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Colorectal cancer risk in adenoma patients: A nation-wide study
Article first published online: 31 MAR 2004
Copyright © 2004 Wiley-Liss, Inc.
International Journal of Cancer
Volume 111, Issue 1, pages 147–151, 10 August 2004
How to Cite
Loeve, F., van Ballegooijen, M., Boer, R., Kuipers, E.J. and Habbema, J.D.F. (2004), Colorectal cancer risk in adenoma patients: A nation-wide study. Int. J. Cancer, 111: 147–151. doi: 10.1002/ijc.20241
- Issue published online: 2 JUN 2004
- Article first published online: 31 MAR 2004
- Manuscript Accepted: 29 JAN 2004
- Manuscript Revised: 2 DEC 2003
- Manuscript Received: 2 MAY 2003
- colorectal neoplasia;
Colorectal cancer incidence after adenoma removal has been studied in selected populations of adenoma patients. Our study estimates the trend in colorectal cancer incidence after adenoma removal in actual clinical practice. From PALGA, a nationwide network and registry of histo- and cytopathology in the Netherlands, we extracted data of all patients diagnosed with colorectal adenomas between 1 January 1988 and 1 October 1998. The data were used to calculate population-based colorectal cancer incidence rates after adenoma removal. A total of 78,473 adenoma patients were followed for a mean of 4.5 years after the first adenoma removal. The colorectal cancer incidence ratio compared with the general population matched by age and gender was 38.4 (37.3–39.5) in the first year after adenoma removal and 1.5 (95% confidence interval (CI): 1.4–1.6) after Year 1. The incidence ratio decreased from 2.8 (2.5–3.1) in Year 2 to 0.9 (0.6–1.2) in Years 9–11. This time trend is the opposite of the upward time trend that was expected after adenoma removal. Adenoma patients in the Netherlands are at increased risk for colorectal cancer compared to the general population. The high cancer incidence in Years 1–5 after polypectomy can be explained by a colonoscopic sensitivity for cancer of approximately 90%. © 2004 Wiley-Liss, Inc.
Adenomas are considered to be precursors of colorectal cancer and are effectively removed by endoscopy. A complete initial colonoscopy with polypectomy is recommended in individuals with adenomas because they are at increased risk for colorectal cancer. Furthermore, colonoscopic surveillance is recommended in these individuals to detect missed and newly developed adenomas and asymptomatic cancer. Several studies in selected centers and selected adenoma patients reported on the colorectal cancer incidence in the first years after adenoma removal. The incidence ratio compared to the general population ranged from 0.2 in the National Polyp Study,1 and 0.4 in the study of Lund et al.2 to 1.3 in the Funen study.3 Patients in these studies had undergone complete initial colonoscopy or incomplete initial colonoscopy followed by (negative) barium enema. In the National Polyp Study, patients with large sessile polyps were excluded from the analysis. In unselected adenoma patients, the incidence ratio after adenoma removal may be higher than in these studies, because the compliance with and the quality of the initial colonoscopy and colonoscopic surveillance is lower than in the selected centers and because patients with large sessile polyps are included.
The studies published to date have been too small to study the trend in colorectal cancer incidence according to time since polypectomy. The expectation, however, was that the effect of polypectomy would decline over time. In the first years after polypectomy, colorectal cancer incidence was expected to be low. It was thought that the incidence would later gradually increase to the level of the incidence in adenoma patients who had not previously undergone polypectomy.
The aim of our study was to estimate the colorectal cancer incidence ratio in actual clinical practice in a large unselected population of adenoma patients. We also wanted to investigate the trend in incidence ratio according to time since first adenoma removal. To this end, we investigated the incidence of colorectal cancer in all 78,473 patients who were diagnosed with adenomas in the period from 1 January 1988 to 1 October 1998 in the Netherlands.
