Colonoscopic perforations in the English National Health Service Bowel Cancer Screening Programme

• Abstract
• Introduction
• Methods
• The Bowel Cancer Screening Programme
• Study definitions
• Statistical analysis
• Ethical approval
• Results
• Diagnostic perforations
• Therapeutic perforations
• Perforation presentation
• Perforation management
• Perforation outcomes
• Discussion
• Study limitations
• Summary
• References

Abstract

Background Perforation is the most serious adverse event associated with colonoscopy. In this study of data from the English National Health Service Bowel Cancer Screening Programme, we aimed to describe the presentation and management of perforations, and to determine factors associated with poorer outcomes post-perforation.

Methods The medical records of patients with a perforation following the national screening colonoscopy were retrospectively examined. All colonoscopies performed from 02/08/2006 to 13/03/2014 were studied. Bowel Cancer Screening Centres across England were contacted and asked to complete a detailed dataset relating to perforation presentation, management, and outcome.

Results 263 129 colonoscopies were analyzed, and the rate of perforation was 0.06 %. Complete data were reviewed for 117 perforations: 70.1 % of perforations (82/117) occurred during therapeutic colonoscopies; 54.9 % (62/113) of patients with perforations who were admitted to hospital and in whom data were complete underwent surgery; 26.1 % (30/115) of hospitalized patients left the hospital with a stoma and 19.1 % (22/115) developed post-perforation morbidity. Perforations not detected during colonoscopy were significantly more likely to require surgery (P = 0.03). Diagnostic perforations were significantly more likely to require surgery (P = 0.002) and were associated with higher rates of post-perforation morbidity (P = 0.01). At presentation, the presence of abdominal pain (P = 0.01), a pulse rate > 100 beats per minute (P = 0.049), and a respiratory rate > 20 breaths per minute (P = 0.01) were significantly associated with the patient having surgery.

Conclusions This is the largest retrospective observational case series in Europe to describe post-perforation presentation, management, and outcomes. We have confirmed that perforation leads to surgical intervention, stoma formation, and post-perforation morbidity. Perforations not recognized during the colonoscopy were significantly more likely to require surgery. Diagnostic perforations were at greater risk of requiring surgery and developing post-perforation morbidity.

Introduction

Colonoscopy is the gold standard investigation for the diagnosis and screening of colorectal diseases. It also enables the resection of precancerous polyps such as adenomas, preventing the development of colorectal cancer [1]. Despite the benefits of colonoscopy and polypectomy, the procedure is associated with adverse events, the most serious of which is perforation.

Many studies have reported perforation rates, although not all have subcategorized into those arising from diagnostic and therapeutic colonoscopies. In addition, numerous case–control studies have examined risk factors for perforation. These include patient-related factors such as age, sex, and comorbidity [2] [3] [4] [5] [6] [7] [8]. Factors relating to the procedure include polypectomy, the number of polypectomies, increasing polyp size, and a polyp location in the right colon [3] [4] [5] [6] [9] [10]. Other reported risk factors include the experience and specialty of the endoscopist [3] [4] [11] [12] [13] [14].

Fewer studies have reported the presentation, management, and outcomes of colonoscopic perforations. Those that have, describe how perforations may be managed endoscopically, conservatively or surgically. Perforation may result in hospital (including intensive care) admission, stoma formation, post-perforation morbidity, and mortality [15] [16]. Despite the identification of factors that may favor conservative management from such retrospective observational data, there is no definitive guidance as to when conservative management is safe [17] [18].

Data from the English National Health Service (NHS) Bowel Cancer Screening Programme (BCSP) have previously been published, and describe both perforation rate and risk factors for perforation [10]. The aims of this study were 1) to describe the presentation, management, and outcomes of perforations, and 2) to determine factors associated with poorer outcomes post-perforation.

Methods

The Bowel Cancer Screening Programme

The English NHS BCSP commenced in 2006. All members of the English public registered with a general practitioner are invited to take part using a guaiac-based fecal occult blood test around the time of their 60th birthday. The invitation is repeated every 2 years to the age of 74. Those with a positive test are invited for a colonoscopy. Colonoscopies are performed at 61 approved Bowel Cancer Screening Centres (BCSC) across England [19]. BCSP colonoscopists receive screening accreditation after undertaking both written and practical examinations, and have performed at least 1000 colonoscopies in their career, with a cecal intubation rate of > 90 % and an adenoma detection rate of > 20 % in the 12 months prior to starting BCSP colonoscopy [20].

Data from all colonoscopies performed in the English NHS BCSP were analyzed from 2 August 2006 to 13 March 2014.

The BCSP has a robust method for capturing adverse events, including perforation, which has previously been demonstrated to be a reliable means of capturing colonoscopy-related adverse events [20]. Data from each procedure are entered onto a single national database, the Bowel Cancer Screening System, by dedicated Specialist Screening Practitioners who are present during each procedure. The Specialist Screening Practitioner contacts the patient by telephone 24 hours after the procedure, and patients receive a questionnaire at 30 days post-procedure with questions specifically relating to perforation and whether the patient sought medical advice post-procedure (the current questionnaire return rate is 83.3 %). All BCSCs complete a detailed record for a perforation, which is flagged on the Bowel Cancer Screening System, and the event is reviewed by the regional BCSP quality assurance lead [10].

