Risk of post-colonoscopy colorectal cancer in Denmark: time trends and comparison with Sweden and the English National Health Service

• Abstract
• Introduction
• Methods
• Data sources
• Identifying cancers, colonoscopies, and comorbidities
• Denmark compared with England
• Denmark compared with Sweden
• Factors associated with PCCRC
• Risk of PCCRC over time: WEO consensus method
• Statistical methods
• Results
• Denmark compared with England
• Denmark compared with Sweden
• Factors associated with PCCRC
• Risk of PCCRC over time: WEO consensus method
• Discussion
• References

Abstract

Background The post-colonoscopy colorectal cancer (PCCRC) rate is a key quality indicator for colonoscopy. Previously published PCCRC rates have been difficult to compare owing to differences in methodology. The primary aim of this study was to compare Danish PCCRC rates internationally and to calculate Danish PCCRC rates using the World Endoscopy Organization (WEO) consensus method for future comparison. The secondary aim was to identify factors associated with PCCRC.

Methods National registries were used to examine the risk of PCCRC. The Danish 3-year rate of PCCRC (PCCRC-3yr) was calculated using previously published methods from England, Sweden, and the WEO. Poisson regression analysis was performed to identify factors associated with PCCRC.

Results The Danish PCCRC-3yr was significantly higher than the rate in the English NHS (relative risk [RR] 1.12, 95 % confidence interval [CI] 1.05 – 1.19) and Sweden (RR 1.15, 95 %CI 1.06 – 1.24). The Danish PCCRC-3yr based on the WEO consensus method fell from 22.5 % in 2001 to 7.9 % in 2012. The multivariable Poisson regression model found PCCRC to be significantly associated with diverticulitis (RR 3.25, 95 %CI 2.88 – 3.66), ulcerative colitis (RR 3.44, 95 %CI 2.79 – 4.23), hereditary cancer (age < 60 years: RR 7.39, 95 %CI 5.77 – 9.47; age ≥ 60 years: RR 3.81, 95 %CI 2.74 – 5.31), and location in the transverse (RR 1.57, 95 %CI 1.28 – 1.94) and ascending colon (RR 1.85, 95 %CI 1.64 – 2.08).

Conclusions The PCCRC-3yr was higher in Denmark than in comparable countries. Differences in colonoscopist training, background, and certification are possible contributing factors. A review of colonoscopist training and certification in Denmark, and continuous audit and feedback of colonoscopist performance may reduce PCCRC-3yr.

Introduction

The incidence of colorectal cancer (CRC) in Denmark is among the highest in the world [1], and with almost 5000 cases annually, it has become the third most common cancer in Denmark [2]. The preferred diagnostic procedure is colonoscopy, either for symptomatic patients or as a follow-up screening test because it can both diagnose cancer and remove pre-cancerous lesions. Unfortunately, CRC is known to occur after a negative colonoscopy (a colonoscopy that does not diagnose cancer). CRC occurring after a negative colonoscopy is known as interval or post-colonoscopy colorectal cancer (PCCRC) [3]. For benchmarking purposes, the World Endoscopy Organization (WEO) recommends a time frame of PCCRC occurring within 3 years of a colonoscopy (PCCRC-3yr) [4] [5].

Until recently, there has been no universally accepted method of calculating the PCCRC-3yr, and rates vary considerably depending on the method used to calculate them [4] [6] [7] [8] [9]. Danish registries enable calculation of the PCCRC-3yr using the different methodologies used previously to calculate the PCCRC-3yr, including those of the English National Health Service (NHS) and Sweden. This allows a direct comparison between colonoscopy services at a national level.

The primary aim of this study was to evaluate the Danish PCCRC-3yr and compare it with the English NHS and the Swedish health system. The Danish PCCRC-3yr based on the WEO method is presented for future reference [5]. The secondary aim was to investigate factors associated with PCCRC.

Methods

Data sources

Data for this population-based cohort study were obtained from two primary sources: the Danish Cancer Registry and the Danish National Patient Registry [10] [11]. The Danish Cancer Registry contains information about every Danish cancer event with mandatory reporting since 1987. The data include date of diagnosis, histology, stage (Dukes classification until 2003, TNM classification from 2004), and International Classification of Disease 10 (ICD-10). Data dating from 1978 – 2003 were originally coded according to ICD-7, but have subsequently been recoded to ICD-10 by the Danish Cancer Registry. The Danish National Patient Registry contains information about every contact with the public Danish health service regarding administrative data, diagnosis, treatments, procedures, and examinations. Data from the Danish National Prescription Registry were further used to calculate the Charlson Comorbidity Index [12] [13]. It is possible to link individuals between the Danish Cancer Registry, the Danish National Patient Registry, and the Danish National Prescription Registry using a unique encrypted number based on the social security number. As Danish health care is based on a universal, free-for-all, public health care system there is little room for any private practice, creating optimal conditions for registries to be as complete as possible.

