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J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01. Published in final edited form as: J Clin Gastroenterol. 2015 July ; 49(6): 483–490. doi:10.1097/MCG.0000000000000183.
Administrative Database Research Overestimates the Rate of Interval Colon Cancer Jonathan Gotfried, MD, Marc Bernstein, MD, Adam C. Ehrlich, MD, MPH, and Frank K. Friedenberg, MD, MS (Epi) Gastroenterology Section, Temple University School of Medicine
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Abstract Goals—Our study re-examines the prevalence of interval colorectal cancer (CRC) by manually reviewing CRC cases at a single institution. Background—In 2-8% of patients with CRC, diagnosis occurs during the interval 6-36 months after a cancer-free colonoscopy. Rates are often determined by linking the date of colonoscopy with cancer registry information.
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Study—We examined all colonoscopies from 1993-2011. These exams were linked with Pennsylvania Cancer Registry data. Matched charts were manually reviewed. We determined if the CRC was “prevalent” or, for patients with a previous colonoscopy, whether they were interval or non-interval based on time from last colonoscopy. For interval cases, we identified “administrative errors” which could falsely increase the number of reported interval colorectal cancers (I-CRC). Results—Over the study period, 43,661 colonoscopies were performed with 1,147 (2.6%) positive for CRC after excluding cases (n=52) in which patients had IBD, previous surgery, or non-adenocarcinoma malignancy. Prevalent CRC's totaled 1,062 (92.6%). Non-interval CRCs (diagnosed over 36 months from index colonoscopy) were present in 40 (3.5%). There remained 45 (3.9%) potential I-CRC cases. However, after manual review, 21 cases were found to be administrative errors. Therefore, the accurate proportion of colonoscopies that found an I-CRC was 2.1% (95% CI; 1.5%-3.2%).
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Conclusions—The prevalence of I-CRC at our institution prior to adjustment was comparable to previously reported rates. This proportion was 47% lower after adjusting for administrative errors placing our figure at the lower end of reported I-CRC incidence. Reported rates of I-CRC may be falsely elevated due to errors unique to merging administrative databases. Keywords colonoscopy; interval colon cancer; Pennsylvania Cancer Registry; surveillance
Correspondence: Adam C. Ehrlich, MD, MPH, Parkinson Pavilion, 8th Floor, 3401 North Broad Street, Philadelphia, PA 19140, Phone: 215-707-9900, Fax: 215-707-2684. Previous presentation: Abstract: Gotfried J, Bernstein M, Ehrlich A, Friedenberg FK. Administrative Database Research May Overestimate the Rate of Interval Colon Cancer. Presidential Poster recipient at the 78th Annual Meeting of the American College of Gastroenterology, San Diego, California. October 2013. Potential competing interests: None
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Introduction
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Colorectal cancer (CRC) is the third most common cancer diagnosed and the second leading cause of cancer-related deaths in North America(1). CRC accounts for 10% of all cancerrelated deaths(2). The goal of CRC screening is to reduce mortality through a reduction in the incidence of advanced disease(3, 4). As such, the purpose of colonoscopy is to identify and remove adenomatous polyps which are associated with an increased risk of CRC if left in situ(3, 4). Colonoscopy has been recommended as the preferred initial CRC screening test by several professional societies and is widely performed in many countries for both highand average-risk individuals. The surveillance guidelines for colonoscopy are published by the United States Multi-Society Task Force and are widely available(5). This is based on a higher detection rate of adenomatous polyps on colonoscopy compared with the other available screening modalities(4, 6-7). Population-based case-control studies have suggested that colonoscopy markedly reduces the risk of future CRC(8, 9). For people at average risk for CRC, a screening interval of 10 years after a normal colonoscopy has been adopted based on the estimated time for normal mucosa to potentially develop an adenomatous polyp which ultimately transforms into a carcinoma(10).
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Because colonoscopy is the criterion standard for the diagnosis of CRC, proper performance by qualified health providers is essential (11). Recent papers describe indicators of a high quality colonoscopy including bowel preparation and photo documentation of cecal landmarks(12). There are several studies evaluating the incidence of CRC after a negative exam. CRCs detected shortly after (usually 6-36 months) a colonoscopy negative for malignancy are considered to be cases of interval colorectal cancers (I-CRC). This time frame (6 months) is arbitrary but was created to disregard cancers which are prevalent at colonoscopy but not yet recorded in a research database due to administrative delay (i.e. they were not missed). The implication of I-CRC is that most cases represent an error by the colonoscopist. Studies have inferred that I-CRC arise due to previously missed lesions(13, 14). It has also been shown in some cases that they occur at sites of previously incomplete polyp resection(15). A minority of cases may occur due to alternate CRC pathways such as seen in HNPCC syndrome and are not related to physician error(16).
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The incidence of I-CRC varies depending on methodology and reports have ranged from 0.4%-7.9%. Risk factors for I-CRC include older age, presence of diverticulosis, inadequate bowel preparation, and colonoscopy performed by a non-gastroenterologist(8, 11, 17, 18). Previous studies have also demonstrated that I-CRC tend to occur in the proximal colon(8). This is likely due to the greater difficulty in visualizing behind folds and the propensity for serrated adenomas to reside in this location(19). Our purpose was to examine the incidence of I-CRC at an urban teaching hospital over an extended period of time. We aimed to replicate real world estimates by including all inpatient and outpatient colonoscopy exams performed for both screening and symptoms. We also aimed to overcome the shortcomings of many studies reporting on the rates of ICRC by manually reviewing each case to overcome misclassification. Our hypothesis was that there are significant reasons for I-CRC that are not the result of endoscopist error.
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Materials and Methods Database Linkage
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We conducted a retrospective study analyzing data in our institution-wide electronic database of colonoscopies performed between 1993 – 2011. All exams were performed by US-trained gastroenterologists either by an attending physician alone or by a gastroenterology fellow with direct, in-room attending supervision. All patients who underwent colonoscopy for diagnostic and therapeutic reasons were compiled and linked to CRC data from the Pennsylvania Cancer Registry (PCR) to identify patients who were diagnosed with a colorectal adenocarcinoma. The PCR is a population-based database established in 1982 that records all cancer diagnoses made at acute care hospitals, health care facilities, health care practices, and pathology laboratories for Pennsylvania residents and out-of-state residents diagnosed in the Commonwealth. Patients from Pennsylvania diagnosed with cancer outside of Pennsylvania are included in the PCR due to cooperative sharing among states. Reporting to the PCR is mandated by state law. Accordingly, the level of state-wide reporting and histological accuracy by the PCR is reported to be > 98% (verbal communication, Matthew Peterson, 2013). Exact matching of at least three variables including name, social security number, and date of birth was required to be considered a match between our endoscopic database and the PCR to ensure accuracy and reliability of matching and to reduce the likelihood of false positive matches. Exclusions
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All records for those who matched were manually reviewed, and those with underlying inflammatory bowel disease, previous cancer diagnosis, or prior surgical resection of the colon were excluded. Patients who had a known prior colonoscopy at an outside institution before the initial colonoscopy at our institution were also excluded. Patients with inflammatory bowel disease were excluded from the study due to the different risks for developing cancer and specific screening and surveillance guidelines unique to that population.Additionally, we also excluded cases in which the final tumor pathology was not adenocarcinoma as these cancers were not a focus of our study. Data Collected
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We extracted data from both the patient chart and PCR. From manual review of the patient's chart, we collected age, gender, date of procedure, indication, endoscopic findings, and histology of biopsies. The colonic segment of each biopsy was noted. Preparation quality (“excellent”, “good”, “fair”, “poor”), when available from the colonoscopy report, was recorded. The following data was extracted from the PCR: date of cancer diagnosis, histology, location of lesion, and stage. Definitions: Prevalent Cancer, Interval Cancer, Surveillance Interval Cancer Adenocarcinomas were defined as prevalent if they were diagnosed at the time of first colonoscopy at our institution. For example, an obviously malignant lesion is identified or a malignant polyp with invasion beyond the mucosa is found. On occasion, a patient's index colonoscopy was inadequate (poor preparation) or incomplete (e.g. due to sedation issues),
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and cancer was not initially diagnosed. However, a repeat exam within 6 months was diagnostic for cancer, and these too were considered prevalent cancers. Consistent with prior literature, an interval colorectal cancer (I-CRC) was defined as a colon cancer in the period 6-36 months after the index colonoscopy where the diagnosis of cancer was not made. On a case by case basis, we reviewed the chart to determine if the diagnosis of an I-CRC was valid or made based on what we defined as an “administrative error”. These errors were defined a priori as reasons that are outside the fault of the endoscopist performing the colonoscopy and include issues such as failure to follow endoscopist recommendations for further testing and delays in reporting a cancer to the PCR.