For the current study, BCSCs where perforations had occurred were contacted and asked to complete a detailed electronic dataset relating to the patient’s subsequent presentation, management, and outcome. Data were captured from a minimum of 30 days post-perforation.

Study definitions

Perforation was defined as evidence of air, luminal contents or instrumentation outside the gastrointestinal tract [21]. Diagnostic perforations were defined as those occurring at a colorectal location where no tissue had been removed from the colon or rectum or where a cold biopsy had been performed for diagnostic purposes only. Therapeutic perforations were defined as those occurring in association with polypectomy or endoscopic mucosal resection (EMR). Post-perforation morbidity was defined as any complication, either a new medical diagnosis or complication related to surgery, during the inpatient admission following presentation of the perforation.

Statistical analysis

Normally distributed continuous variables were expressed as means and non-normally distributed continuous variables were expressed as medians. Categorical variables were expressed as percentages. The Statistical Package for the Social Sciences version 20 (IBM Corp., Armonk, New York, USA) was used for data analysis. Pearson’s chi-squared, Fisher’s exact test (univariable analysis), and binomial logistic regression (multivariable analysis) were used to test the association between explanatory and outcome variables, with a P value of < 0.05 considered to be significant.

Ethical approval

Ethical approval to conduct the study was given by the Newcastle and North Tyneside 2 local Regional Ethics Committee of the NHS Health Research Authority.

Results

A total of 263 129 colonoscopies were performed during the study period. Of these, 60.5 % were performed in men. The mean patient age was 65.5 years. In total, 147 patients with a perforation were identified, which is a rate of 0.06 % per colonoscopy, or 1 in 1790 procedures. [Table 1] shows the baseline patient characteristics of the 147 patients.

Complete electronic data were received from BCSCs on 117 perforations. For the 30 patients in whom complete data were not received, limited data were available on the screening system relating to the patients’ management and outcome. To ensure that the complete data received broadly represented the total number of perforations, a comparison between the complete (n = 117) and incomplete (n = 30) data groups was performed ([Table 2]).

The colorectal location of the perforation was not recorded in 7.7 % of patients (9/117). Overall, 70.1 % of perforations (82/117) were therapeutic, 18.8 % (22/117) were diagnostic, and in the remaining 11.1 % (13/117) it was either unclear whether any therapy had taken place at the site of the perforation or the colorectal location of the perforation was unknown.

Diagnostic perforations

[Fig. 1] shows the colorectal location of the diagnostic perforations. Of the diagnostic perforations in the sigmoid colon, 50 % (6 /12) had diverticula in the sigmoid colon, compared with the 30.4 % (80 023/263 129) of colonoscopies overall in the study (P = 0.08). Overall, 31.8 % (7/22) of the diagnostic perforations were at colorectal locations where a cold biopsy had been performed for diagnostic purposes, including five patients with colorectal cancer. Four of these five perforations were asymptomatic radiologically detected perforations that were seen on staging computed tomography (CT) scans for colorectal cancer. It was unclear whether these perforations resulted from the cold biopsy, or the cancer. The other two diagnostic perforations associated with cold biopsies were in the cecum.

Therapeutic perforations

[Fig. 2] shows the colorectal location of the therapeutic perforations. Of the therapeutic perforations, 95.1 % (78/82) were associated with a single polypectomy or EMR at the site of the perforation; in the remaining 4.9 % (4/82), multiple polypectomies or EMRs had taken place at the site of the perforation. When examining the single polypectomies or EMRs associated with a therapeutic perforation, 30.8 % (24/78) were Paris classification Ip polyps, the majority of which (70.8 %; 17/24) were in the sigmoid colon. Of the 14 single polypectomies or EMRs associated with therapeutic perforation in the cecum, all bar one were Paris classification Is polyps. EMR of four laterally spreading tumors (three granular type and one nongranular type), ranging from 15 mm to 60 mm, were also associated with therapeutic perforation. Overall polyp size ranged from 2 mm to 60 mm, with a median polyp size of 19 mm. Two cold therapy polypectomies were associated with therapeutic perforation (a cold biopsy polypectomy of a 2-mm Is polyp in the cecum and a cold snare polypectomy of a 9-mm Ip polyp in the sigmoid colon).

Perforation presentation

In 12.8 % (15/117), the perforation presented during the colonoscopy, and the endoscopist visualized the perforation and applied endoclips in 80.0 % (12/15) of those visualized. The estimated endoscopic size of the perforations visualized by the endoscopist was documented in 8 of the 15 patients. Six of these perforations ranged from 1.5 mm to 8 mm, with a further two of 15 mm and 25 mm, respectively. The endoscopists visualized a tear in the serosa (n = 6), a defect in the muscularis propria (n = 4), and an extraintestinal structure (n = 3), such as that shown in [Fig. 3]. One endoscopist saw the endoscopy knife pass through the colon, and a further endoscopist visualized the perforation but what was seen was not documented. [Table 3] shows the outcomes for those perforations visualized and not visualized by the endoscopist at the time of the colonoscopy.