Identifying cancers, colonoscopies, and comorbidities

A master dataset containing CRC and colonoscopies was obtained by searching the Danish Cancer Registry and the Danish National Patient Registry from 1 January 1998 to 31 December 2015. CRC was identified using Danish ICD-10 codes DC18, DC19, and DC20. Colonoscopies were identified using Nordic Medico-Statistical Committee Classification of Surgical Procedure Codes UJF32 and UJF35 Colonoscopy without/with biopsy. A comorbidity database was constructed containing information about every case of Crohn’s disease, ulcerative colitis, and diverticulitis (using Danish ICD-10 DK50, DK51, and DK57, respectively) diagnosed to 31 December 2015. Hereditary CRC disease was defined as one of the following: DZ848A1 – familial history of hereditary nonpolyposis CRC; DZ800 – familial history with cancer in the gastrointestinal tract; DD126B – hereditary polyposis coli; or DD126F – familial adenomatous polyposis. Comorbidities present at the time of the colonoscopy were used for further analysis. The Charlson Comorbidity Index was calculated based on ICD-10 codes according to the method of Quan et al. 1 year prior to the date of colonoscopy [12] [14].

Denmark compared with England

The comparison between the Danish and English NHS PCCRC-3yr was based on a previously published paper by Morris et al. [4]. In the original paper, English NHS PCCRC-3yr rates were calculated using four methods previously described by Bressler, Cooper, le Clercq, and Singh, respectively [6] [7] [8] [9]. The Cooper method was used for Danish comparison as it best resembles the method used by Forsberg, which is the method used in Sweden [15]. The English NHS PCCRC-3yr was based on the year of cancer diagnosis between 2001 and 2010, and limited to the first primary CRC. A PCCRC was defined as a CRC diagnosed 6 – 36 months after a negative colonoscopy. The nominator was PCCRC and the denominator was all CRCs within 36 months after colonoscopy (i. e. CRCs detected 6 – 36 months after a negative colonoscopy and CRCs detected at colonoscopy or within 6 months following colonoscopy).

Denmark compared with Sweden

The comparison between the Danish and Swedish PCCRC-3yr was based on a previously published paper by Forsberg et al. [15]. The data used had a different structure, as the denominator was changed from cancer to colonoscopies. Our master dataset was recoded to meet identical specifications and time frame (year of colonoscopy 2001 – 2010 with 3-year CRC follow-up). The time frames for both detected CRC and PCCRC were similar in the study by Forsberg to those described above: 0 – 6 months and 6 – 36 months, respectively. In cases of multiple colonoscopies, only the first colonoscopy performed in the interval (0 – 36 months) was considered in the analysis. Individuals with CRC, Crohn’s disease, or ulcerative colitis diagnosed before the first colonoscopy were excluded. In cases of multiple CRCs, only the first CRC diagnosis was used. Using the Forsberg method, the PCCRC-3yr is calculated by dividing the number of individuals in the PCCRC group (6 – 36 months) by the number of individuals with a colonoscopy followed by a CRC (0 – 36 months).

Factors associated with PCCRC

For the current study, the dataset was limited to include colonoscopies from 2001 to 2012 with a CRC diagnosed within 3 years from colonoscopy (i. e. CRC from 2001 to 2015). In cases of multiple colonoscopies, only the first colonoscopy within 3 years of a CRC diagnosis was used for further analysis. The outcome variable was the occurrence of a colonoscopy resulting in a PCCRC (CRC 6 – 36 months after a negative colonoscopy) or a detected CRC (0 – 6 months after colonoscopy). The predictor variables were: year of colonoscopy, age (at colonoscopy), sex, site of tumor, hereditary CRC, diverticular disease, Crohn’s disease, ulcerative colitis, tumor stage, and Charlson Comorbidity Index. Tumor site was based on Danish ICD-10 and grouped into: rectum and sigmoid (DC187, DC19 + DC20), left flexure and descending colon (DC185 + DC186), transverse colon (DC184), right colon (DC180 – DC183), and not otherwise specified (DC188 + DC189). Age was grouped into five categories: 18 – 49, 50 – 59, 60 – 69, 70 – 79, and ≥ 80 years at time of colonoscopy. Year of colonoscopy was grouped into two groups: 2001 – 2006 and 2007 – 2012. Tumor stage was defined as tumor size (T1/T2 /Dukes A vs. T3/T4/Dukes B), metastasis (yes/no/unknown), or regional lymph nodes (yes/no/unknown).

The Poisson regression model was used to test for an interaction between age and hereditary CRC, as the article by Forsberg suspected that an increased PCCRC risk among young individuals was caused by hereditary CRC [15].