MATERIAL AND METHODS
All Dutch pathology laboratories are connected to the PALGA, a nationwide network and registry of histo- and cytopathology. The last laboratory was connected in 1990. This registry contains 99% of all pathology reports in the Netherlands. Patients in this registry are identified by date of birth, gender, and the first 4 characters of their family name. All pathology reports on colorectal tissue in the observation period between 1 January 1988 and 1 October 1998 were retrieved. The following items were made available for each report: gender, date of birth, date of pathology review, conclusion text and diagnostic code.4 The diagnostic code is based on the Systematized Nomenclature of Medicine (SNOMED) issued by the College of American Pathologists. It contains a topological term and a morphology term describing the finding, e.g., ‘colon*villous adenoma’. The SNOMED morphology codes are identical to the codes in the International Classification of Diseases for Oncology (ICD-O-2; World Health Organization).5 The SNOMED codes that were used to classify a lesion as an adenoma, a carcinoma in situ or colorectal cancer are described in Appendix. Although it is unknown whether these adenomas were removed or only biopsied, it was recommended that diagnosed adenomas were removed immediately. Therefore, the date of first adenoma diagnosis or diagnosis of carcinoma in situ in the observation period is referred to as the date of first adenoma removal. It was unknown whether an adenoma was located in the proximal or distal colon.
The SNOMED codes for colorectal cancer used in our study are identical to the codes used by the Netherlands Cancer Registry to classify histological results as colorectal cancer. The colorectal cancer definition used and retrieval from PALGA was checked by comparing the resulting number of new colorectal cancer cases in 1995 (7,985 cases) to the number of histologically confirmed colorectal cancer cases reported in the national cancer registry (7,993 cases).6 In young age groups, the number of cancer cases differed, but the numbers were small. In the 55–59 age group, the number of cancer cases was 630 according to the definition, whereas the national cancer registry reported 599 cases (difference: 5.2%). In the 5-year age groups between 60–79 years, the difference in colorectal cancer cases was <2%.
During the period of observation, adenomas were found in 101,290 individuals. The results are based on 78,473 of these individuals who had no bowel disease or resection of the bowel at the date of first adenoma removal. Thus, patients with colorectal cancer (n = 8,188) or a resection of the colorectal tract (n = 100) before or at the date of the first adenoma removal were excluded. Furthermore, patients recorded in the pathology report as having inflammatory bowel disease (n = 10,484), polyposis coli (n = 406), and hereditary bowel disease (n = 54) were excluded from the analysis. Patients with a lesion that was classified as ‘suspect’ at the date of first adenoma removal (n = 3,585) were also excluded from the analysis, as these were mainly expected to be suspected malignancies. This was confirmed by the high number of colorectal cancers detected in these patients (incidence rate 560/1,000 person years).
Adenoma patients were followed up in the registry from the date on which they underwent adenoma removal for the first time to 1 October 1998 for the occurrence of colorectal cancer or a diagnosis of metastases of colorectal cancer in other sites. Follow-up was stopped if a non-colorectal cancer in the colorectal tract, such as lymphoma, was diagnosed, if metastases of a primary cancer in another site of the body were found in the colorectal tract, or if (partial) resection of the colorectal tract was carried out for other reasons. Calculation of the expected number of cancers was based on site-, gender- and age-specific colorectal cancer incidence rates in the general population of the Netherlands in 19937 multiplied by the observed sex- and age-specific number of person-years at risk. The ratio of observed to expected cases is reported as a standardized incidence ratio. Based on the exact Poisson distribution and calculated using Stata 7.0 (StataCorp., College Station, TX), 95% confidence intervals (CI) are reported between brackets.