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We defined surveillance interval cancers (SI-CRC) as malignancies that occurred beyond 36 months but prior to the next recommended surveillance. We used the surveillance intervals recommended by the US Multi-Society Task Force on Colorectal Cancer (5). The study was approved by our institutional review board and the Pennsylvania Cancer Registry.
Results Figure 1 highlights the flow of patients included in the study. For the years 1993 – 2011, there were 43,661 colonoscopy exams performed, and 1,199 (2.7%) patients were diagnosed with a colonic malignancy. Of these, 52 cases (4.3%) did not meet inclusion criteria for further analysis including 18 cases of non-adenocarcinoma malignancies and 34 cases of previous colon surgery or inflammatory bowel disease. Of the remaining 1,147 CRC cases, 1,062 (92.6%) were diagnosed on index colonoscopy. Thus, 85 patients (7.4%) were diagnosed with CRC during a period after their index colonoscopy.
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There were 45 patients with CRC diagnosed 6-36 months after index colonoscopy. Of these, 24/45 (53.3%) had a “true” I-CRC (Table 1). Our actual prevalence of I-CRC was therefore 24/1147 (2.1%; 95 % confidence interval 1.5%-3.2%). Per the endoscopy report, I-CRC patients had an initial colonoscopy which was reported as negative for malignancy and were advised not to return for a follow-up exam in less than 3 years. There were 15/24 females (62.5%) and the mean age was 69 ± 10 years. The majority of index exams 15/24 (62.5%) were performed for CRC screening. The remainder of indications were for occult or overt gastrointestinal bleeding. Reflecting our urban minority patient pool, there were 14/24 (58.3%) African Americans. The mean time to diagnosis of I-CRC after index colonoscopy was 21.3 ± 9.9 months (range 7-36). Overall, 11/24 (45.8%) I-CRC cases were stage I (cancer spread to the muscularis propria). There were 13/24 (54.2%) I-CRC cases found proximal to the splenic flexure and 8/24 (33.3%) in the rectum. In 7/24 (29.2%) cases, the malignancy was ultimately found in the same colonic segment as a previous biopsy or polypectomy on the index colonoscopy. Quality of bowel preparation for index colonoscopy was not listed in six reports. There were 2/18 (11.1%) described as “poor” and 13/18 (72.2%) listed as “good” or “excellent”. Despite a “poor” or “fair” prep, patients were not advised to undergo an expedited repeat exam. There were 21/45 (46.7%) patients who potentially could have been misclassified as having an I-CRC had their charts not been manually reviewed. We labeled these as administrative
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errors. If misclassifications were not identified, our rate of I-CRC would have erroneously been reported as “true” I-CRC + administrative errors = 45/1147 (3.9%). Table 2 provides a list of the administrative error patients and Figure 2 highlights the nature of these errors. There were 10/21 (47.6%) females and the mean age was 69 ± 11 years. The median interval between the initial colonoscopy and the time the diagnosis was established was 14 months (range 6-33).
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Examples of administrative errors often centered on compliance with physician recommendations. Several patients had an incomplete colonoscopy due to poor bowel preparation or inability to visualize a desired colon segment (9/21 or 43%). Patients failed to return for a scheduled repeat exam within 12 months despite an automated phone call and reminder letter sent to the residence in 7/21 (33%) cases and failed to get a requested barium enema in 2/21 (10%) of cases. Cancer was subsequently found on the follow-up exam but administratively it appears that this was an I-CRC and the first exam missed the lesion. Another common example occurred when the initial colonoscopy visualized a malignantappearing mass but biopsies were non-diagnostic. Pathologic diagnosis of malignancy was confirmed at surgery which occurred more than 6 months later in 8/21 (38%) cases. Patients failed to return for repeat colonoscopy in the setting of an inadequately removed polpy in 3/21 (14%) of cases. In one case (5%), the administrative error was caused by a delay in the cancer diagnosis being reported to the PCR.
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The rate of SI-CRC was 3.5%. SI-CRC is defined as CRC occurring at any interval more than 36 months after index colonoscopy but prior to the next recommended exam. These are shown in Table 3. The mean age of these patients was 69 ± 11 years (range 48-89). The interval between colonoscopy and time to malignancy was 60.5 ± 18.0 months (range 37-110). Sixteen malignancies (40%) developed in the ascending colon and 57.5% developed proximal to the splenic flexure.
Discussion This study illustrates potential sources of error that may arise when linking administrative databases to determine the rate of I-CRC. The removal of administrative errors reduced our rate by 47%, from 3.9% to 2.1%. That is, in roughly 1 out of every 50 new cases of CRC diagnosed in our unit, the patient had a colonoscopy within the previous 3 years which was felt to be satisfactory. Satisfactory means that the initial colonoscopy did not diagnose CRC and that the physician did not recommend additional testing or repeat examination in fewer than 3 years. The rate of I-CRC at our institution was found to be lower than reported rates in most previous studies.
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Our I-CRC rate (2.1%; 95 % confidence interval (CI) 1.5%-3.2%) occurred in a real world setting which included colonoscopy exams on symptomatic individuals and inpatients. Because of the setting, our I-CRC rate is likely biased toward a higher percent relative to other endoscopic environments. For example, patients with both overt and occult gastrointestinal bleeding were included; therefore the prevalence of underlying CRC is likely to be much higher than in a screening population. Theoretically, there were more opportunities to miss a neoplasm. Additionally, in order to expedite discharge, procedures
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on inpatients often are performed despite a suboptimal bowel preparation because of both stool and residual blood. The potential to miss flat carcinomas and advanced polyps is theoretically magnified in this setting (12). Ultimately, if patients were diagnosed with a CRC after discharge, the diagnosis would be captured in the Pennsylvania Cancer Registry. Finally, many procedures were performed by newly trained gastroenterologists (< 3 years post-fellowship) and research-oriented staff who perform a relatively low volume of procedures. Despite all of these factors, our rate of “true” I-CRC was at the lower end of previously published reports.