Risk of PCCRC over time: WEO consensus method

The PCCRC-3yr was calculated according to the WEO consensus method recently presented by Rutter et al. in the WEO consensus statements on post-colonoscopy and post-imaging CRC [5]. CRC and procedure codes were identified as previously described, but ICD-10 C181 (malignant neoplasms of the appendix) was excluded. With this method, each individual is allowed multiple CRCs and multiple colonoscopies; however, for each CRC, only one colonoscopy in the detected CRC group and one colonoscopy in the PCCRC group are allowed. The PCCRC-3yr using the WEO consensus method is calculated by dividing the number of PCCRCs (6 – 36 months) by the total number of detected CRCs (0 – 6 months) and PCCRCs.

Statistical methods

Confidence intervals (CIs) for rates were calculated assuming a Poisson distribution. Relative risks (RRs) when comparing countries were calculated according to Altman [16]. A multivariable Poisson regression model was constructed to identify factors associated with PCCRC. Poisson regression was performed using SAS 9.4 (SAS Institute, Cary, North Carolina, USA) with the PROC GENMOD procedure. In the Poisson regression model there was an interaction between hereditary CRC and age, and for this reason the effect of hereditary CRC was stratified by age above and below 60 years.

Results

Denmark compared with England

From 2001 to 2010, 39 100 Danish individuals were diagnosed with first primary CRC, of whom 11 483 individuals had undergone colonoscopy within 3 years of the diagnosis. A total of 992 PCCRCs were identified. The Danish PCCRC-3yr using the Cooper method was 8.6 % (95 %CI 8.1 % – 9.2 %). The Danish PCCRC-3yr was significantly higher than the reported PCCRC-3yr of 7.7 % (95 %CI 7.6 % – 7.9 %) from the English NHS (RR 1.12, 95 %CI 1.05 – 1.19) [4].

Denmark compared with Sweden

From 2001 to 2010, 415 991 colonoscopies were performed in Denmark on 295 952 individuals. When excluding individuals with Crohn’s disease, ulcerative colitis, and age < 18 years, a total of 11 369 individuals were diagnosed with CRC within 3 years of a colonoscopy, of whom 1027 individuals were diagnosed with CRC within 6 – 36 months of a colonoscopy. The Danish PCCRC-3yr using the Forsberg method was 9.0 % (95 %CI 8.5 % – 9.5 %). The corresponding Swedish numbers were 16 319 individuals diagnosed with CRC within 3 years of a colonoscopy and 1286 diagnosed with CRC within 6 – 36 months of a colonoscopy [15]. The Swedish rate was 7.9 % (95 %CI 7.5 % – 8.3 %). The Danish PCCRC-3yr was significantly higher than the Swedish rate (RR 1.15, 95 %CI 1.06 – 1.24).

Factors associated with PCCRC

Baseline characteristics are summarized in [Table 1] and results from the multivariable Poisson regression model are shown in [Table 2]. The risk of PCCRC in hereditary CRC differed between patients above and below 60 years of age (P for interaction 0.02). Hereditary CRC was highly associated with PCCRC both in patients aged < 60 years (RR 7.39, 95 %CI 5.77 – 9.47) and in those aged ≥ 60 years (RR 3.81, 95 %CI 2.74 – 5.31). No significant association between PCCRC and age groups in general was found when using the age group > 80 years as a reference.

The risk of a PCCRC increased when moving through each colon segment using the rectum/sigmoid colon as a reference. Higher risk was found in the transverse colon (RR 1.57, 95 %CI 1.28 – 1.94) and in the ascending colon and cecum (RR 1.85, 95 %CI 1.64 – 2.08). PCCRC was less likely when the tumor was large (T3/T4/Dukes B vs. T1/T2/Dukes A: RR 0.70, 95 %CI 0.61 – 0.81). PCCRC was not associated with an increased risk of lymph node or solid metastasis. Diseases such as diverticulitis (RR 3.25, 95 %CI 2.88 – 3.66), ulcerative colitis (RR 3.44, 95 %CI 2.79 – 4.23), and a Charlson Comorbidity Index of 1 or 2 (RR 1.20, 95 %CI 1.03 – 1.40 and RR 1.25, 95 %CI 1.06 – 1.48, respectively) were also significantly associated with PCCRC.

Risk of PCCRC over time: WEO consensus method

Biannual results are shown in [Fig. 1], with falling PCCRC-3yr over time, from 22.5 % in 2001 to 7.9 % in 2012. Annual numbers of detected CRC and PCCRC colonoscopies are available in [Table 3] for future comparison with Danish rates.