Results are based on 78,473 patients registered as having undergone adenoma removal in the period between 1 January 1988 and 1 October 1998. Table I shows the age and gender distribution of the patients undergoing initial adenoma removal during the period of our study. The adenoma diagnosis rate in the population of the Netherlands during the study period was 51/100,000 person years, increasing from 10 per 100,000 person years in individuals aged <50 years to 232 per 100,000 person years in individuals aged 70–79 years. Although the prevalence of adenomas is known to climb with age, this increase also reflects the (unknown) frequency of endoscopy according to age and possible calendar time. The mean age of patients undergoing adenoma removal for the first time was 64.9 years and the mean number of follow-up years after first adenoma removal was 4.5 years.
|Age group (years)|
Figure 1 shows the colorectal cancer incidence rate by time interval since the first adenoma, and the expected incidence in the general population with the same age and gender distribution. During follow-up, 5,949 colorectal cancers were diagnosed. In the year immediately after diagnosis of the first adenoma, 5,002 colorectal cancers were diagnosed, which corresponded to a very high cancer incidence of 72 per 1,000 person years and a standardized incidence ratio of 38.4 (37.3–39.5). In Year 2, 327 colorectal cancers were diagnosed and the incidence dropped to 5.4 per 1,000 person-years. In later years, the incidence declined somewhat over time, from 3.2 per 1,000 person years in Year 3 to 2.2 in Year 11. The standardized incidence ratio declined from 2.8 (2.5–3.1) in the second year after initial polypectomy to 0.9 (0.6–1.2) in Year 9–11 after the first adenoma removal.
Some patients will be diagnosed with colorectal cancer very shortly after the initial adenoma removal, due to the adenoma being detected during the process of diagnosing cancer. Table II shows the standardized incidence ratio of colorectal cancer with exclusion of a certain period immediately after initial adenoma removal. The incidence ratio was 7.9 (7.7–8.1) when taking the total follow-up period into account, but was found to decrease to 1.5 (1.4–1.6) on exclusion of the first year, and to 1.1 (0.9–1.2) if the first 5 years after first adenoma removal are excluded. Between 5 and 11 years after undergoing adenoma removal for the first time, therefore, the colorectal cancer risk is comparable to that of the general population. In the remainder of this section, results are presented for the 64,699 patients with at least 1 year of follow-up who had a total of 282,151 person-years after the first year of follow-up. The standardized incidence ratio excluding the first year after adenoma removal was 1.5 (1.3–1.7) for rectal cancer and also 1.5 (1.4–1.6) for colon cancer. The time trend in incidence of colon cancer and rectum cancer were comparable.
|Follow-up time (months After first adenoma removal)||SIR (95% CI)|
In Table III, colorectal cancer incidence is stratified by age, gender, histology, and site of the first adenoma. The incidence of colorectal cancer increased with age (from 1.1 in ages <50 years to 4.1 in ages 80+ years), as expected, but the incidence ratio compared to the general population decreased with age (from 4.0 in ages <50 years to 1.1 in ages 80+ years). This age trend may be explained by the hypothesis that in young age groups, most colonoscopies are carried out in individuals with a familial colorectal cancer risk or with symptoms. There were significant differences in standardized incidence ratio according to pathology of the first adenoma. The standardized incidence ratio was smallest among patients with tubular adenomas and highest among patients with villous adenomas. The 1,135 patients with carcinoma in situ had a standardized incidence ratio comparable with the patients with tubular adenomas.