Of the perforations visualized by the endoscopist and where an endoclip had been applied, such as that shown in [Fig. 4], 83.3 % (10 /12) were successfully managed conservatively without the need for surgery. However, the association between using endoclips and the need for surgery did not reach statistical significance in this small cohort of patients who were admitted to hospital (P = 0.42).

A total of 115 patients with colonoscopic perforation were admitted acutely to hospital. [Fig. 5] summarizes how these patients presented. A total of 77 patients were discharged and subsequently presented with symptoms; however, it was unclear whether these patients had any symptoms at the time of discharge. Two perforations, subclinical CT-detected perforations found on staging scans for colorectal cancers, were not admitted to hospital. A further two patients were recalled to hospital following staging scans for colorectal cancer. Of those patients admitted to hospital, median time to presentation was 1 day in 87 patients, with time to presentation being unclear in the remaining 28 cases. [Fig. 6] shows the time to presentation in patients who had symptoms. [Table 1] includes the initial observations of the 115 patients with perforation who were admitted to hospital.

Perforation management

Whether or not surgery had occurred was recorded in 113 patients admitted to hospital; 54.9 % of these patients (62/113) underwent surgery. [Table 4] summarizes how patients who were managed surgically and conservatively presented. [Table 5] summarizes the operations.

Perforation outcomes

The colorectal location of the perforation in patients who underwent surgery was not recorded for three patients, including one operation necessitating a stoma. The operations performed resulted in 48.4 % (30/62) of patients who had surgery leaving hospital with a stoma, which is 26.1 % (30/115) of all patients with perforations who were admitted to hospital. The sigmoid colon was the commonest colorectal location of a perforation that required a stoma (n = 18), although all three patients who had surgery following a perforation in the rectum also underwent stoma formation. Male sex (P = 0.02) and a perforation located in the sigmoid colon when compared with all other colorectal locations (P = 0.001) were significantly associated with stoma formation.

In 53 patients the grade of the surgeon performing the operation was recorded; consultant surgeons performed the majority of operations (81.1 %; 43/53). In those patients who underwent surgery, nonconsultant surgeon was significantly associated with stoma formation (P = 0.03).

Only those patients who underwent surgery developed post-perforation morbidity at 30 days – 19.1 % (22/115) of perforations admitted to hospital. Post-perforation morbidity included cardiorespiratory morbidity (n = 8), wound-related morbidity (n = 7), ileus (n = 6), and pelvic collection (n = 1). In all 115 patients admitted to hospital, the length of hospital stay ranged from 0 days to 51 days, with a median stay of 6 days.

One patient died, giving a 30-day mortality rate of 0.87 % (1/115). This patient who was American Society of Anesthesiologists grade 2, presented with abdominal pain following a diagnostic colonoscopy showing diverticular disease in the sigmoid colon. The patient was found to have a sigmoid perforation, underwent a Hartmann’s procedure, and was admitted to the intensive care unit. The patient developed post-perforation morbidity including mucus plugging, a pneumothorax, and small-bowel ischemia. The patient died 6 days following admission.

[Table 6] compares the outcomes of patients admitted following a diagnostic and therapeutic perforation.

Discussion

This is the largest study in Europe to specifically describe the presentation, management, and outcome of post-colonoscopic perforation. We have shown that diagnostic perforations were significantly associated with having surgery and post-perforation morbidity.

The overall perforation rate of 0.06 % reported in this study is reassuring when compared with other rates outlined in [Table 7]. It is also in line with the 0.05 % perforation rate reported in a meta-analysis of post-colonoscopy complications from 1 966 340 colonoscopies reported by Reumkens et al. [32]. Our study reports a lower perforation rate than series prior to 1990, which reported rates of 0.12 % – 0.48 % [24] [25]. Four similarly sized series published since 2008 report rates of 0.03 % – 0.08 %, suggesting that the figure in the current work is in line with current global data [3] [5] [16] [31]. Although these figures are reassuring for the BCSP, perforation rates have to be interpreted and compared within the context of the indication and nature of the colonoscopy; our data were from the BCSP in which just under half of colonoscopies (47.2 %) were diagnostic examinations [10].

The majority of perforations in our study occurred as a result of therapy. Although the breakdown of diagnostic and therapeutic colonoscopies in the study was not recorded, data previously published from the NHS BCSP showed that over half (52.8 %) of the colonoscopies in the programme are therapeutic [10]. These results are in contrast to other large studies of over 100 000 colonoscopies, where greater numbers of diagnostic procedures were performed and diagnostic perforations occurred [5] [16] [29]. The overall therapeutic perforation rate in the current study was 0.03 % and the diagnostic perforation rate was 0.008 %. The fewer number of diagnostic perforations may simply reflect the fact that the majority of procedures in the BCSP are therapeutic in nature.