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Other studies have used some component of manual chart review similar to our methodology. For example, in a study from Japan, the reported rate of I-CRC was 6.0%(20). I-CRC occurred predominantly in the proximal colon and was more common in individuals over 60 years of age. A study from New Zealand found an I-CRC rate of 5.9%(21). In 5/17 I-CRC patients, a poor bowel preparation lead to a delay in diagnosis for as long as 22 months. In a case control study from the Veterans Administration system, the rate of I-CRC was found to be 5.4% (95%CI; 4.1%-7.2%)(15). The authors used an interval of 12-60 months after index colonoscopy to define the window for I-CRC thus their rate may not be directly comparable and cases in which the index colonoscopy had a poor bowel preparation were not censored. The authors also found that I-CRC tended to occur in the proximal colon compared to sporadic CRC (59% vs. 29%, P=0.011). The DACHS study from Germany used structured interviews supplemented by medical records when available to establish whether patients could be categorized as having an I-CRC(17). They reported a rate of 1.8%. As a generality, these studies did not specifically address the issue of administrative errors examined in our study.
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Although other studies have cross referenced healthcare databases with centralized tumor registries in order to determine I-CRC rates, these studies did not review potential I-CRC cases manually. Similar to our methods, these studies aggregate data for inpatients, outpatients, screening exams, and those performed for signs and symptoms of colorectal disease. For example, Bressler, et al. cross-referenced several databases and reported I-CRC rates of 2.4% at 2 years, 3.4% at 3 years, and 4.6% at 5 years after eliminating cases that occurred within 6 months of index colonoscopy(11). A similar study from Manitoba, Canada found an overall I-CRC rate of 7.9% (ranging from 4.5%-14.4% depending on scenario), which is one of the highest reported in the literature(14). Risk factors for an ICRC included index colonoscopy by a family physician and location in the proximal colon. Singh, et al. used a random sample of Medicare claims data to determine I-CRC rates in older Americans(18). In an attempt to address some administrative errors, they censored both CRC cases occurring within one year of index colonoscopy and those with an incomplete index exam; they found a remarkably low I-CRC rate of 0.4%. In contrast, Cooper, et al.examined the linked Surveillance, Epidemiology, and End Results (SEER)Medicare database and found that 7.2% of patients developed I-CRC(22). Risk factors for ICRC seen in this study included the presence of diverticulosis, proximal tumor location, and performance of the index exam by non-gastroenterologists. A small cohort study by Imperiale, et al. provides some measure of comfort that the rate of I-CRC may be very low in average risk individuals after screening colonoscopy(10). They
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reported a 0% incidence of colon malignancy following a negative index colonoscopy in 1,256 individuals who agreed to a surveillance exam a mean of 5.3 years later. This data is consistent with the results of the group from Manitoba which found that the standardized incidence ratio (SIR) for CRC was 0.55 (95% CI; 0.41-0.73) after a “negative” colonoscopy(8).
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A recent population-based study in the Netherlands attempted to examine the reasons underlying the diagnosis of post-colonoscopy CRC (23). Similar to our study, investigators manually examined the medical records from CRC cases in the Dutch cancer registry. They categorized cancers as either related to procedural factors (inadequate examination or surveillance, incomplete resection, or missed lesions) or tumor biology (newly developed cancers). They concluded that 86% of all post-colonoscopy CRCs could be explained by procedural factors, most notably missed lesions which accounted for 58% of all observed cancers. This finding is very similar to our finding that 53% of observed cancers (“true” ICRC) after an index colonoscopy can be attributed to missed lesions or new tumors.
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What accounts for I-CRC overall? One possibility is the failure to recognize and remove serrated adenomas. The sessile serrated adenoma pathway is recognized for its predilection for the proximal colon and may result in more rapid progression to malignancy in some individuals (24). Studies have shown that interval cancers found in the proximal colon are often microsatellite unstable, and it has been proposed that associated mismatch repair genetic defects can lead to a rapid accumulation of mutations and accelerated tumor growth (25). Another possibility is incomplete adenoma removal which results in residual neoplastic tissue that progresses to malignancy. Studies have shown that 19-27% of interval cancers occur in the same portion of the colon as the site of prior polypectomy(26-28). This is especially relevant in cases where the index polyp was a sessile adenoma that required piecemeal resection. A final source of error is the failure to adhere to quality guidelines. For example, patients undergoing screening colonoscopy with a poor bowel preparation should undergo a repeat examination within the year (5). We suspect these mechanisms may have led to the 40 SI-CRC cases we observed. It is curious that I-CRC commonly occurs in the rectum. Our study found that 33% of I-CRC developed in this location, which confirms previously published data. Singh, et al. found 39% of I-CRC in the rectum/rectosigmoid region over a period of five years (17% at 6-24 months, 22% at 2-5 years) (8). Another study found that 41% of I-CRC occurred in the rectum/rectosigmoid region (11). In the study from Manitoba, 40% of men and 25% of women had an interval cancer distal to the splenic flexure (13). The reason for this observation remains unknown.
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Legal liability in colorectal cancer is a common concern among gastroenterologists. The notion of I-CRC emphasizes the need to be familiar with the issues that may arise given the rate, albeit low, of I-CRCs. In a recent editorial by Douglas Rex, the author states the needs to obtain proper informed consent about “missed cancers” and possibly have a conversation with the patient about factors that may influence the chance of a missed cancer. Additionally, physicians must ensure diligent follow up of patients with ongoing complaints
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as a false negative colonoscopy result may offer false reassurance for concerning symptoms. Lastly, close communication with the referring physician is essential(29).
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There were some important limitations of our study. The data comes from a single institution. We did not have access to colonoscopy reports from other institutions. In reviewing the available patient pool from our institution, we attempted to remove all patients that referenced a prior colonoscopy elsewhere. In some cases, these records were not available for review. Thus, there may have been a small number of cases where patients had a prior colonoscopy so an exam we thought was an index exam was actually a follow-up. The PCR includes data from all cancers diagnosed in the Commonwealth of Pennsylvania. Although the registry reports that few patients are missed because of sharing data across state databases, it is possible that some additional patients had cancers diagnosed at centers in other states either by colonoscopy or surgery which were not recognized in our analysis. This could bias our reported results toward a lower rate of I-CRC. This may be additionally likely as our hospital is located within a short distance of New Jersey and Delaware. Additionally, sessile serrated adenomas (SSA) were not identified among patients with interval cancers or those classified as administrative errors. SSAs were not a widely recognized entity during the majority of the study period. Administrative errors may be more likely in the setting of an SSA however these were not an identified source of classification or administrative error among our study subjects.
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In summary, we demonstrated that over a nearly 20 year period the “true” rate of interval cancer was low at 2.1% (95 % CI 1.5%-3.2%). This is at or below the reported rate from other institutions despite the fact that we included inpatients, patients with active signs and symptoms of colorectal disease, and cases performed by relatively inexperienced gastroenterologists. Our number was determined after eliminating cases of administrative error through manual chart review. We confirmed that the rectum is a common site for interval colorectal cancers. By manually reviewing charts we also could provide data on the rate of surveillance interval cancers (3.5%, 95 % CI; 2.7-4.8%) because the recommendations of the physician were available. As we routinely inform patients about the risk of a missed lesion during the colonoscopy consent process, our results provide additional information physicians can discuss with patients. Patients who present with colorectal cancer in the 6-36 months after an index colonoscopy have often not followed the post-colonoscopy recommendations for additional testing. These patients are often misclassified as having an I-CRC when the additional testing may have discovered the malignancy. The true rate of I-CRC appears to be low. Our study emphasizes the need to manually review potential cases of I-CRC to determine validity. This distinction becomes especially important in a healthcare environment where changes to the reimbursement structure may be tied to quality measures. We believe our data demonstrates that colonoscopy is an effective test for the identification and prevention of colorectal cancer and that efforts should be undertaken to improve patient compliance with physician recommendations.