Discussion

This nationwide population-based cohort study is the first to directly compare PCCRC-3yr rates between countries using equivalent methodologies. Furthermore, the analysis confirms previous associations and identifies new factors associated with PCCRC. Our finding of over-representation of PCCRC in both the transverse and ascending colon/cecum is in line with previous studies that found increased risk of PCCRC in the proximal colon [4] [6] [7] [8] [9] [15]. Procedure-related factors are likely to play a part, as the right colon is more difficult to cleanse with oral agents, landmarks are less clear, and it is more technically challenging to reach the proximal colon and maintain proper scope position. Additionally, there is increasing evidence that polyps and cancers in the right colon might also represent a different entity. PCCRC is associated with microsatellite instability and CpG island methylator phenotype (CIMP) [17]. The precursor lesions for CIMP-positive tumors are suspected to be sessile serrated adenomas (SSAs) [17]. SSAs are known to occur more frequently in the right colon and their flat appearance makes them more difficult to detect during colonoscopy [18].

We also found an association between PCCRC and a previous diagnosis of diverticulitis, which is in line with previous studies [4] [6] [15] [19]. In general, diverticular disease is known to make a colonoscopy more difficult, with increased patient pain, impaired views in the affected areas, and the risk of mistaking neoplastic tissue for an area of severe inflammation [19]. Long-standing chronic inflammation in diverticulitis has been suggested as a risk for CRC; however, the finding has been disputed by others, and might be a result of misclassification and intensive surveillance [20] [21] [22].

Previous studies have shown conflicting results regarding the association between age and PCCRC. Bressler et al. found that older age was associated with an increased risk of PCCRC, whereas other studies have found no association with age [6] [15] [23]. Forsberg et al. found an increased risk of PCCRC in the age group of 18 – 30 years and suspected that hereditary cancers might be part of the explanation [15]. Our analysis supports the Swedish hypothesis. When adjusting for interaction between hereditary cancer and age there was no significant association between any age group and the risk of PCCRC, but borderline associations were found in both the 18 – 50 years and 70 – 79 years age groups. Hereditary cancer disease was associated with a higher risk of PCCRC both among younger (< 60 years) and older (≥ 60 years) age groups. The exact reasons for this association cannot be established from this study, but hereditary cancers are known to have a different biological pathway, occur earlier in life, and be fast growing [24].

Ulcerative colitis was associated with an increased risk of PCCRC but Crohn’s disease was not. In previous studies, inflammatory bowel disease (IBD) has often been excluded before the initial analysis, mainly because IBD-associated cancers are considered a different entity, with different genomic alterations compared with CRC that is not related to IBD [6] [7] [15] [25]. It is unknown whether IBD affects the adenoma – carcinoma sequence directly or whether the higher risk of PCCRC is procedure related. The mucosa is often abnormal in patients with long-standing IBD and subtle lesions might be missed, and the short surveillance intervals recommended for high risk patients will inevitably raise the chance of finding a cancer within 3 years. Short surveillance intervals are unlikely to be a reason for higher rates of PCCRC in IBD in the Danish cohort because, until 2014, the Danish guidelines did not require such intensive surveillance. Of course, it is possible that the patients most at risk were having frequent colonoscopies at shorter intervals to assess disease and guide treatment, and this will accentuate PCCRC-3yr rates.

From a Danish perspective, it is concerning that the PCCRC-3yr was significantly higher than in both Sweden and the English NHS. Since a nationwide colonoscopy quality survey (performed in 1999 and reported in 2004) demonstrated poor results in the English NHS, there have been many quality improvement initiatives in the English NHS that might explain some of the differences [26]. A certification process for both newly independent screening colonoscopists and those screening fecal occult blood tests, a national training infrastructure, and participation of endoscopy services in a unit accreditation scheme that requires services to monitor colonoscopist key performance indicators and act on poor performance, are just some of the initiatives that have not occurred in Denmark [27] [28]. A closer look into the colonoscopist background and training reveals differences that may also be relevant. In England and the USA, gastroenterologists perform most of the colonoscopies, whereas in Canada, Sweden, and Denmark surgeons perform a higher proportion of colonoscopies. Our study did not find any difference in the risk of PCCRC between colonoscopies performed in a surgical unit and those performed in a nonsurgical unit; however, previous studies have found increased risk of PCCRC with nongastroenterologists, surgeons, and family physicians [7] [29] [30]. For years, at least in Denmark, colonoscopy might have been regarded as a minor procedure among surgeons, just one among many procedures that needed to be mastered during surgical training. As described by Rabeneck et al., the time spent on endoscopy training by gastroenterologists is almost 16 months vs. 2 months for surgeons during their residency/training program in Canada [30]. Such differences between surgeons and gastroenterologists do not exist in Denmark: there are no official endoscopy training programs during residency. Current training to become a surgeon in Denmark requires 200 colonoscopies during the 5-year training program, whereas gastroenterologists have no minimum requirements regarding colonoscopies. Gastroenterology trainees are required to pass a 2-day colonoscopy course and perform to acceptable standards; however, few gastroenterologists have performed more than 100 colonoscopies at the end of their 5-year specialist training program (personal correspondence with chief education gastroenterologists, North Region, Denmark).