The sigmoid colon (n = 40) and cecum (n = 22) were the commonest colorectal locations of perforations; 70.0 % (28/40) of the perforations in the sigmoid colon and 72.7 % (16/22) in the cecum were therapeutic. The finding that the majority of perforations occurred in these two colorectal locations is consistent with the only other study describing outcomes following a larger (n = 165) number of perforations [16]. Our data reinforce our knowledge of the mechanisms associated with perforation. In the BCSP, the majority of therapy occurs in the sigmoid colon, as this is where the majority of polyps are found. Similarly, when considering therapeutic polypectomy, it is the cecal location, as opposed to any other colonic location, that is significantly associated with therapeutic perforation as reported by Rutter et al. [10]. One hypothesis for this is the thinness of the cecal wall compared with other colorectal locations. A second possible explanation is that therapy in the cecum is often performed perpendicularly to the mucosa compared with a more tangential approach in other colorectal locations [10]. In our study, the only perforation associated with a cold biopsy polypectomy occurred in the cecum, where these hypotheses may have been relevant. When diagnostic perforations were specifically examined, the colorectal locations again reinforce our knowledge of the mechanisms of diagnostic perforation. Indeed, sigmoid diverticula was present in 50 % of the sigmoid diagnostic perforations, compared with only 30 % in the overall cohort; although this did not reach statistical significance, this might be due to type II error, and it is certainly plausible that diverticula may contribute to some diagnostic perforations. The sigmoid colon is also the segment where the majority of looping occurs. Loop resolution and sheer forces generated by “pushing through a loop” may account for a proportion of sigmoid diagnostic perforations. Diagnostic perforations occurring in the cecum from “air trapping” or barotrauma are recognized; although our data cannot corroborate this mechanism, it is a plausible explanation for the higher diagnostic perforation rate seen in this location.

Within the subgroup of diagnostic perforations in the study, four were in asymptomatic patients and were detected radiologically on staging CT scans for colorectal cancer. In two of these patients, the TNM staging was at least T4 (T4N1M0 and T4N2M0, respectively), which would be consistent with these cancers penetrating the serosa; however, one was T3N0M0. We should also be aware that these perforations are likely only ever to be seen in association with colorectal cancer, as only these patients would undergo a CT scan when asymptomatic.

The number of perforations visualized by the endoscopist (12.8 %) was less than that described by other series, which range from 23 % to 37.5 % [17] [33]. It may be that the perforations in the current study were smaller and therefore more difficult to detect, although size is not specifically mentioned in the abovementioned papers. The smaller number of diagnostic perforations in our study may also go some way to explaining this, as diagnostic perforations have been reported to be larger [15] [34] [35] [36].

Where the perforation was visualized, our data suggest that not only is the patient less likely to require surgery but also that the use of an endoclip to close the perforation may improve patient outcomes; 83.3 % of those perforations that were visualized by the endoscopist and had endoclips applied were successfully managed endoscopically and conservatively without the need for surgery, although this association did not reach statistical significance. This figure is consistent with the 68 % – 93 % of patients reported as being successfully managed in this way by other studies [37] [38] [39] [40]. A study by Burgess et al. specifically advocates the use of endoclips following EMR in cases where there is any deep focal loss of the submucosal plane, raising concern for muscularis propria injury or rendering a muscularis propria defect uninterpretable, for an actual muscularis propria defect, or for a complete hole in the muscularis propria [41]. With increasing endoscopist experience and skill in using endoscopic closure devices and improvements in the technologies (including endoclips, suturing devices, and over-the-scope clips), there is increasing potential to manage perforations endoscopically at the time of the procedure.

Our work has identified that patients who were managed conservatively, with or without the use of endoclips, did not develop post-perforation morbidity. This, of course, may reflect the fact that patients with perforations undergoing surgery are likely to be more unwell at presentation and are, therefore, perhaps, more likely to have surgery and post-operative complications. However, it also follows that, where possible, conservative management should be attempted. Specific indicators that can guide a clinician as to when it is safe to manage a colonoscopic perforation conservatively have yet to be conclusively established. Although our data have shown that those patients who have abdominal pain, with a respiratory rate of > 20 breaths per minute, and a pulse rate of > 100 beats per minute at initial presentation were significantly more likely to have surgery, these factors cannot currently be used on the basis of our data alone to inform clinician decision making regarding perforation management. A small proportion of patients with no abdominal pain, a pulse rate ≤ 100 beats per minute, and a respiratory rate of ≤ 20 breaths per minute still underwent surgery – it is unclear from our data, however, whether this surgery was actually necessary. Further research using these predictors in order to create a management algorithm may be worthwhile.

Male sex and perforation in the sigmoid colon were significantly associated with stoma formation. The latter is not unsurprising, as the majority of perforations in the sigmoid colon underwent a Hartmann’s procedure, particularly in the case of the diagnostic perforations, where there may be greater fecal contamination. With regard to male sex, 76.7 % (23/30) of the stomas formed were in men. The reason for this is not clear. One explanation could be that men have longer sigmoid colons, which are more likely to loop during intubation with consequent diagnostic perforation. The experience of the surgeon was also an important factor in stoma formation; nonconsultant surgeons were significantly more likely to perform an operation where a stoma was formed.

Although any death associated with a screening investigation is disappointing, a 30-day post-perforation mortality rate of 0.87 % does compare favorably with other series that have reported mortality, both overall post-perforation and for post-perforation surgery.

Study limitations

The main limitation of our study is the retrospective design. Thus, on analysis of patient records, some data were unclear or could not be traced. Data were incomplete for 30 of the 147 perforations in the study. The nonsignificant differences reported suggest that the perforations in the incomplete data group were predominantly less likely to have had poorer outcomes. A larger complete data group may have added further weight to our findings.