Acknowledgments Financial support: Funded in part by grant NIH K24 DK83268 awarded to Frank K. Friedenberg.
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Figure 1.
Flow diagram of study patients.
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Figure 2.
Nature of administrative errors.
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Cecum
Transverse
Cecum
Tumor Location
2008
2007
2001
2011
2002
2006
2008
1993
2001
2004
2001
1995
2006
2000
2001
2002
1993
1997
2004
1997
1999
2008
1998
1995
Year of Diagnosis
Author Manuscript
Patient
IIIA
I
IIIA
I
I
IV
IIIA
I
I
IIA
Red blood per rectum
Screening
Iron Deficiency Anemia
Screening
Screening
Heme + Stool
Iron Deficiency Anemia
Screening
Screening
Iron Deficiency Anemia
Red blood per rectum
Iron Deficiency Anemia
IIb I
Screening
Heme + Stool
I
Red blood per rectum
IIIb
Screening
IIIA
Screening + Family History
IIb
Screening
Screening
Screening
Screening + Family Historya
Screening
Screening
Screening
Indication
IV
I
I
IIIB
I
IIIB
IV
I
Stage
Good
Good
Fair
Good
Fair
Fair
Good
Not Listed
Excellent
Good
Good
Not Listed
Good
Good
Good
Good
Not Listed
Not Listed
Excellent
Poor
Good
Poor
Not Listed
Not Listed
Prep Quality
Author Manuscript Table 1
Yes
Yes
No
No
No
N/A
No
No
No
No
Yes
No
Yes
No
No
No
N/A
No
Yes
Yes
N/A
N/A
No
Yes
Interval Cancer at Same Site as Polyp Removal
14
15
32
7
29
14
28
11
19
10
9
10
30
12
17
12
24
36
33
32
23
36
30
9
Interval (months)
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“True” Interval Colorectal Cancer
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Extent of lymph node involvement not specified
b
Family History indicates first-degree relative with CRC.
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Gotfried et al. Page 14
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Author Manuscript
Author Manuscript
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Author Manuscript Table 2
Author Manuscript
Author Manuscript
Age
88
79
83
78
77
83
75
74
77
66
69
62
64
63
59
62
57
50
49
77
63
Patient
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01.
21
M
F
M
M
M
F
M
F
F
M
M
F
M
F
M
M
F
F
F
F
M
Sex
Rectum
Cecum
Rectum
Rectum
Rectum
Rectum
Ascending
Rectum
Rectum
Sigmoid
Sigmoid
Ascending
Ascending
Cecum
Descending
Descending
Ascending
Sigmoid
Cecum
Cecum
Sigmoid
Tumor Location
I
II
IIA
I
I
I
I
I
IIIA
I
I
I
I
I
IIIA
IIIC
IVA
I
IIB
I
I
Stage
Screening
Screening
Screening
Red blood per rectum
Screening – High risk family history
Polyp Surveillance
Polyp Surveillance
Screening
Screening
Rectal bleeding
Incidental mass seen on imaging.
Red blood per rectum
Screening
Screening
Weight Loss
Polyp Surveillance
Heme Positive Stool
Heme Positive Stool
Iron Deficiency Anemia
Red blood per rectum
Red blood per rectum
Indication for Index Colonoscopy
Poor
Poor
Fair
Excellent
Fair
Good
Good
Fair
Excellent
Fair
Excellent
Fair
Fair
Fair
Fair
Good
Good
Poor
Poor
Poor
Poor
Prep Quality
33
29
17
6
22
15
11
18
16
6
13
33
19
6
14
21
22
25
10
16
6
Months from Index Colonoscopy to Diagnosis
Author Manuscript
Patients misclassified due to Administrative Error as having an Interval Colon Cancer
Gotfried et al. Page 15
Author Manuscript
Author Manuscript
Age
89
87
79
83
78
83
80
83
73
81
71
72
76
81
68
73
72
79
72
72
75
69
68
65
60
67
69
Patient
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
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21
22
23
24
25
26
27
AA
AA
AA
AA
AA
Caucasian
AA
AA
AA
Caucasian
AA
AA
Hispanic
AA
Caucasian
Caucasian
Caucasian
AA
AA
AA
AA
AA
Caucasian
AA
Caucasian
Caucasian
AA
Race
Sigmoid
Descending
Descending
Descending
Rectum
Ascending
Sigmoid
Sigmoid
Ascending
Ascending
Cecum
Cecum
Ascending
Ascending
Cecum
Sigmoid
Splenic Flexure
Rectum
Rectum
Ascending
Ascending
Ascending
Cecum
Ascending
Ascending
Cecum
Ascending
Tumor Location
Good
Good
Not Listed
Excellent
Good
Good
Excellent
Fair
Good
Good
Not Listed
Not Listed
Not Listed
Good
Fair
Not Listed
Fair
Fair
Fair
Fair
Not Listed
Good
Not Listed
Fair
Not Listed
Poor
Poor
Prep Quality
10 years
10 years
10 years
5 years
5 years
5 years
5 years
10 years
5-10 years
10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
10 years
10 years
5-10 years
5-10 years
10 years
Recommended interval for follow up
74
80
44
40
40
55
58
65
62
110
62
41
53
65
40
68
52
68
52
99
84
61
56
40
86
42
75
Months from Index Colonoscopy to Diagnosis
Author Manuscript Table 3
Author Manuscript
Surveillance interval cancers diagnosed before recommended exam
Gotfried et al. Page 16
54
50
48
48
37
38
39
40
AA
AA
Hispanic
AA
AA
AA
Caucasian
AA
AA
AA
Hispanic
AA
Hispanic
AA: African American
57
60
33
36
54
32
59
60
31
35
57
30
60
61
29
34
65
Author Manuscript
28
Rectum
Rectum
Ascending
Ascending
Ascending
Ascending
Rectum
Sigmoid
Descending
Cecum
Ascending
Hepatic Flexure
Cecum
Tumor Location
Fair
Good
Not Listed
Good
Good
Not Listed
Good
Not Listed
Excellent
Excellent
Good
Excellent
Excellent
Prep Quality
5-10 years
5-10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
5 years
10 years
5 years
10 years
5 years
Recommended interval for follow up
Author Manuscript Race
50
51
65
65
48
39
63
82
41
37
46
95
64
Months from Index Colonoscopy to Diagnosis
Author Manuscript
Age
Author Manuscript
Patient
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J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01. Published in final edited form as: J Clin Gastroenterol. 2015 July ; 49(6): 483–490. doi:10.1097/MCG.0000000000000183.
Administrative Database Research Overestimates the Rate of Interval Colon Cancer Jonathan Gotfried, MD, Marc Bernstein, MD, Adam C. Ehrlich, MD, MPH, and Frank K. Friedenberg, MD, MS (Epi) Gastroenterology Section, Temple University School of Medicine
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Abstract Goals—Our study re-examines the prevalence of interval colorectal cancer (CRC) by manually reviewing CRC cases at a single institution. Background—In 2-8% of patients with CRC, diagnosis occurs during the interval 6-36 months after a cancer-free colonoscopy. Rates are often determined by linking the date of colonoscopy with cancer registry information.