Falling PCCRC-3yr has previously been demonstrated in the English NHS and in Sweden [8] [15]. We also found declining PCCRC-3yr over time in the Danish system. The multivariable analysis showed an RR for PCCRC of 1.55 (95 %CI 1.40 – 1.71) when comparing 2001 – 2006 with 2007 – 2012, indicating better performance over time ([Table 2]). [Fig. 1] shows biannual PCCRC-3yr from 2001 to 2012 using the WEO consensus method. Rates are clearly falling over time. However, it must be remembered that both [Fig. 1] and [Table 2] are based on a cancer-only model. The model compares the number of colonoscopies that diagnosed a CRC (0 – 6 months before CRC) and the number of colonoscopies missing a cancer (6 – 36 months before CRC). This methodology is identical to multiple previous studies but it does come with a risk [4] [6] [7] [8] [9]. If the way colonoscopy is used changes over time, the PCCRC-3yr may decline without any real improvements.

For example, more than a decade ago, it was unusual in Denmark to always require preoperative histological confirmation of CRC. Today, a pre-operative colonoscopy would almost certainly be required to achieve a histological confirmation, resulting in a colonoscopy-detected CRC that would not have registered in previous years. This will have the effect of increasing the denominator and lowering the PCCRC-3yr. Such a phenomenon does seem to have affected the Danish numbers. As seen from [Table 3], the numbers of colonoscopy-detected CRCs tripled between 2003 and 2004, whereas the numbers of PCCRC remained relatively stable. From procedure codes we could identify the main driving force as colonoscopy with biopsies, indicating a pre-operative regime shift (see Appendix A in the online-only Supplementary material). More recent data are less likely to be affected by changes in approach and it is reassuring that they show falling PCCRC-3yr rates over time ([Fig. 1]).

Registries may over-report PCCRC. A study from Pennsylvania showed that 47 % of PCCRCs were due to registry errors [31]. However, the Danish Cancer Registry is known to be very accurate, but there is always a risk of procedures and cancers being miscoded, misclassified, or misdated [10] [11]. A previous Danish study reviewed patient records in 101 interval cancers from one Danish medical center [32]. The time frame for detected CRC was shorter than in our study, with an increased risk of CRC being incorrectly assigned to the PCCRC group. Despite the short time frame for detected CRCs, 89 % of PCCRCs were correctly assigned. Overall, registry errors seem to be less of a concern in the Danish Cancer Registry and Danish National Patient Registry than other registries.

Registries make it possible to explore associations between CRC and colonoscopies, but very little information about the actual procedures is available. There is limited reporting of colonoscopy key performance indicators at local level and no plans for a nationwide colonoscopy database. There are supplemental procedure codes for completeness and bowel preparation but, unfortunately, there is no mandatory reporting [33].

This study has demonstrated that it is possible to compare rates of PCCRC in different jurisdictions. The key finding of higher PCCRC-3yr rates in Denmark compared with England and Sweden prompts the question of whether differences in the provision of services, training of endoscopists, and/or quality improvement practices such as accreditation are influencing rates. Given that 76 % – 86 % of PCCRC cases are considered avoidable [8] [34], there is an urgent need to change practice in order to reduce rates. National improvement programs, important as they might be, will take years to implement and have an effect. However, the data from this and other studies indicate that there are some things that can be done immediately, such as ensuring that patients with the highest risk of PCCRC (such as those with diverticulosis, hereditary cancer, ulcerative colitis, and high comorbidity) have their colonoscopy performed by the most competent colonoscopists. Furthermore, endoscopy services could ensure that all patients with suboptimal visualization of the colon (whether this is due to poor preparation or incomplete procedures) have further colonic imaging, either repeat colonoscopy or computed tomography colonoscopy. Finally, performing root cause analysis (as recommended by WEO) of individual PCCRCs will identify other factors amenable to improvement interventions.