It is also possible that some perforations were not captured on the screening system, and therefore may have been missed. However, we have previously demonstrated that the BCSP has a robust system for capturing the details of adverse events, so we think this is unlikely to be a significant issue.

Summary

This is the largest study in Europe to specifically describe the presentation, management, and outcomes of colonoscopic perforation. A perforation rate of 0.06 % is in line with other similarly sized series reported globally. We have reported the successful use of endoclips to close perforations in 83.3 % of cases where the perforation was visualized by the endoscopist. The absence of abdominal pain at initial review, a pulse rate ≤ 100 beats per minute, and a respiratory rate ≤ 20 breaths per minute were predictors of successful conservative management. Over half of the patients with perforations in the study underwent surgery, and half of these required a stoma. Diagnostic perforations were significantly associated with surgery and post-perforation morbidity, and the sigmoid colon was significantly associated with stoma formation. No post-perforation morbidity was identified in those who were managed conservatively.

Competing interests

None.

• References

• 1 Gavin DR, Valori RM, Anderson JT. et al. The national colonoscopy audit: a nationwide assessment of the quality and safety of colonoscopy in the UK. Gut 2013; 62: 242-249
  CrossrefPubMedSearch in Google Scholar
• 2 Gatto NM, Frucht H, Sundararajan V. et al. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J Natl Cancer Inst 2003; 95: 230-236
  CrossrefPubMedSearch in Google Scholar
• 3 Blotière P-O, Weill A, Ricordeau P. et al. Perforations and haemorrhages after colonoscopy in 2010: a study based on comprehensive French health insurance data (SNIIRAM). Clin Res Gastroenterol Hepatol 2014; 38: 112-117
  PubMedSearch in Google Scholar
• 4 Rabeneck L, Paszat LF, Hilsden RJ. et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice. Gastroenterology 2008; 135: 1899-1906
  CrossrefPubMedSearch in Google Scholar
• 5 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: 654-664
  CrossrefPubMedSearch in Google Scholar
• 6 Lohsiriwat V, Sujarittanakarn S, Akaraviputh T. et al. What are the risk factors of colonoscopic perforation?. BMC Gastroenterol 2009; 9: 71
  CrossrefPubMedSearch in Google Scholar
• 7 Hamdani U, Naeem R, Haider F. et al. Risk factors for colonoscopic perforation: a population-based study of 80118 cases. World J Gastroenterol 2013; 19: 3596-3601
  CrossrefPubMedSearch in Google Scholar
• 8 Warren JL, Klabunde CN, Mariotto AB. et al. Adverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med 2009; 150: 849-858
  CrossrefPubMedSearch in Google Scholar
• 9 Heldwein W, Dollhopf M, Meining A. et al. The Munich Polypectomy Study (MUPS): prospective analysis of complications and risk factors in 4000 colonic snare polypectomies. Endoscopy 2005; 37: 1116-1122
  Thieme ConnectPubMedSearch in Google Scholar
• 10 Rutter M, Nickerson C, Rees C. et al. Risk factors for adverse events related to polypectomy in the English Bowel Cancer Screening Programme. Endoscopy 2014; 46: 90-97
  Thieme ConnectPubMedSearch in Google Scholar
• 11 Hayashi N, Tanaka S, Nishiyama S. et al. Predictors of incomplete resection and perforation associated with endoscopic submucosal dissection for colorectal tumors. Gastrointest Endosc 2014; 79: 427-435
  CrossrefPubMedSearch in Google Scholar
• 12 Singh H, Penfold RB, Moffatt M. Predictors of serious complications associated with lower gastrointestinal endoscopy in a major city-wide health region. Can J Gastroenterol 2010; 24: 425-430
  CrossrefPubMedSearch in Google Scholar
• 13 Chukmaitov A, Bradley CJ, Dahman B. et al. Association of polypectomy techniques, endoscopist volume, and facility type with colonoscopy complications. Gastrointest Endosc 2012; 77: 436-446
  PubMedSearch in Google Scholar
• 14 Lorenzo-Zúñiga V, Moreno de Vega V, Doménech E. et al. Endoscopist experience as a risk factor for colonoscopic complications. Colorectal Dis 2010; 12: 273-277
  CrossrefPubMedSearch in Google Scholar
• 15 Iqbal CW, Chun YS, Farley DR. Colonoscopic perforations: a retrospective review. J Gastrointest Surg 2005; 9: 1229-1235
  CrossrefPubMedSearch in Google Scholar
• 16 Iqbal CW, Cullinane DC, Schiller HJ. et al. Surgical management and outcomes of 165 colonoscopic perforations from a single institution. Arch Surg 2008; 143: 701-707
  CrossrefPubMedSearch in Google Scholar
• 17 Panteris V, Haringsma J, Kuipers EJ. Colonoscopy perforation rate, mechanisms and outcome: from diagnostic to therapeutic colonoscopy. Endoscopy 2009; 41: 941-951
  Thieme ConnectPubMedSearch in Google Scholar
