayan S. Colonoscopy: a prospective report of complications.  J Clin Gastroenterol. 1992;  15(4) 347-351
• 87 Early D S, Saifuddin T, Johnson J C et al. Patient attitudes toward undergoing colonoscopy without sedation.  Am J Gastroenterol. 1999;  94(7) 1862-1865
• 88 Rex D K, Imperiale T F, Portish V. Patients willing to try colonoscopy without sedation: associated clinical factors and results of a randomized controlled trial.  Gastrointest Endosc. 1999;  49(5) 554-559
• 89 Wehrmann T, Riphaus A. Sedation, surveillance, and preparation.  Endoscopy. 2009;  41(1) 86-90
• 90 The u se. Council on Scientific Affairs, American Medical Association.  JAMA. 1993;  270(12) 1463-1468
• 91 Vargo J J, Cohen L B, Rex D K, Kwo P Y. Position statement: nonanesthesiologist administration of propofol for GI endoscopy.  Gastrointest Endosc. 2009;  70(6) 1053-1059
• 92 Wang A, Hoda K M, Holub J L, Eisen G M. Does level of sedation impact detection of advanced neoplasia?.  Dig Dis Sci. 2010;  55(8) 2337-2343
• 93 Shumaker D A, Zaman A, Katon R M. Use of a variable-stiffness colonoscope allows completion of colonoscopy after failure with the standard adult colonoscope.  Endoscopy. 2002;  34(9) 711-714
• 94 Campillo-Soto A, Pellicer-Franco E, Parlorio-Andres E et al. [CT colonography vs. barium enema for the preoperative study of colorectal cancer in patients with incomplete colonoscopy].  Med Clin (Barc ). 2007;  129(19) 725-728
• 95 Rosman A S, Korsten M A. Meta-analysis comparing CT colonography, air contrast barium enema, and colonoscopy.  Am J Med. 2007;  120(3) 03-210
• 96 Sosna J, Sella T, Sy O et al. Critical analysis of the performance of double-contrast barium enema for detecting colorectal polyps ≥ 6 mm in the era of CT colonography.  AJR Am J Roentgenol. 2008;  190(2) 374-385
• 97 Johnson C D, Chen M H, Toledano A Y et al. Accuracy of CT colonography for detection of large adenomas and cancers.  N Engl J Med. 2008;  359(12) 1207-1217
• 98 Kim D H, Pickhardt P J, Taylor A J et al. CT colonography versus colonoscopy for the detection of advanced neoplasia.  N Engl J Med. 2007;  357(14) 1403-1412
• 99 Pickhardt P J, Choi J R, Hwang I et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults.  N Engl J Med. 2003;  349(23) 2191-2200
• 100 Ajaj W, Lauenstein T C, Pelster G et al. MR colonography in patients with incomplete conventional colonoscopy.  Radiology. 2005;  234(2) 452-9
• 101 Hartmann D, Bassler B, Schilling D et al. Incomplete conventional colonoscopy: magnetic resonance colonography in the evaluation of the proximal colon.  Endoscopy. 2005;  37(9) 816-820
• 102 Wong T Y, Lam W W, So N M et al. Air-inflated magnetic resonance colonography in patients with incomplete conventional colonoscopy: Comparison with intraoperative findings, pathology specimens, and follow-up conventional colonoscopy.  Am J Gastroenterol. 2007;  102(1) 6-63
• 103 Nelson D B. Infectious disease complications of GI endoscopy: part II, exogenous infections.  Gastrointest Endosc. 2003;  57(6) 695-711
• 104 Multi-society guideline for reprocessing flexible gastrointestinal endoscopes.  Gastrointest Endosc. 2003;  58(1) 1-8
• 105 Cronmiller J R, Nelson D K, Salman G et al. Antimicrobial efficacy of endoscopic disinfection procedures: a controlled, multifactorial investigation.  Gastrointest Endosc. 1999;  50(2) 152-158
• 106 Fraser V J, Zuckerman G, Clouse R E et al. A prospective randomized trial comparing manual and automated endoscope disinfection methods.  Infect Control Hosp Epidemiol. 1993;  14(7) 383-389
• 107 Ortiz V, Sala T, Arguello L et al. [Comparison of the efficacy of cleaning and disinfection of videoscopes: mechanized versus manual].  Gastroenterol Hepatol. 2000;  23(9) 412-415
• 108 Santolaria S, Ducons J, Bordas J M. [Cleaning and disinfection in gastrointestinal endoscopy].  Gastroenterol Hepatol. 2007;  30(1) 25-35
• 109 Beilenhoff U, Neumann C S, Biering H et al. ESGE/ESGENA guideline for process validation and routine testing for reprocessing endoscopes in washer-disinfectors, according to the European Standard prEN ISO 15 883 parts 1, 4 and 5.  Endoscopy. 2007;  39(1) 85-94
• 110 Beilenhoff U, Neumann C S, Rey J F et al. ESGE-ESGENA guideline for quality assurance in reprocessing: microbiological surveillance testing in endoscopy.  Endoscopy. 2007;  39(2) 175-181
• 111 Radaelli F, Meucci G, Terruzzi V et al. Single bolus of midazolam versus bolus midazolam plus meperidine for colonoscopy: a prospective, randomized, double-blind trial.  Gastrointest Endosc. 2003;  57(3) 329-335
• 112 Willey J, Vargo J J, Connor J T et al. Quantitative assessment of psychomotor recovery after sedation and analgesia for outpatient EGD.  Gastrointest Endosc. 2002;  56(6) 810-816
• 113 Simon M A, Bordas J M, Campo R et al. [Consensus document of the Spanish Association of Gastroenterology on sedoanalgesia in digestive endoscopy].  Gastroenterol Hepatol. 2006;  29(3) 131-149
• 114 Bretthauer M, Hoff G, Severinsen H et al. [Systematic quality control programme for colonoscopy in an endoscopy centre in Norway].  Tidsskr Nor Laegeforen. 2004;  124(10) 1402-1405
• 115 Johanson J F, Schmitt C M, Deas T M et al. Quality and outcomes assessment in Gastrointestinal Endoscopy.  Gastrointest Endosc. 2000;  52(6 Pt 1) 827-830
• 116 Cohen L B, Delegge M H, Aisenberg J et al. AGA Institute review of endoscopic sedation.  Gastroenterology. 2007;  133(2) 675-701