Competing interests

None

• References

• 1 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424
  CrossrefPubMedSearch in Google Scholar
• 2 Ingeholm P. Danish Colorectal Cancer Group database annual report 2016. Available from: https://dccg.dk/wp-content/uploads/2017/10/Aarsrapport_2016.pdf Accessed: 17 September 2018
  PubMed
• 3 Rabeneck L, Paszat L. Circumstances in which colonoscopy misses cancer. Frontline Gastroenterol 2010; 3: 52-58
  PubMedSearch in Google Scholar
• 4 Morris EJA, Rutter MD, Finan PJ. et al. Post-colonoscopy colorectal cancer (PCCRC) rates vary considerably depending on the method used to calculate them: a retrospective observational population-based study of PCCRC in the English National Health Service. Gut 2015; 64: 1248-1256
  CrossrefPubMedSearch in Google Scholar
• 5 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925
  CrossrefPubMedSearch in Google Scholar
• 6 Bressler B, Paszat LF, Chen Z. et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology 2007; 132: 96-102
  CrossrefPubMedSearch in Google Scholar
• 7 Cooper GS, Xu F, Barnholtz Sloan JS. et al. Prevalence and predictors of interval colorectal cancers in medicare beneficiaries. Cancer 2012; 118: 3044-3052
  CrossrefPubMedSearch in Google Scholar
• 8 le Clercq CMC, Bouwens MWE, Rondagh EJA. et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014; 63: 957-963
  CrossrefPubMedSearch in Google Scholar
• 9 Singh H, Nugent Z, Demers AA. et al. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105: 2588-2596
  CrossrefPubMedSearch in Google Scholar
• 10 Gjerstorff ML. The Danish Cancer Registry. Scand J Public Health 2011; 39: 42-45
  CrossrefPubMedSearch in Google Scholar
• 11 Schmidt M, Schmidt SAJ, Sandegaard JL. et al. The Danish National Patient Registry: a review of content, data quality, and research potential. Clin Epidemiol 2015; 7: 449-490
  Search in Google Scholar
• 12 Charlson ME, Pompei P, Ales KL. et al. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987; 40: 373-383
  CrossrefPubMedSearch in Google Scholar
• 13 Kildemoes HW, Sørensen HT, Hallas J. The Danish National Prescription Registry. Scand J Public Health 2011; 39 (Suppl. 07) 38-41
  CrossrefPubMedSearch in Google Scholar
• 14 Quan H, Sundararajan V, Halfon P. et al. Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med Care 2005; 43: 1132-1139
  PubMedSearch in Google Scholar
• 15 Forsberg A, Hammar U, Ekbom A. et al. Post-colonoscopy colorectal cancers in Sweden. Eur J Gastroenterol Hepatol 2017; 29: 855-860
  CrossrefPubMedSearch in Google Scholar
• 16 Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991
  Search in Google Scholar
• 17 Arain MA, Sawhney M, Sheikh S. et al. CIMP status of interval colon cancers: another piece to the puzzle. Am J Gastroenterol 2010; 105: 1189-1195
  CrossrefPubMedSearch in Google Scholar
• 18 Yang JF, Tang SJ, Lash RH. et al. Anatomic distribution of sessile serrated adenoma/polyp with and without cytologic dysplasia. Arch Pathol Lab Med 2015; 139: 388-393
  CrossrefPubMedSearch in Google Scholar
• 19 Cooper GS, Xu F, Schluchter MD. et al. Diverticulosis and the risk of interval colorectal cancer. Dig Dis Sci 2014; 59: 2765-2772
  CrossrefPubMedSearch in Google Scholar
• 20 Lam TJ, Meurs-Szojda MM, Gundlach L. et al. There is no increased risk for colorectal cancer and adenomas in patients with diverticulitis: a retrospective longitudinal study. Colorectal Dis 2010; 12: 1122-1126
  CrossrefPubMedSearch in Google Scholar
• 21 Meurs-Szojda MM, Droste JSTS, Kuik DJ. et al. Diverticulosis and diverticulitis form no risk for polyps and colorectal neoplasia in 4,241 colonoscopies. Int J Colorectal Dis 2008; 23: 979-984
  CrossrefPubMedSearch in Google Scholar
• 22 Morini S, Zullo A, Hassan C. et al. Diverticulosis and colorectal cancer: between lights and shadows. J Clin Gastroenterol 2008; 42: 763-770
  CrossrefPubMedSearch in Google Scholar
• 23 Brenner H, Chang-Claude J, Seiler CM. et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012; 61: 1576-1582
  CrossrefPubMedSearch in Google Scholar
• 24 Gryfe R. Inherited colorectal cancer syndromes. Clin Colon Rectal Surg 2009; 22: 198-208
  Thieme ConnectPubMedSearch in Google Scholar
• 25 Yaeger R, Shah MA, Miller VA. et al. Genomic alterations observed in colitis-associated cancers are distinct from those found in sporadic colorectal cancers and vary by type of inflammatory bowel disease. Gastroenterology 2016; 151: 278-287
  CrossrefPubMedSearch in Google Scholar
• 26 Bowles CJA, Leicester R, Romaya C. et al. A prospective study of colonoscopy practice in the UK today: are we adequately prepared for national colorectal cancer screening tomorrow?. Gut 2004; 53: 277-283
  CrossrefPubMedSearch in Google Scholar
• 27 Quyn AJ, Fraser CG, Stanners G. et al. Scottish Bowel Screening Programme colonoscopy quality – scope for improvement. Colorectal Dis 2018; 20: 277-283
  CrossrefPubMedSearch in Google Scholar
• 28 Valori RM, Thomas-Gibson S. Commentary: Accrediting colonoscopy services and colonoscopists for screening makes a difference. Colorectal Dis 2018; 20: 283-285
  CrossrefPubMedSearch in Google Scholar
• 29 Baxter NN, Sutradhar R, Forbes SS. et al. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140: 65-72
  CrossrefPubMedSearch in Google Scholar
• 30 Rabeneck L, Paszat LF, Saskin R. Endoscopist specialty is associated with incident colorectal cancer after a negative colonoscopy. Clin Gastroenterol Hepatol 2010; 8: 275-279
  CrossrefPubMedSearch in Google Scholar
• 31 Gotfried J, Bernstein M, Ehrlich AC. et al. Administrative database research overestimates the rate of interval colon cancer. J Clin Gastroenterol 2015; 49: 483-490
  CrossrefPubMedSearch in Google Scholar
• 32 Erichsen R, Baron JA, Stoffel EM. et al. Characteristics and survival of interval and sporadic colorectal cancer patients: a nationwide population-based cohort study. Am J Gastroenterol 2013; 108: 1332-1340
  CrossrefPubMedSearch in Google Scholar
• 33 Rasmussen M, Tybjerg J, Njor S. Danish bowel cancer screening database annual report 2016. 10/2017: 1-99 Available from: https://www.sundhed.dk/content/cms/45/61245_dts%C3%A5rsrapport-2016_offentlig-version.pdf Accessed: May 2019
  PubMedSearch in Google Scholar
• 34 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
  CrossrefPubMedSearch in Google Scholar