• 18 Castellví J, Pi F, Sueiras A. et al. Colonoscopic perforation: useful parameters for early diagnosis and conservative treatment. Int J Colorectal Dis 2011; 26: 1183-1190
  CrossrefPubMedSearch in Google Scholar
• 19 Logan RF, Patnick J, Nickerson C. et al. Outcomes of the Bowel Cancer Screening Programme (BCSP) in England after the first 1 million tests. Gut 2012; 61: 1439-1446
  CrossrefPubMedSearch in Google Scholar
• 20 Lee TJW, Rutter MD, Blanks RG. et al. Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme. Gut 2012; 61: 1050-1057
  CrossrefPubMedSearch in Google Scholar
• 21 Rembacken B, Hassan C, Riemann JF. et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 2012; 44: 957-968
  Thieme ConnectPubMedSearch in Google Scholar
• 22 Rogers BH, Silvis SE, Nebel OT. et al. Complications of flexible fiberoptic colonoscopy and polypectomy. Gastrointest Endosc 1975; 22: 73-77
  CrossrefPubMedSearch in Google Scholar
• 23 Smith LE. Fiberoptic colonoscopy: complications of colonoscopy and polypectomy. Dis Colon Rectum 1976; 19: 407-412
  CrossrefPubMedSearch in Google Scholar
• 24 Frumorghen P, Demling L. Complications of diagnostic and therapeutic colonoscopy in the Federal Republic of Germany. Results of an inquiry. Endoscopy 1979; 11: 146-150
  Thieme ConnectPubMedSearch in Google Scholar
• 25 Macrae FA, Tan KG, Williams CB. Towards safer colonoscopy: a report on the complications of 5000 diagnostic or therapeutic colonoscopies. Gut 1983; 24: 376-383
  CrossrefPubMedSearch in Google Scholar
• 26 Hall C, Dorricot N, Donovan I. et al. Colon perforation during colonoscopy: surgical versus conservative management. Br J Surg 1991; 78: 542-544
  CrossrefPubMedSearch in Google Scholar
• 27 Lo AY, Beaton HL. Selective management of colonoscopic perforations. J Am Coll Surg 1994; 179: 333-337
  PubMedSearch in Google Scholar
• 28 Farley DR, Bannon MP, Zietlow SP. et al. Management of colonoscopic perforations. Mayo Clinica Proceedings 1997; 72: 729-723
  PubMedSearch in Google Scholar
• 29 Avgerinos DV, Llaguna OH, Lo AY. et al. Evolving management of colonoscopic perforations. J Gastrointest Surg 2008; 12: 1783-1789
  CrossrefPubMedSearch in Google Scholar
• 30 Korman LY, Overholt BF, Box T. et al. Perforation during colonoscopy in endoscopic ambulatory surgical centers. Gastrointest Endosc 2003; 58: 554-557
  CrossrefPubMedSearch in Google Scholar
• 31 Crispin A, Birkner B, Munte A. et al. Process quality and incidence of acute complications in a series of more than 230,000 outpatient colonoscopies. Endoscopy 2009; 41: 1018-1025
  Thieme ConnectPubMedSearch in Google Scholar
• 32 Reumkens A, Rondagh EJA, Bakker CM. et al. Post-colonoscopy complications: a systematic review, time trends, and meta-analysis of population-based studies. Am J Gastroenterol 2016; 111: 1092-1101
  CrossrefPubMedSearch in Google Scholar
• 33 Sagawa T, Kakizaki S, Iizuka H. et al. Analysis of colonoscopic perforations at a local clinic and a tertiary hospital. World J Gastroenterol 2012; 18: 4898-4904
  CrossrefPubMedSearch in Google Scholar
• 34 Teoh AYB, Poon CM, Lee JFY. et al. Outcomes and predictors of mortality and stoma formation in surgical management of colonoscopic perforations: a multicenter review. Arch Surg 2009; 144: 9-13
  CrossrefPubMedSearch in Google Scholar
• 35 Dafnis G, Ekbom A, Pahlman L. et al. Complications of diagnostic and therapeutic colonoscopy within a defined population in Sweden. Gastrointest Endosc 2001; 54: 302-309
  CrossrefPubMedSearch in Google Scholar
• 36 Cai S, Chen T, Yao L. et al. Management of iatrogenic colorectal perforation: from surgery to endoscopy. World J Gastroenterol 2015; 7: 819-823
  CrossrefPubMedSearch in Google Scholar
• 37 Magdeburg R, Collet P, Post S. et al. Endoclipping of iatrogenic colonic perforation to avoid surgery. Surg Endosc 2008; 22: 1500-1504
  CrossrefPubMedSearch in Google Scholar
• 38 Yang D-H, Byeon J-S, Lee K-H. et al. Is endoscopic closure with clips effective for both diagnostic and therapeutic colonoscopy-associated bowel perforation?. Surg Endosc 2010; 24: 1177-1185
  CrossrefPubMedSearch in Google Scholar
• 39 Jovanovic I, Zimmermann L, Fry LC. et al. Feasibility of endoscopic closure of an iatrogenic colon perforation occurring during colonoscopy. Gastrointest Endosc 2011; 73: 550-555
  CrossrefPubMedSearch in Google Scholar
• 40 Kim JS, Kim B-W, Kim JIl. et al. Endoscopic clip closure versus surgery for the treatment of iatrogenic colon perforations developed during diagnostic colonoscopy: a review of 115,285 patients. Surg Endosc 2013; 27: 501-504
  CrossrefPubMedSearch in Google Scholar
• 41 Burgess NG, Bassan MS, McLeod D. et al. Deep mural injury and perforation after colonic endoscopic mucosal resection: a new classification and analysis of risk factors. Gut 2016; 0: 1-11
  PubMedSearch in Google Scholar