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Study—We examined all colonoscopies from 1993-2011. These exams were linked with Pennsylvania Cancer Registry data. Matched charts were manually reviewed. We determined if the CRC was “prevalent” or, for patients with a previous colonoscopy, whether they were interval or non-interval based on time from last colonoscopy. For interval cases, we identified “administrative errors” which could falsely increase the number of reported interval colorectal cancers (I-CRC). Results—Over the study period, 43,661 colonoscopies were performed with 1,147 (2.6%) positive for CRC after excluding cases (n=52) in which patients had IBD, previous surgery, or non-adenocarcinoma malignancy. Prevalent CRC's totaled 1,062 (92.6%). Non-interval CRCs (diagnosed over 36 months from index colonoscopy) were present in 40 (3.5%). There remained 45 (3.9%) potential I-CRC cases. However, after manual review, 21 cases were found to be administrative errors. Therefore, the accurate proportion of colonoscopies that found an I-CRC was 2.1% (95% CI; 1.5%-3.2%).
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Conclusions—The prevalence of I-CRC at our institution prior to adjustment was comparable to previously reported rates. This proportion was 47% lower after adjusting for administrative errors placing our figure at the lower end of reported I-CRC incidence. Reported rates of I-CRC may be falsely elevated due to errors unique to merging administrative databases. Keywords colonoscopy; interval colon cancer; Pennsylvania Cancer Registry; surveillance
Correspondence: Adam C. Ehrlich, MD, MPH, Parkinson Pavilion, 8th Floor, 3401 North Broad Street, Philadelphia, PA 19140, Phone: 215-707-9900, Fax: 215-707-2684. Previous presentation: Abstract: Gotfried J, Bernstein M, Ehrlich A, Friedenberg FK. Administrative Database Research May Overestimate the Rate of Interval Colon Cancer. Presidential Poster recipient at the 78th Annual Meeting of the American College of Gastroenterology, San Diego, California. October 2013. Potential competing interests: None
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Introduction
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Colorectal cancer (CRC) is the third most common cancer diagnosed and the second leading cause of cancer-related deaths in North America(1). CRC accounts for 10% of all cancerrelated deaths(2). The goal of CRC screening is to reduce mortality through a reduction in the incidence of advanced disease(3, 4). As such, the purpose of colonoscopy is to identify and remove adenomatous polyps which are associated with an increased risk of CRC if left in situ(3, 4). Colonoscopy has been recommended as the preferred initial CRC screening test by several professional societies and is widely performed in many countries for both highand average-risk individuals. The surveillance guidelines for colonoscopy are published by the United States Multi-Society Task Force and are widely available(5). This is based on a higher detection rate of adenomatous polyps on colonoscopy compared with the other available screening modalities(4, 6-7). Population-based case-control studies have suggested that colonoscopy markedly reduces the risk of future CRC(8, 9). For people at average risk for CRC, a screening interval of 10 years after a normal colonoscopy has been adopted based on the estimated time for normal mucosa to potentially develop an adenomatous polyp which ultimately transforms into a carcinoma(10).
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Because colonoscopy is the criterion standard for the diagnosis of CRC, proper performance by qualified health providers is essential (11). Recent papers describe indicators of a high quality colonoscopy including bowel preparation and photo documentation of cecal landmarks(12). There are several studies evaluating the incidence of CRC after a negative exam. CRCs detected shortly after (usually 6-36 months) a colonoscopy negative for malignancy are considered to be cases of interval colorectal cancers (I-CRC). This time frame (6 months) is arbitrary but was created to disregard cancers which are prevalent at colonoscopy but not yet recorded in a research database due to administrative delay (i.e. they were not missed). The implication of I-CRC is that most cases represent an error by the colonoscopist. Studies have inferred that I-CRC arise due to previously missed lesions(13, 14). It has also been shown in some cases that they occur at sites of previously incomplete polyp resection(15). A minority of cases may occur due to alternate CRC pathways such as seen in HNPCC syndrome and are not related to physician error(16).
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The incidence of I-CRC varies depending on methodology and reports have ranged from 0.4%-7.9%. Risk factors for I-CRC include older age, presence of diverticulosis, inadequate bowel preparation, and colonoscopy performed by a non-gastroenterologist(8, 11, 17, 18). Previous studies have also demonstrated that I-CRC tend to occur in the proximal colon(8). This is likely due to the greater difficulty in visualizing behind folds and the propensity for serrated adenomas to reside in this location(19). Our purpose was to examine the incidence of I-CRC at an urban teaching hospital over an extended period of time. We aimed to replicate real world estimates by including all inpatient and outpatient colonoscopy exams performed for both screening and symptoms. We also aimed to overcome the shortcomings of many studies reporting on the rates of ICRC by manually reviewing each case to overcome misclassification. Our hypothesis was that there are significant reasons for I-CRC that are not the result of endoscopist error.
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Materials and Methods Database Linkage
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We conducted a retrospective study analyzing data in our institution-wide electronic database of colonoscopies performed between 1993 – 2011. All exams were performed by US-trained gastroenterologists either by an attending physician alone or by a gastroenterology fellow with direct, in-room attending supervision. All patients who underwent colonoscopy for diagnostic and therapeutic reasons were compiled and linked to CRC data from the Pennsylvania Cancer Registry (PCR) to identify patients who were diagnosed with a colorectal adenocarcinoma. The PCR is a population-based database established in 1982 that records all cancer diagnoses made at acute care hospitals, health care facilities, health care practices, and pathology laboratories for Pennsylvania residents and out-of-state residents diagnosed in the Commonwealth. Patients from Pennsylvania diagnosed with cancer outside of Pennsylvania are included in the PCR due to cooperative sharing among states. Reporting to the PCR is mandated by state law. Accordingly, the level of state-wide reporting and histological accuracy by the PCR is reported to be > 98% (verbal communication, Matthew Peterson, 2013). Exact matching of at least three variables including name, social security number, and date of birth was required to be considered a match between our endoscopic database and the PCR to ensure accuracy and reliability of matching and to reduce the likelihood of false positive matches. Exclusions
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All records for those who matched were manually reviewed, and those with underlying inflammatory bowel disease, previous cancer diagnosis, or prior surgical resection of the colon were excluded. Patients who had a known prior colonoscopy at an outside institution before the initial colonoscopy at our institution were also excluded. Patients with inflammatory bowel disease were excluded from the study due to the different risks for developing cancer and specific screening and surveillance guidelines unique to that population.Additionally, we also excluded cases in which the final tumor pathology was not adenocarcinoma as these cancers were not a focus of our study. Data Collected
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We extracted data from both the patient chart and PCR. From manual review of the patient's chart, we collected age, gender, date of procedure, indication, endoscopic findings, and histology of biopsies. The colonic segment of each biopsy was noted. Preparation quality (“excellent”, “good”, “fair”, “poor”), when available from the colonoscopy report, was recorded. The following data was extracted from the PCR: date of cancer diagnosis, histology, location of lesion, and stage. Definitions: Prevalent Cancer, Interval Cancer, Surveillance Interval Cancer Adenocarcinomas were defined as prevalent if they were diagnosed at the time of first colonoscopy at our institution. For example, an obviously malignant lesion is identified or a malignant polyp with invasion beyond the mucosa is found. On occasion, a patient's index colonoscopy was inadequate (poor preparation) or incomplete (e.g. due to sedation issues),
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and cancer was not initially diagnosed. However, a repeat exam within 6 months was diagnostic for cancer, and these too were considered prevalent cancers. Consistent with prior literature, an interval colorectal cancer (I-CRC) was defined as a colon cancer in the period 6-36 months after the index colonoscopy where the diagnosis of cancer was not made. On a case by case basis, we reviewed the chart to determine if the diagnosis of an I-CRC was valid or made based on what we defined as an “administrative error”. These errors were defined a priori as reasons that are outside the fault of the endoscopist performing the colonoscopy and include issues such as failure to follow endoscopist recommendations for further testing and delays in reporting a cancer to the PCR.