|Characteristic||Incidence per 1,000 person-years (cases)||SIR (95% CI)|
|All||3.4 (947)||1.5 (1.4–1.6)|
|Male||3.3 (503)||1.3 (1.2–1.5)|
|Female||3.4 (444)||1.8 (1.6–1.9)|
|P < 0.001|
|Age at first adenoma removal (years)|
|<50||1.1 (44)||4.0 (2.9–5.4)|
|50–59||2.8 (152)||2.7 (2.3–3.1)|
|60–69||3.6 (296)||1.6 (1.4–1.8)|
|70–79||4.4 (330)||1.3 (1.1–1.4)|
|80+||4.1 (125)||1.1 (0.9–1.3)|
|P < 0.001|
|Pathology of most advanced adenoma at first adenoma removal|
|Carcinoma in situ||3.6 (17)||1.4 (0.8–2.2)|
|Villous adenoma||5.3 (84)||2.1 (1.7–2.6)|
|Tubulovillous adenoma||3.5 (194)||1.6 (1.3–2.6)|
|Tubular adenoma||2.9 (217)||1.4 (1.2–1.5)|
|Adenoma, histology unknown||3.3 (435)||1.5 (1.4–1.7)|
|P = 0.02|
|Site of first adenoma|
|Rectum||4.0 (253)||1.8 (1.6–2.1)|
|Colon||3.1 (679)||1.4 (1.3–1.5)|
|Colon and rectum||3.8 (15)||1.6 (0.9–2.6)|
|P = 0.004|
|Date of first adenoma removal1|
|1 October 1988–1 October 1992||4.9 (262)||2.4 (2.1–2.7)|
|1 October 1992–1 October 1996||3.8 (209)||1.9 (1.7–2.2)|
|P = 0.07|
The number of preventive colonoscopies carried out in individuals with a familial risk for colorectal cancer probably increased between 1988–1998, due to publication of guidelines for follow-up after polypectomy in general and screening patients with familial risk for colorectal cancer.8, 9 For example, it became common practice to perform periodic colonoscopy in family members of HNPCC patients.10 This could explain the lower standardized incidence ratio in patients diagnosed with adenomas in the period 1992–1996 (in follow-up Year 2 and 3 after first adenoma removal) compared to patients diagnosed with adenomas in 1988–1992 (1.9 vs. 2.4, see Table III).
In the pathology registry, individuals were identified by an identification code consisting of the date of birth, gender, and the first 4 characters of their family name. This code was not 100% unique: individuals with the same date of birth, gender, and first 4 characters of their family name were registered under a single identification code. Thus, it was possible that a colorectal cancer diagnosed in another individual was incorrectly assigned to an adenoma patient. This will have raised the reported incidence rates. To find a lowerbound for the incidence rates, an analysis was carried out in which patients were identified not only by the date of birth, gender, first 4 characters of the family name but also by the patient's first initial, birth place and place of residence. This will produce an underestimate for the incidence rates, because patients may have moved to other places and because registration errors may have occurred. In particular, the first initial may not be correctly registered in all pathology reports. According to these alternative analyses, the standardized incidence ratio excluding the first year after first adenoma removal was 1.3 (95% CI = 1.3–1.4), declining from 2.5 (2.3–2.8) in Year 2 to 0.8 (0.5–1.0) in Years 9–11. The incidence ratio in Year 1 was 37.4 (36.3–38.4). The trend in incidence ratio was unchanged. The true incidence rates will be between these somewhat lower incidence rates and the presented incidence rates.
Our study provides an estimate of the colorectal cancer incidence in a nation-wide population of patients after endoscopic removal of a first adenoma. The study shows that, with the current polypectomy and surveillance practice, adenoma patients have a significantly higher risk for colorectal cancer than the general population, as evidenced by the incidence ratio of 1.5 (1.4–1.6) on excluding the year immediately after initial adenoma removal. The standardized incidence ratio declined from 2.8 (2.5–3.1) in Year 2 to 0.9 (0.6–1.2) in Years 9–11 after adenoma removal was first carried out.
This unexpected downward time trend in cancer incidence after initial adenoma removal was also observed by Levi et al.,11 the only other population-based study published until now. The authors of this study followed a group of Swiss patients for a mean of 4.1 years after removal of a first adenoma. They reported a colorectal cancer incidence ratio of 3.1 in Months 4–12 after polypectomy, declining to an incidence ratio of 1.8 thereafter without any further time trend.