Corresponding author

• References

• 1 Gavin DR, Valori RM, Anderson JT. et al. The national colonoscopy audit: a nationwide assessment of the quality and safety of colonoscopy in the UK. Gut 2013; 62: 242-249
  CrossrefPubMedSearch in Google Scholar
• 2 Gatto NM, Frucht H, Sundararajan V. et al. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J Natl Cancer Inst 2003; 95: 230-236
  CrossrefPubMedSearch in Google Scholar
• 3 Blotière P-O, Weill A, Ricordeau P. et al. Perforations and haemorrhages after colonoscopy in 2010: a study based on comprehensive French health insurance data (SNIIRAM). Clin Res Gastroenterol Hepatol 2014; 38: 112-117
  PubMedSearch in Google Scholar
• 4 Rabeneck L, Paszat LF, Hilsden RJ. et al. Bleeding and perforation after outpatient colonoscopy and their risk factors in usual clinical practice. Gastroenterology 2008; 135: 1899-1906
  CrossrefPubMedSearch in Google Scholar
• 5 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: 654-664
  CrossrefPubMedSearch in Google Scholar
• 6 Lohsiriwat V, Sujarittanakarn S, Akaraviputh T. et al. What are the risk factors of colonoscopic perforation?. BMC Gastroenterol 2009; 9: 71
  CrossrefPubMedSearch in Google Scholar
• 7 Hamdani U, Naeem R, Haider F. et al. Risk factors for colonoscopic perforation: a population-based study of 80118 cases. World J Gastroenterol 2013; 19: 3596-3601
  CrossrefPubMedSearch in Google Scholar
• 8 Warren JL, Klabunde CN, Mariotto AB. et al. Adverse events after outpatient colonoscopy in the Medicare population. Ann Intern Med 2009; 150: 849-858
  CrossrefPubMedSearch in Google Scholar
• 9 Heldwein W, Dollhopf M, Meining A. et al. The Munich Polypectomy Study (MUPS): prospective analysis of complications and risk factors in 4000 colonic snare polypectomies. Endoscopy 2005; 37: 1116-1122
  Thieme ConnectPubMedSearch in Google Scholar
• 10 Rutter M, Nickerson C, Rees C. et al. Risk factors for adverse events related to polypectomy in the English Bowel Cancer Screening Programme. Endoscopy 2014; 46: 90-97
  Thieme ConnectPubMedSearch in Google Scholar
• 11 Hayashi N, Tanaka S, Nishiyama S. et al. Predictors of incomplete resection and perforation associated with endoscopic submucosal dissection for colorectal tumors. Gastrointest Endosc 2014; 79: 427-435
  CrossrefPubMedSearch in Google Scholar
• 12 Singh H, Penfold RB, Moffatt M. Predictors of serious complications associated with lower gastrointestinal endoscopy in a major city-wide health region. Can J Gastroenterol 2010; 24: 425-430
  CrossrefPubMedSearch in Google Scholar
• 13 Chukmaitov A, Bradley CJ, Dahman B. et al. Association of polypectomy techniques, endoscopist volume, and facility type with colonoscopy complications. Gastrointest Endosc 2012; 77: 436-446
  PubMedSearch in Google Scholar
• 14 Lorenzo-Zúñiga V, Moreno de Vega V, Doménech E. et al. Endoscopist experience as a risk factor for colonoscopic complications. Colorectal Dis 2010; 12: 273-277
  CrossrefPubMedSearch in Google Scholar
• 15 Iqbal CW, Chun YS, Farley DR. Colonoscopic perforations: a retrospective review. J Gastrointest Surg 2005; 9: 1229-1235
  CrossrefPubMedSearch in Google Scholar
• 16 Iqbal CW, Cullinane DC, Schiller HJ. et al. Surgical management and outcomes of 165 colonoscopic perforations from a single institution. Arch Surg 2008; 143: 701-707
  CrossrefPubMedSearch in Google Scholar
• 17 Panteris V, Haringsma J, Kuipers EJ. Colonoscopy perforation rate, mechanisms and outcome: from diagnostic to therapeutic colonoscopy. Endoscopy 2009; 41: 941-951
  Thieme ConnectPubMedSearch in Google Scholar
• 18 Castellví J, Pi F, Sueiras A. et al. Colonoscopic perforation: useful parameters for early diagnosis and conservative treatment. Int J Colorectal Dis 2011; 26: 1183-1190
  CrossrefPubMedSearch in Google Scholar
• 19 Logan RF, Patnick J, Nickerson C. et al. Outcomes of the Bowel Cancer Screening Programme (BCSP) in England after the first 1 million tests. Gut 2012; 61: 1439-1446
  CrossrefPubMedSearch in Google Scholar
• 20 Lee TJW, Rutter MD, Blanks RG. et al. Colonoscopy quality measures: experience from the NHS Bowel Cancer Screening Programme. Gut 2012; 61: 1050-1057
  CrossrefPubMedSearch in Google Scholar