Corresponding author

• References

• 1 Bray F, Ferlay J, Soerjomataram I. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394-424
  CrossrefPubMedSearch in Google Scholar
• 2 Ingeholm P. Danish Colorectal Cancer Group database annual report 2016. Available from: https://dccg.dk/wp-content/uploads/2017/10/Aarsrapport_2016.pdf Accessed: 17 September 2018
  PubMed
• 3 Rabeneck L, Paszat L. Circumstances in which colonoscopy misses cancer. Frontline Gastroenterol 2010; 3: 52-58
  PubMedSearch in Google Scholar
• 4 Morris EJA, Rutter MD, Finan PJ. et al. Post-colonoscopy colorectal cancer (PCCRC) rates vary considerably depending on the method used to calculate them: a retrospective observational population-based study of PCCRC in the English National Health Service. Gut 2015; 64: 1248-1256
  CrossrefPubMedSearch in Google Scholar
• 5 Rutter MD, Beintaris I, Valori R. et al. World Endoscopy Organization consensus statements on post-colonoscopy and post-imaging colorectal cancer. Gastroenterology 2018; 155: 909-925
  CrossrefPubMedSearch in Google Scholar
• 6 Bressler B, Paszat LF, Chen Z. et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis. Gastroenterology 2007; 132: 96-102
  CrossrefPubMedSearch in Google Scholar
• 7 Cooper GS, Xu F, Barnholtz Sloan JS. et al. Prevalence and predictors of interval colorectal cancers in medicare beneficiaries. Cancer 2012; 118: 3044-3052
  CrossrefPubMedSearch in Google Scholar
• 8 le Clercq CMC, Bouwens MWE, Rondagh EJA. et al. Postcolonoscopy colorectal cancers are preventable: a population-based study. Gut 2014; 63: 957-963
  CrossrefPubMedSearch in Google Scholar
• 9 Singh H, Nugent Z, Demers AA. et al. Rate and predictors of early/missed colorectal cancers after colonoscopy in Manitoba: a population-based study. Am J Gastroenterol 2010; 105: 2588-2596
  CrossrefPubMedSearch in Google Scholar
• 10 Gjerstorff ML. The Danish Cancer Registry. Scand J Public Health 2011; 39: 42-45
  CrossrefPubMedSearch in Google Scholar
• 11 Schmidt M, Schmidt SAJ, Sandegaard JL. et al. The Danish National Patient Registry: a review of content, data quality, and research potential. Clin Epidemiol 2015; 7: 449-490
  Search in Google Scholar
• 12 Charlson ME, Pompei P, Ales KL. et al. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987; 40: 373-383
  CrossrefPubMedSearch in Google Scholar
• 13 Kildemoes HW, Sørensen HT, Hallas J. The Danish National Prescription Registry. Scand J Public Health 2011; 39 (Suppl. 07) 38-41
  CrossrefPubMedSearch in Google Scholar
• 14 Quan H, Sundararajan V, Halfon P. et al. Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data. Med Care 2005; 43: 1132-1139
  PubMedSearch in Google Scholar
• 15 Forsberg A, Hammar U, Ekbom A. et al. Post-colonoscopy colorectal cancers in Sweden. Eur J Gastroenterol Hepatol 2017; 29: 855-860
  CrossrefPubMedSearch in Google Scholar
• 16 Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991
  Search in Google Scholar
• 17 Arain MA, Sawhney M, Sheikh S. et al. CIMP status of interval colon cancers: another piece to the puzzle. Am J Gastroenterol 2010; 105: 1189-1195
  CrossrefPubMedSearch in Google Scholar
• 18 Yang JF, Tang SJ, Lash RH. et al. Anatomic distribution of sessile serrated adenoma/polyp with and without cytologic dysplasia. Arch Pathol Lab Med 2015; 139: 388-393
  CrossrefPubMedSearch in Google Scholar