An explanation for the downward incidence trend may be that the high incidence in the first years after polypectomy is mainly caused by cancers missed at the first adenoma removal in patients with cancer-related symptoms. Because in the clinical situation all patients with suspected colorectal cancer undergo endoscopy, the missed cases in the present data all relate to individuals in the total population with symptomatic colorectal cancer and synchronous adenomas. Examining the colorectal cancers diagnosed within a period of 3 months before to 3 months after initial adenoma removal, we found that a total of 8,393 colorectal cancers were diagnosed ‘at’ the initial adenoma diagnosis. During 5 years of follow-up (excluding the first 3 months), 1,289 colorectal cancers were detected. On the basis of these figures, we were able to arrive at an 87% sensitivity of colonoscopy for colorectal cancer. Some of the 1,289 cancers will have been new cases that were not present as cancers at the first adenoma removal. Using the Miscan-colon model,12 we estimated that approximately 230 of the cancer cases occurring between Years 1–5 were new. The sensitivity estimate adjusted for these new cancer cases is 90%. This estimate agrees with the results of studies on colonoscopic sensitivity for cancer or large adenomas,13, 14, 15 which supports the hypothesis that the high incidence in Years 1–5 after polypectomy is mainly caused by cancers missed at the initial adenoma removal. Not performing a second colonoscopy in adenoma patients with persistent symptoms can obviously result in delayed diagnosis and high colorectal cancer incidence that is not limited to the first year after polypectomy.
The adenoma patients that did not really have colorectal cancer at the initial colonoscopy were comprised of those who were screened because of a family history of colorectal cancer, as well as patients with symptoms not caused by colorectal adenoma or cancer. There was no screening carried out in the general population during the study period. A low incidence of cancer was expected in these patients in the first years after adenoma removal because of their having no (missed) cancer at baseline and having been screened and treated for colorectal cancer precursors: adenomas. An increase in colorectal cancer incidence was expected in later years because of new, progressive disease developing in these higher (than average) risk patients.
In summary, the patients with symptoms related to colorectal cancer govern the observed colorectal cancer incidence in the first years, and the patients without colorectal cancer related symptoms govern in later years. To investigate this hypothesis further, we calculated the observed time trend in incidence ratio separately for patients with tubular, tubulovillous, or villous adenomas (Fig. 2). Patients with a carcinoma in situ or an adenoma with unknown histology were not included in the figure. Colorectal cancer incidence was expected to be high throughout the first years after the adenoma diagnosis, after which this would decrease and then once again increase in later years. As not only patients with missed cancer, but also patients at high risk for colorectal cancer in later years are more likely to have villous adenomas than other patients, this incidence trend was expected to be the most pronounced in patients with villous adenomas. Indeed, a high incidence was seen in patients with villous adenomas in Years 2–3, presumably due to cancers missed at the first adenoma removal. By Years 5–7, most missed cancers had shown up and the incidence ratio was relatively low. According to the point estimates, the incidence rate will once again start to rise in Years 8–11 due to newly developed cancers. The hypothesis that two separate phenomena in two separate types of patients play a role is supported by the biphasic shape of the curve in patients with villous adenoma. Moreover, this shape is more pronounced for these patients compared to patients with tubular adenomas, whereas the results for patients with tubulovillous adenomas are intermediate.
Is the incidence of colorectal cancer after polypectomy affected by colonoscopic surveillance? Surveillance reduces the increase in incidence in later years in the second group of adenoma patients. Figure 3 shows the effect of the initial polypectomy alone and combined with surveillance colonoscopies on the colorectal cancer incidence in the National Polyp Study as estimated by the Miscan-colon expert model.16 A major reduction in incidence results from the initial polypectomy. The model further predicts that with surveillance, the incidence will rise in the third year after the initial polypectomy, due to detection of asymptomatic cancer at the 3-yearly surveillance colonoscopy. By the sixth year after initial polypectomy, however, the number of colorectal cancers prevented will have compensated this increase. Thus, surveillance cannot explain the time trend in the first years after polypectomy, but may explain the absence of an increase in incidence ratio in the latter years of the present study.