• 21 Rembacken B, Hassan C, Riemann JF. et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 2012; 44: 957-968
  Thieme ConnectPubMedSearch in Google Scholar
• 22 Rogers BH, Silvis SE, Nebel OT. et al. Complications of flexible fiberoptic colonoscopy and polypectomy. Gastrointest Endosc 1975; 22: 73-77
  CrossrefPubMedSearch in Google Scholar
• 23 Smith LE. Fiberoptic colonoscopy: complications of colonoscopy and polypectomy. Dis Colon Rectum 1976; 19: 407-412
  CrossrefPubMedSearch in Google Scholar
• 24 Frumorghen P, Demling L. Complications of diagnostic and therapeutic colonoscopy in the Federal Republic of Germany. Results of an inquiry. Endoscopy 1979; 11: 146-150
  Thieme ConnectPubMedSearch in Google Scholar
• 25 Macrae FA, Tan KG, Williams CB. Towards safer colonoscopy: a report on the complications of 5000 diagnostic or therapeutic colonoscopies. Gut 1983; 24: 376-383
  CrossrefPubMedSearch in Google Scholar
• 26 Hall C, Dorricot N, Donovan I. et al. Colon perforation during colonoscopy: surgical versus conservative management. Br J Surg 1991; 78: 542-544
  CrossrefPubMedSearch in Google Scholar
• 27 Lo AY, Beaton HL. Selective management of colonoscopic perforations. J Am Coll Surg 1994; 179: 333-337
  PubMedSearch in Google Scholar
• 28 Farley DR, Bannon MP, Zietlow SP. et al. Management of colonoscopic perforations. Mayo Clinica Proceedings 1997; 72: 729-723
  PubMedSearch in Google Scholar
• 29 Avgerinos DV, Llaguna OH, Lo AY. et al. Evolving management of colonoscopic perforations. J Gastrointest Surg 2008; 12: 1783-1789
  CrossrefPubMedSearch in Google Scholar
• 30 Korman LY, Overholt BF, Box T. et al. Perforation during colonoscopy in endoscopic ambulatory surgical centers. Gastrointest Endosc 2003; 58: 554-557
  CrossrefPubMedSearch in Google Scholar
• 31 Crispin A, Birkner B, Munte A. et al. Process quality and incidence of acute complications in a series of more than 230,000 outpatient colonoscopies. Endoscopy 2009; 41: 1018-1025
  Thieme ConnectPubMedSearch in Google Scholar
• 32 Reumkens A, Rondagh EJA, Bakker CM. et al. Post-colonoscopy complications: a systematic review, time trends, and meta-analysis of population-based studies. Am J Gastroenterol 2016; 111: 1092-1101
  CrossrefPubMedSearch in Google Scholar
• 33 Sagawa T, Kakizaki S, Iizuka H. et al. Analysis of colonoscopic perforations at a local clinic and a tertiary hospital. World J Gastroenterol 2012; 18: 4898-4904
  CrossrefPubMedSearch in Google Scholar
• 34 Teoh AYB, Poon CM, Lee JFY. et al. Outcomes and predictors of mortality and stoma formation in surgical management of colonoscopic perforations: a multicenter review. Arch Surg 2009; 144: 9-13
  CrossrefPubMedSearch in Google Scholar
• 35 Dafnis G, Ekbom A, Pahlman L. et al. Complications of diagnostic and therapeutic colonoscopy within a defined population in Sweden. Gastrointest Endosc 2001; 54: 302-309
  CrossrefPubMedSearch in Google Scholar
• 36 Cai S, Chen T, Yao L. et al. Management of iatrogenic colorectal perforation: from surgery to endoscopy. World J Gastroenterol 2015; 7: 819-823
  CrossrefPubMedSearch in Google Scholar
• 37 Magdeburg R, Collet P, Post S. et al. Endoclipping of iatrogenic colonic perforation to avoid surgery. Surg Endosc 2008; 22: 1500-1504
  CrossrefPubMedSearch in Google Scholar
• 38 Yang D-H, Byeon J-S, Lee K-H. et al. Is endoscopic closure with clips effective for both diagnostic and therapeutic colonoscopy-associated bowel perforation?. Surg Endosc 2010; 24: 1177-1185
  CrossrefPubMedSearch in Google Scholar
• 39 Jovanovic I, Zimmermann L, Fry LC. et al. Feasibility of endoscopic closure of an iatrogenic colon perforation occurring during colonoscopy. Gastrointest Endosc 2011; 73: 550-555
  CrossrefPubMedSearch in Google Scholar
• 40 Kim JS, Kim B-W, Kim JIl. et al. Endoscopic clip closure versus surgery for the treatment of iatrogenic colon perforations developed during diagnostic colonoscopy: a review of 115,285 patients. Surg Endosc 2013; 27: 501-504
  CrossrefPubMedSearch in Google Scholar
• 41 Burgess NG, Bassan MS, McLeod D. et al. Deep mural injury and perforation after colonic endoscopic mucosal resection: a new classification and analysis of risk factors. Gut 2016; 0: 1-11
  PubMedSearch in Google Scholar