• 19 Cooper GS, Xu F, Schluchter MD. et al. Diverticulosis and the risk of interval colorectal cancer. Dig Dis Sci 2014; 59: 2765-2772
  CrossrefPubMedSearch in Google Scholar
• 20 Lam TJ, Meurs-Szojda MM, Gundlach L. et al. There is no increased risk for colorectal cancer and adenomas in patients with diverticulitis: a retrospective longitudinal study. Colorectal Dis 2010; 12: 1122-1126
  CrossrefPubMedSearch in Google Scholar
• 21 Meurs-Szojda MM, Droste JSTS, Kuik DJ. et al. Diverticulosis and diverticulitis form no risk for polyps and colorectal neoplasia in 4,241 colonoscopies. Int J Colorectal Dis 2008; 23: 979-984
  CrossrefPubMedSearch in Google Scholar
• 22 Morini S, Zullo A, Hassan C. et al. Diverticulosis and colorectal cancer: between lights and shadows. J Clin Gastroenterol 2008; 42: 763-770
  CrossrefPubMedSearch in Google Scholar
• 23 Brenner H, Chang-Claude J, Seiler CM. et al. Interval cancers after negative colonoscopy: population-based case-control study. Gut 2012; 61: 1576-1582
  CrossrefPubMedSearch in Google Scholar
• 24 Gryfe R. Inherited colorectal cancer syndromes. Clin Colon Rectal Surg 2009; 22: 198-208
  Thieme ConnectPubMedSearch in Google Scholar
• 25 Yaeger R, Shah MA, Miller VA. et al. Genomic alterations observed in colitis-associated cancers are distinct from those found in sporadic colorectal cancers and vary by type of inflammatory bowel disease. Gastroenterology 2016; 151: 278-287
  CrossrefPubMedSearch in Google Scholar
• 26 Bowles CJA, Leicester R, Romaya C. et al. A prospective study of colonoscopy practice in the UK today: are we adequately prepared for national colorectal cancer screening tomorrow?. Gut 2004; 53: 277-283
  CrossrefPubMedSearch in Google Scholar
• 27 Quyn AJ, Fraser CG, Stanners G. et al. Scottish Bowel Screening Programme colonoscopy quality – scope for improvement. Colorectal Dis 2018; 20: 277-283
  CrossrefPubMedSearch in Google Scholar
• 28 Valori RM, Thomas-Gibson S. Commentary: Accrediting colonoscopy services and colonoscopists for screening makes a difference. Colorectal Dis 2018; 20: 283-285
  CrossrefPubMedSearch in Google Scholar
• 29 Baxter NN, Sutradhar R, Forbes SS. et al. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140: 65-72
  CrossrefPubMedSearch in Google Scholar
• 30 Rabeneck L, Paszat LF, Saskin R. Endoscopist specialty is associated with incident colorectal cancer after a negative colonoscopy. Clin Gastroenterol Hepatol 2010; 8: 275-279
  CrossrefPubMedSearch in Google Scholar
• 31 Gotfried J, Bernstein M, Ehrlich AC. et al. Administrative database research overestimates the rate of interval colon cancer. J Clin Gastroenterol 2015; 49: 483-490
  CrossrefPubMedSearch in Google Scholar
• 32 Erichsen R, Baron JA, Stoffel EM. et al. Characteristics and survival of interval and sporadic colorectal cancer patients: a nationwide population-based cohort study. Am J Gastroenterol 2013; 108: 1332-1340
  CrossrefPubMedSearch in Google Scholar
• 33 Rasmussen M, Tybjerg J, Njor S. Danish bowel cancer screening database annual report 2016. 10/2017: 1-99 Available from: https://www.sundhed.dk/content/cms/45/61245_dts%C3%A5rsrapport-2016_offentlig-version.pdf Accessed: May 2019
  PubMedSearch in Google Scholar
• 34 Robertson DJ, Lieberman DA, Winawer SJ. et al. Colorectal cancers soon after colonoscopy: a pooled multicohort analysis. Gut 2014; 63: 949-956
  CrossrefPubMedSearch in Google Scholar

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