Until now, most estimated incidences of colorectal cancer in adenoma patients have been based on prospective studies in selected adenoma patients with complete initial colonoscopy, polypectomy and regular surveillance in selected medical centers. The incidence ratio in these studies compared to the general population ranged from 0.2 (0.1–0.6) in the National Polyp Study (1), and 0.4 (0.1–1.1) in the study of Lund et al.2 to 1.3 (0.6–2.3) in the Funen study.3 All ratios included the first year after adenoma removal. This compares to 2.1 (2.0–2.2) in the present study (excluding the first three months after adenoma removal). Citarda et al.17 recently conducted a retrospective study in adenoma patients at 7 reference centers for gastrointestinal diseases and neoplasms, in which the colorectal cancer incidence ratio was 0.3 (0.1–0.7) excluding the first 2 years after adenoma removal. This compares to an incidence ratio of 1.2 (1.1–1.3) in the present study. It may well be possible that many patients with symptoms related to cancer or large adenomas were excluded from these studies. Moreover, the study populations were too small and follow-up time too short to study the time trend in colorectal cancer incidence after adenoma removal.
Differences in selection criteria based on patient characteristics or the completeness of the initial examination of adenoma patients may partly cause the high incidence ratio in the present study compared to the studies mentioned. We only excluded patients with a registered history of colorectal cancer, a colonic resection, patients with registered inflammatory bowel disease, polyposis coli and other hereditary bowel disease. We had no information on gastrointestinal symptoms. In the other studies, clinical information was available and “unresolved” cases, e.g., with persistent symptoms, may not have been included. Moreover, in the National Polyp Study and the study of Citarda et al.,17 patients with sessile adenomas larger than 3 cm were excluded, a proportion of whom may have developed colorectal cancer. If these patients had been included, the colorectal cancer incidence ratio after adenoma removal may have increased to one or higher compared to the general population.
The National Polyp Study only included patients in whom the initial colonoscopy was complete and the colonoscopist felt confident that the colon had been successfully cleared.1 In the Lund study, a barium enema was carried out if the initial colonoscopy was not completed to the cecum; 6 months after the initial examination, a further flexible sigmoidoscopy was carried out to ensure a clean left colon.2 In the Funen study, complete colonoscopy was attempted at the initial examination to ensure a clean colon.3 Barium enema was added if colonoscopy was incomplete. In patients with multiple polyps or unsatisfactory bowel preparation, colonoscopy was repeated within 3 months. The Citarda study only included patients with complete initial colonoscopy or partial initial colonoscopy and double contrast barium enema.17 It is unknown how often only a sigmoidoscopy was carried out at the initial examination in the present nation-wide study, although the 1988 Dutch guidelines recommended complete initial colonoscopy with removal of all identified polyps.18 This may partly explain the high colorectal cancer incidence ratio in the present study. It indicates that it is important that surveillance guidelines clearly state that patients in whom adenomas are detected should undergo a complete colonoscopy. Many guidelines for surveillance of adenoma patients have been published over the past few years,18, 19, 20, 21, 22 but most guidelines do not provide recommendations for the initial examination.
A case-control study can be carried out in the present adenoma patient population to test our explanation of the high colorectal cancer incidence seen in the first years after the initial adenoma removal and to investigate possible improvements in patient treatment that will result in lower colorectal cancer incidence rates in the first years after adenoma removal. Cases should be individuals diagnosed with colorectal cancer within a short period after the first adenoma removal, e.g., in the second and third year, and controls should be comprised of individuals with no diagnosis of colorectal cancer and the same follow-up time. The symptoms at the initial examination, the number and quality of colonic examinations carried out in these patients and the size, shape and pathology of the initial adenomas may differ between the cases and controls. The results of the case-control study may confirm or reject the hypothesis that the high colorectal cancer incidence in the years immediately after initial adenoma removal occurs in adenoma patients with persistent symptoms. The results of such a case-control study may also lead to modified clinical guidelines, such as a recommendation to perform a second colonoscopy shortly after the initial colonoscopy in adenoma patients with persistent otherwise unexplained symptoms.