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We defined surveillance interval cancers (SI-CRC) as malignancies that occurred beyond 36 months but prior to the next recommended surveillance. We used the surveillance intervals recommended by the US Multi-Society Task Force on Colorectal Cancer (5). The study was approved by our institutional review board and the Pennsylvania Cancer Registry.
Results Figure 1 highlights the flow of patients included in the study. For the years 1993 – 2011, there were 43,661 colonoscopy exams performed, and 1,199 (2.7%) patients were diagnosed with a colonic malignancy. Of these, 52 cases (4.3%) did not meet inclusion criteria for further analysis including 18 cases of non-adenocarcinoma malignancies and 34 cases of previous colon surgery or inflammatory bowel disease. Of the remaining 1,147 CRC cases, 1,062 (92.6%) were diagnosed on index colonoscopy. Thus, 85 patients (7.4%) were diagnosed with CRC during a period after their index colonoscopy.
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There were 45 patients with CRC diagnosed 6-36 months after index colonoscopy. Of these, 24/45 (53.3%) had a “true” I-CRC (Table 1). Our actual prevalence of I-CRC was therefore 24/1147 (2.1%; 95 % confidence interval 1.5%-3.2%). Per the endoscopy report, I-CRC patients had an initial colonoscopy which was reported as negative for malignancy and were advised not to return for a follow-up exam in less than 3 years. There were 15/24 females (62.5%) and the mean age was 69 ± 10 years. The majority of index exams 15/24 (62.5%) were performed for CRC screening. The remainder of indications were for occult or overt gastrointestinal bleeding. Reflecting our urban minority patient pool, there were 14/24 (58.3%) African Americans. The mean time to diagnosis of I-CRC after index colonoscopy was 21.3 ± 9.9 months (range 7-36). Overall, 11/24 (45.8%) I-CRC cases were stage I (cancer spread to the muscularis propria). There were 13/24 (54.2%) I-CRC cases found proximal to the splenic flexure and 8/24 (33.3%) in the rectum. In 7/24 (29.2%) cases, the malignancy was ultimately found in the same colonic segment as a previous biopsy or polypectomy on the index colonoscopy. Quality of bowel preparation for index colonoscopy was not listed in six reports. There were 2/18 (11.1%) described as “poor” and 13/18 (72.2%) listed as “good” or “excellent”. Despite a “poor” or “fair” prep, patients were not advised to undergo an expedited repeat exam. There were 21/45 (46.7%) patients who potentially could have been misclassified as having an I-CRC had their charts not been manually reviewed. We labeled these as administrative
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errors. If misclassifications were not identified, our rate of I-CRC would have erroneously been reported as “true” I-CRC + administrative errors = 45/1147 (3.9%). Table 2 provides a list of the administrative error patients and Figure 2 highlights the nature of these errors. There were 10/21 (47.6%) females and the mean age was 69 ± 11 years. The median interval between the initial colonoscopy and the time the diagnosis was established was 14 months (range 6-33).
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Examples of administrative errors often centered on compliance with physician recommendations. Several patients had an incomplete colonoscopy due to poor bowel preparation or inability to visualize a desired colon segment (9/21 or 43%). Patients failed to return for a scheduled repeat exam within 12 months despite an automated phone call and reminder letter sent to the residence in 7/21 (33%) cases and failed to get a requested barium enema in 2/21 (10%) of cases. Cancer was subsequently found on the follow-up exam but administratively it appears that this was an I-CRC and the first exam missed the lesion. Another common example occurred when the initial colonoscopy visualized a malignantappearing mass but biopsies were non-diagnostic. Pathologic diagnosis of malignancy was confirmed at surgery which occurred more than 6 months later in 8/21 (38%) cases. Patients failed to return for repeat colonoscopy in the setting of an inadequately removed polpy in 3/21 (14%) of cases. In one case (5%), the administrative error was caused by a delay in the cancer diagnosis being reported to the PCR.
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The rate of SI-CRC was 3.5%. SI-CRC is defined as CRC occurring at any interval more than 36 months after index colonoscopy but prior to the next recommended exam. These are shown in Table 3. The mean age of these patients was 69 ± 11 years (range 48-89). The interval between colonoscopy and time to malignancy was 60.5 ± 18.0 months (range 37-110). Sixteen malignancies (40%) developed in the ascending colon and 57.5% developed proximal to the splenic flexure.
Discussion This study illustrates potential sources of error that may arise when linking administrative databases to determine the rate of I-CRC. The removal of administrative errors reduced our rate by 47%, from 3.9% to 2.1%. That is, in roughly 1 out of every 50 new cases of CRC diagnosed in our unit, the patient had a colonoscopy within the previous 3 years which was felt to be satisfactory. Satisfactory means that the initial colonoscopy did not diagnose CRC and that the physician did not recommend additional testing or repeat examination in fewer than 3 years. The rate of I-CRC at our institution was found to be lower than reported rates in most previous studies.
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Our I-CRC rate (2.1%; 95 % confidence interval (CI) 1.5%-3.2%) occurred in a real world setting which included colonoscopy exams on symptomatic individuals and inpatients. Because of the setting, our I-CRC rate is likely biased toward a higher percent relative to other endoscopic environments. For example, patients with both overt and occult gastrointestinal bleeding were included; therefore the prevalence of underlying CRC is likely to be much higher than in a screening population. Theoretically, there were more opportunities to miss a neoplasm. Additionally, in order to expedite discharge, procedures
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on inpatients often are performed despite a suboptimal bowel preparation because of both stool and residual blood. The potential to miss flat carcinomas and advanced polyps is theoretically magnified in this setting (12). Ultimately, if patients were diagnosed with a CRC after discharge, the diagnosis would be captured in the Pennsylvania Cancer Registry. Finally, many procedures were performed by newly trained gastroenterologists (< 3 years post-fellowship) and research-oriented staff who perform a relatively low volume of procedures. Despite all of these factors, our rate of “true” I-CRC was at the lower end of previously published reports.
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Other studies have used some component of manual chart review similar to our methodology. For example, in a study from Japan, the reported rate of I-CRC was 6.0%(20). I-CRC occurred predominantly in the proximal colon and was more common in individuals over 60 years of age. A study from New Zealand found an I-CRC rate of 5.9%(21). In 5/17 I-CRC patients, a poor bowel preparation lead to a delay in diagnosis for as long as 22 months. In a case control study from the Veterans Administration system, the rate of I-CRC was found to be 5.4% (95%CI; 4.1%-7.2%)(15). The authors used an interval of 12-60 months after index colonoscopy to define the window for I-CRC thus their rate may not be directly comparable and cases in which the index colonoscopy had a poor bowel preparation were not censored. The authors also found that I-CRC tended to occur in the proximal colon compared to sporadic CRC (59% vs. 29%, P=0.011). The DACHS study from Germany used structured interviews supplemented by medical records when available to establish whether patients could be categorized as having an I-CRC(17). They reported a rate of 1.8%. As a generality, these studies did not specifically address the issue of administrative errors examined in our study.
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Although other studies have cross referenced healthcare databases with centralized tumor registries in order to determine I-CRC rates, these studies did not review potential I-CRC cases manually. Similar to our methods, these studies aggregate data for inpatients, outpatients, screening exams, and those performed for signs and symptoms of colorectal disease. For example, Bressler, et al. cross-referenced several databases and reported I-CRC rates of 2.4% at 2 years, 3.4% at 3 years, and 4.6% at 5 years after eliminating cases that occurred within 6 months of index colonoscopy(11). A similar study from Manitoba, Canada found an overall I-CRC rate of 7.9% (ranging from 4.5%-14.4% depending on scenario), which is one of the highest reported in the literature(14). Risk factors for an ICRC included index colonoscopy by a family physician and location in the proximal colon. Singh, et al. used a random sample of Medicare claims data to determine I-CRC rates in older Americans(18). In an attempt to address some administrative errors, they censored both CRC cases occurring within one year of index colonoscopy and those with an incomplete index exam; they found a remarkably low I-CRC rate of 0.4%. In contrast, Cooper, et al.examined the linked Surveillance, Epidemiology, and End Results (SEER)Medicare database and found that 7.2% of patients developed I-CRC(22). Risk factors for ICRC seen in this study included the presence of diverticulosis, proximal tumor location, and performance of the index exam by non-gastroenterologists. A small cohort study by Imperiale, et al. provides some measure of comfort that the rate of I-CRC may be very low in average risk individuals after screening colonoscopy(10). They
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reported a 0% incidence of colon malignancy following a negative index colonoscopy in 1,256 individuals who agreed to a surveillance exam a mean of 5.3 years later. This data is consistent with the results of the group from Manitoba which found that the standardized incidence ratio (SIR) for CRC was 0.55 (95% CI; 0.41-0.73) after a “negative” colonoscopy(8).
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A recent population-based study in the Netherlands attempted to examine the reasons underlying the diagnosis of post-colonoscopy CRC (23). Similar to our study, investigators manually examined the medical records from CRC cases in the Dutch cancer registry. They categorized cancers as either related to procedural factors (inadequate examination or surveillance, incomplete resection, or missed lesions) or tumor biology (newly developed cancers). They concluded that 86% of all post-colonoscopy CRCs could be explained by procedural factors, most notably missed lesions which accounted for 58% of all observed cancers. This finding is very similar to our finding that 53% of observed cancers (“true” ICRC) after an index colonoscopy can be attributed to missed lesions or new tumors.
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What accounts for I-CRC overall? One possibility is the failure to recognize and remove serrated adenomas. The sessile serrated adenoma pathway is recognized for its predilection for the proximal colon and may result in more rapid progression to malignancy in some individuals (24). Studies have shown that interval cancers found in the proximal colon are often microsatellite unstable, and it has been proposed that associated mismatch repair genetic defects can lead to a rapid accumulation of mutations and accelerated tumor growth (25). Another possibility is incomplete adenoma removal which results in residual neoplastic tissue that progresses to malignancy. Studies have shown that 19-27% of interval cancers occur in the same portion of the colon as the site of prior polypectomy(26-28). This is especially relevant in cases where the index polyp was a sessile adenoma that required piecemeal resection. A final source of error is the failure to adhere to quality guidelines. For example, patients undergoing screening colonoscopy with a poor bowel preparation should undergo a repeat examination within the year (5). We suspect these mechanisms may have led to the 40 SI-CRC cases we observed. It is curious that I-CRC commonly occurs in the rectum. Our study found that 33% of I-CRC developed in this location, which confirms previously published data. Singh, et al. found 39% of I-CRC in the rectum/rectosigmoid region over a period of five years (17% at 6-24 months, 22% at 2-5 years) (8). Another study found that 41% of I-CRC occurred in the rectum/rectosigmoid region (11). In the study from Manitoba, 40% of men and 25% of women had an interval cancer distal to the splenic flexure (13). The reason for this observation remains unknown.
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Legal liability in colorectal cancer is a common concern among gastroenterologists. The notion of I-CRC emphasizes the need to be familiar with the issues that may arise given the rate, albeit low, of I-CRCs. In a recent editorial by Douglas Rex, the author states the needs to obtain proper informed consent about “missed cancers” and possibly have a conversation with the patient about factors that may influence the chance of a missed cancer. Additionally, physicians must ensure diligent follow up of patients with ongoing complaints
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as a false negative colonoscopy result may offer false reassurance for concerning symptoms. Lastly, close communication with the referring physician is essential(29).
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There were some important limitations of our study. The data comes from a single institution. We did not have access to colonoscopy reports from other institutions. In reviewing the available patient pool from our institution, we attempted to remove all patients that referenced a prior colonoscopy elsewhere. In some cases, these records were not available for review. Thus, there may have been a small number of cases where patients had a prior colonoscopy so an exam we thought was an index exam was actually a follow-up. The PCR includes data from all cancers diagnosed in the Commonwealth of Pennsylvania. Although the registry reports that few patients are missed because of sharing data across state databases, it is possible that some additional patients had cancers diagnosed at centers in other states either by colonoscopy or surgery which were not recognized in our analysis. This could bias our reported results toward a lower rate of I-CRC. This may be additionally likely as our hospital is located within a short distance of New Jersey and Delaware. Additionally, sessile serrated adenomas (SSA) were not identified among patients with interval cancers or those classified as administrative errors. SSAs were not a widely recognized entity during the majority of the study period. Administrative errors may be more likely in the setting of an SSA however these were not an identified source of classification or administrative error among our study subjects.
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In summary, we demonstrated that over a nearly 20 year period the “true” rate of interval cancer was low at 2.1% (95 % CI 1.5%-3.2%). This is at or below the reported rate from other institutions despite the fact that we included inpatients, patients with active signs and symptoms of colorectal disease, and cases performed by relatively inexperienced gastroenterologists. Our number was determined after eliminating cases of administrative error through manual chart review. We confirmed that the rectum is a common site for interval colorectal cancers. By manually reviewing charts we also could provide data on the rate of surveillance interval cancers (3.5%, 95 % CI; 2.7-4.8%) because the recommendations of the physician were available. As we routinely inform patients about the risk of a missed lesion during the colonoscopy consent process, our results provide additional information physicians can discuss with patients. Patients who present with colorectal cancer in the 6-36 months after an index colonoscopy have often not followed the post-colonoscopy recommendations for additional testing. These patients are often misclassified as having an I-CRC when the additional testing may have discovered the malignancy. The true rate of I-CRC appears to be low. Our study emphasizes the need to manually review potential cases of I-CRC to determine validity. This distinction becomes especially important in a healthcare environment where changes to the reimbursement structure may be tied to quality measures. We believe our data demonstrates that colonoscopy is an effective test for the identification and prevention of colorectal cancer and that efforts should be undertaken to improve patient compliance with physician recommendations.
Acknowledgments Financial support: Funded in part by grant NIH K24 DK83268 awarded to Frank K. Friedenberg.