In conclusion, adenoma patients in the Netherlands are at increased risk for colorectal cancer, especially in the first years after first adenoma removal. In our study, the colorectal cancer incidence after polypectomy decreased with time since polypectomy, whereas an increase was expected. It is hypothesized that cancers missed during the diagnostic process cause the high cancer incidence in the first years after polypectomy, even until the fifth year after adenoma removal. This is supported by the fact that the results are consistent with a colonoscopic sensitivity for cancer of approximately 90%. Confirmation of this hypothesis by further studies may lead to modified clinical guidelines.
The authors thank R. Kamps and M. Casparie, Stichting Palga, U. and E. van den Akker-van Marle, Department of Public Health, Erasmus MC, University Medical Center, The Netherlands, for their assistance in the preparation of this article.
- 4PALGA-Thesaurus, editie 1999. Culemborg: Technimedia, 1999..
- 5WHO. International classification of diseases for oncology. 2nd ed. Geneva: WHO, 1990.
- 6VisserO, CoeberghJWW, SchoutenLJ, van DijkJAAM, eds. Incidence of cancer in the Netherlands 1995. Utrecht: Vereniging van Integrale Kankercentra, 1998.
- 7VisserO, CoeberghJWW, SchoutenLJ, eds. Incidence of cancer in the Netherlands 1993. Utrecht: Vereniging van Integrale Kankercentra, 1996.
- 16Effect of initial polypectomy versus surveillance polypectomy on colorectal cancer incidence reduction: micro-simulation modeling of National Polyp Study data. Gastroenterology Part 1 Suppl. 2 2000; 118: A187., , , , .
SNOMED codes used in the analysis
All SNOMED codes in the Palga registry are listed in PALGA.4
SNOMED codes classified as adenoma
A T-code of format T68… or T67… combined with an M-code with format: M74000, M74006, M74007, M74008, M74009, M74850, M81400, M81401, M82100, M82110, M82210, M82600, M82611, M82630, M90100, M90130, M90140.
SNOMED codes classified as carcinoma in situ
A T-code of format T68… or T67… combined with an M-code with format: M80102, M80105, M81402, M81405, M82632.
SNOMED codes classified as rectal cancer
A T-code of format T68… combined with an M-code with format: M8…3, M8…9, M9…3, M8…9 and the first 4 digits of the M-code in the range: 8000–8004, 8010–8012, 8020–8022, 8030–8035, 8050–8052, 8070–8075, 8140, 8144, 8200–8201, 8210–8211, 8220–8221, 8230–8231, 8240–8246, 8260–8263, 8480–8481, 8490, 8560, 8570–8573, 8720–8722, 8730, 8743, 8770–8772, 8775, 8800, 8890–8891, 8894–8896, 9140, 9590–9593, 9595, 9670–9673, 9675, 9677, 9680–9682, 9684–9688, 9690–9691, 9693–9695, 9697–9698, 9702–9705, 9711–9716, 9723, 9750, 9990.
SNOMED-codes classified as colon cancer
A T-code of format T67… combined with an M-code with format: M8…3, M8…9, M9…3, M8…9 and the first 4 digits of the M-code in the range: 8000–8004, 8010–8012, 8020–8022, 8030–8035, 8140, 8144, 8200–8201, 8210–8211, 8220–8221, 8230–8231, 8240–8246, 8260–8263, 8480–8481, 8490, 8800, 8890–8891, 8894–8896, 9140, 9590–9593, 9595, 9670–9673, 9675, 9677, 9680–9682, 9684–9688, 9690–9691, 9693–9695, 9697–9698, 9702–9705, 9711–9716, 9723, 9750, 9990.