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Figure 1.
Flow diagram of study patients.
Author Manuscript J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01.
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Figure 2.
Nature of administrative errors.
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J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01.
83
74
67
72
72
69
76
64
68
69
65
56
69
63
58
65
56
53
49
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
F
F
F
F
M
F
F
M
M
M
F
M
F
M
F
M
M
F
F
F
F
F
F
M
Sex
AA: African American
78
91
3
5
83
2
79
83
1
4
Age
AA
AA
AA
Hispanic
Not Listed
Caucasian
AA
Caucasian
AA
AA
AA
Caucasian
AA
Caucasian
Caucasian
AA
Caucasian
AA
AA
AA
AA
AA
Hispanic
Caucasian
Race/Ethnicity
Rectum
Rectum
Rectum
Rectum
Descending
Cecum
Cecum
Ascending
Cecum
Rectum
Descending
Rectum
Rectum
Transverse
Rectum
Ascending
Cecum
Ascending
Ascending
Sigmoid
Ascending
Cecum
Transverse
Cecum
Tumor Location
2008
2007
2001
2011
2002
2006
2008
1993
2001
2004
2001
1995
2006
2000
2001
2002
1993
1997
2004
1997
1999
2008
1998
1995
Year of Diagnosis
Author Manuscript
Patient
IIIA
I
IIIA
I
I
IV
IIIA
I
I
IIA
Red blood per rectum
Screening
Iron Deficiency Anemia
Screening
Screening
Heme + Stool
Iron Deficiency Anemia
Screening
Screening
Iron Deficiency Anemia
Red blood per rectum
Iron Deficiency Anemia
IIb I
Screening
Heme + Stool
I
Red blood per rectum
IIIb
Screening
IIIA
Screening + Family History
IIb
Screening
Screening
Screening
Screening + Family Historya
Screening
Screening
Screening
Indication
IV
I
I
IIIB
I
IIIB
IV
I
Stage
Good
Good
Fair
Good
Fair
Fair
Good
Not Listed
Excellent
Good
Good
Not Listed
Good
Good
Good
Good
Not Listed
Not Listed
Excellent
Poor
Good
Poor
Not Listed
Not Listed
Prep Quality
Author Manuscript Table 1
Yes
Yes
No
No
No
N/A
No
No
No
No
Yes
No
Yes
No
No
No
N/A
No
Yes
Yes
N/A
N/A
No
Yes
Interval Cancer at Same Site as Polyp Removal
14
15
32
7
29
14
28
11
19
10
9
10
30
12
17
12
24
36
33
32
23
36
30
9
Interval (months)
Author Manuscript
“True” Interval Colorectal Cancer
Gotfried et al. Page 13
Extent of lymph node involvement not specified
b
Family History indicates first-degree relative with CRC.
Author Manuscript a
Gotfried et al. Page 14
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Author Manuscript
Author Manuscript
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Author Manuscript Table 2
Author Manuscript
Author Manuscript
Age
88
79
83
78
77
83
75
74
77
66
69
62
64
63
59
62
57
50
49
77
63
Patient
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
J Clin Gastroenterol. Author manuscript; available in PMC 2016 July 01.
21
M
F
M
M
M
F
M
F
F
M
M
F
M
F
M
M
F
F
F
F
M
Sex
Rectum
Cecum
Rectum
Rectum
Rectum
Rectum
Ascending
Rectum
Rectum
Sigmoid
Sigmoid
Ascending
Ascending
Cecum
Descending
Descending
Ascending
Sigmoid
Cecum
Cecum
Sigmoid
Tumor Location
I
II
IIA
I
I
I
I
I
IIIA
I
I
I
I
I
IIIA
IIIC
IVA
I
IIB
I
I
Stage
Screening
Screening
Screening
Red blood per rectum
Screening – High risk family history
Polyp Surveillance
Polyp Surveillance
Screening
Screening
Rectal bleeding
Incidental mass seen on imaging.
Red blood per rectum
Screening
Screening
Weight Loss
Polyp Surveillance
Heme Positive Stool
Heme Positive Stool
Iron Deficiency Anemia
Red blood per rectum
Red blood per rectum
Indication for Index Colonoscopy
Poor
Poor
Fair
Excellent
Fair
Good
Good
Fair
Excellent
Fair
Excellent
Fair
Fair
Fair
Fair
Good
Good
Poor
Poor
Poor
Poor
Prep Quality
33
29
17
6
22
15
11
18
16
6
13
33
19
6
14
21
22
25
10
16
6
Months from Index Colonoscopy to Diagnosis
Author Manuscript
Patients misclassified due to Administrative Error as having an Interval Colon Cancer
Gotfried et al. Page 15
Author Manuscript
Author Manuscript
Age
89
87
79
83
78
83
80
83
73
81
71
72
76
81
68
73
72
79
72
72
75
69
68
65
60
67
69
Patient
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
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21
22
23
24
25
26
27
AA
AA
AA
AA
AA
Caucasian
AA
AA
AA
Caucasian
AA
AA
Hispanic
AA
Caucasian
Caucasian
Caucasian
AA
AA
AA
AA
AA
Caucasian
AA
Caucasian
Caucasian
AA
Race
Sigmoid
Descending
Descending
Descending
Rectum
Ascending
Sigmoid
Sigmoid
Ascending
Ascending
Cecum
Cecum
Ascending
Ascending
Cecum
Sigmoid
Splenic Flexure
Rectum
Rectum
Ascending
Ascending
Ascending
Cecum
Ascending
Ascending
Cecum
Ascending
Tumor Location
Good
Good
Not Listed
Excellent
Good
Good
Excellent
Fair
Good
Good
Not Listed
Not Listed
Not Listed
Good
Fair
Not Listed
Fair
Fair
Fair
Fair
Not Listed
Good
Not Listed
Fair
Not Listed
Poor
Poor
Prep Quality
10 years
10 years
10 years
5 years
5 years
5 years
5 years
10 years
5-10 years
10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
10 years
10 years
5-10 years
5-10 years
10 years
Recommended interval for follow up
74
80
44
40
40
55
58
65
62
110
62
41
53
65
40
68
52
68
52
99
84
61
56
40
86
42
75
Months from Index Colonoscopy to Diagnosis
Author Manuscript Table 3
Author Manuscript
Surveillance interval cancers diagnosed before recommended exam
Gotfried et al. Page 16
54
50
48
48
37
38
39
40
AA
AA
Hispanic
AA
AA
AA
Caucasian
AA
AA
AA
Hispanic
AA
Hispanic
AA: African American
57
60
33
36
54
32
59
60
31
35
57
30
60
61
29
34
65
Author Manuscript
28
Rectum
Rectum
Ascending
Ascending
Ascending
Ascending
Rectum
Sigmoid
Descending
Cecum
Ascending
Hepatic Flexure
Cecum
Tumor Location
Fair
Good
Not Listed
Good
Good
Not Listed
Good
Not Listed
Excellent
Excellent
Good
Excellent
Excellent
Prep Quality
5-10 years
5-10 years
10 years
10 years
10 years
5-10 years
10 years
10 years
5 years
10 years
5 years
10 years
5 years
Recommended interval for follow up
Author Manuscript Race
50
51
65
65
48
39
63
82
41
37
46
95
64
Months from Index Colonoscopy to Diagnosis
Author Manuscript
Age
Author Manuscript
Patient
Gotfried et al. Page 17
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