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Colorectal cancer after open-access colonoscopy: a community and case survey

John Croese
Med J Aust 1999; 170 (6): 251-254.
Published online: 15 March 1999

Research

Colorectal cancer after open-access colonoscopy: a community and case survey

John Croese

MJA 1999; 170: 251-254
 For editorial comment, see Bolin & Korman

Abstract Objective: To evaluate whether colonoscopy protects against subsequent colorectal cancer (CRC).
Design: Case and population survey.
Setting: Townsville region in northern Queensland, between mid 1985 and January 1998.
Subjects: All 8430 patients who underwent 11 148 colonoscopies performed by the author at the Mater Private Hospital (a community-based open-access colonoscopy service) between July 1985 and December 1996; those who were subsequently diagnosed with CRC, to January 1998; and all 476 residents diagnosed with colorectal cancer between 1994 and 1997.
Main outcome measures: Age-standardised CRC incidence for 1994-1997 for patients who had had a previous colonoscopy and for the remaining community; Dukes' grade of CRCs.
Results: For people aged 50 years and over, the incidence of CRC was significantly lower among those who had had a previous colonoscopy than in the remaining community (1.14 versus 2.31 per 1000 patient-years; P = 0.0046). For people aged 35-49 years, the incidence was 0.35 versus 0.31 per 1000 patient-years (P = 0.86). Thirty-one CRCs developed in 29 people who had had previous colonoscopy; only five of these CRCs were graded Dukes C, with none graded Dukes D. In contrast, almost half the CRCs in the rest of the community were graded Dukes C or D (P < 0.001). All but one of those diagnosed with CRC on repeat colonoscopy had risk factors (personal or family history), and 23 of the CRCs were subclinical, with 20 being diagnosed during surveillance colonoscopy.
Conclusions: Patients aged over 50 years who had previously undergone a colonoscopy and ensuing treatment were less likely to be diagnosed with CRC than otherwise expected. Surveillance colonoscopy led to diagnosis of CRCs with lower Dukes grades.

Introduction Colorectal cancer (CRC) is the most common internal malignancy and the second most common cause of death from cancer in Australia. CRC incidence in Australia is similar to that in other developed countries,1 but in the US both incidence and mortality are now decreasing.2 This change has been attributed to removal of premalignant polyps, detection of proportionally more early lesions by colonoscopy, and more effective treatment.3 Strategies based on colonoscopic surveillance and targeting people at increased risk of developing CRC are being promoted.3-5 However, colonoscopy, particularly in community-based, open-access practice, has not been shown to reduce CRC mortality. Indeed, although the rate of colonoscopies in Australia has increased fourfold since 1984, the incidence of CRC in New South Wales between 1973 to 1992 continued to increase by 2% per year in men and 0.9% per year in women.6

This study aimed to evaluate whether colonoscopy protects against subsequent CRC by comparing CRC incidence and pathological grading between people who have had a previous colonoscopy and the rest of the population in a geographically isolated area.

Methods
Setting The study was set in Townsville and the surrounding region (defined by the postcodes 4804-4822, 4849 and 4850; Figure 1). Townsville is a regional centre in northern Queensland that provides centralised health services, including colonoscopy, for a population of 198 000 dispersed over 200 000 km2. The nearest alternative colonoscopy services are located at Cairns and Mackay, 400 km distant.

Colonoscopy patients Subjects were patients who underwent colonoscopy performed by myself at the Mater Private Hospital, Townsville. All patients who underwent colonoscopy between July 1985 and December 1996 were identified, most from the hospital's detailed computerised records, but some of those examined between 1985 and 1990 from a hospital work ledger which gave only surname and given name.

In addition, detailed demographic and clinical information was collected prospectively in a procedural database for all colonoscopy patients from April 1994 to December 1997. Similar information was obtained retrospectively from the case records of 600 randomly chosen patients who underwent colonoscopy between 1986 and 1990.

Colonoscopic procedures and surveillance Colonoscopies were performed on patients referred by a general practitioner or specialist either for surveillance or for investigation of symptoms. Through concessions available until mid 1996, the service was equally available to all patients irrespective of financial resources. Fibreoptic colonoscopes were used before 1990, and video colonoscopes after then. Patients were lightly sedated with fentanyl (100 µg) and midazolam (2.5-5 mg). Treatment (eg, polypectomy, CRC resection) was given as necessary.

Surveillance recommendations were mostly included in procedure reports and passed to both the patient and the referring doctor. While these recommendations changed over time consistent with published guidelines,3,7 a general summary is:

  • Annual surveillance for either active ulcerative pancolitis of seven years' duration or longer or a previous malignancy plus a family history of hereditary non-polyposis colorectal cancer (HNPCC);3,7

  • One- to two-yearly surveillance for a previous CRC before 50 years and for those older than 25-40 years with either CRC developing in a first-degree relative before 50 years or a family history of HNPCC;

  • Two- to five-yearly surveillance for longstanding quiescent pancolitis or active limited colitis, CRC or polyps in a first-degree relative, previous CRC, or large (>1 cm diameter) or multiple colonic polyps; and

  • Five- to 10-yearly surveillance, depending on age, for a small adenomatous polyp.

Colorectal cancer diagnoses All patients diagnosed with CRC in Townsville between January 1994 and December 1997 were identified retrospectively by searching the computerised databases of all three pathology services, three hospitals, three endoscopy services, three colonoscopists (including myself) and one oncology service provider in Townsville, and from the CRC audits maintained by the six surgeons in Townsville. From 1995, patients diagnosed with CRC were also identified prospectively by clinicians and institutions. Patients diagnosed with CRC who had had a previous colonoscopy performed by myself at the Mater Private Hospital were identified to January 1998.

Clinical records of all patients diagnosed with CRC were audited by myself. A modified Dukes classification (A, B, C or D) was used for staging cancer spread.8,9 A malignant polyp was classified separately if colonoscopic resection was regarded as the definitive treatment. In cases of synchronous lesions, the lesion with the most invasive grading was registered.

Incidence of CRC

Colonoscopy population: The incidence of CRC was calculated as the number of cases per thousand patient-years for the period 1994-1997 for patients who had had a previous colonoscopy and still lived in the region in 1997 (colonoscopy population).

Residence was determined from the electoral register current in January 1997,10 which is considered reliable as voter registration is compulsory in Australia. To reduce mismatch errors caused by individuals with identical names, only patients with a known middle name (duplication rate, 0.3%) were cross-referenced against voters who also had a recorded middle name (duplication rate, 1.3%). The number of patients without a middle name who were still resident was estimated and added to the above on the assumption that the proportion still resident would be the same in the groups with and without a known middle name.

CRC incidence in each year was calculated for patients who had undergone previous colonoscopy up until the previous calendar year. For example, the incidence of CRC in 1994 was calculated for patients who had undergone previous colonoscopy up to 1993. Age of colonoscopy patients was determined for the year of incidence. The number of patient-years was the total for all patients in a given age range who had previously had a colonoscopy up to 1993, 1994, 1995 and 1996.

Community: The incidence of CRC in the remaining population (community) was determined from the number of cases that occurred between 1994 and 1997 in people not registered as a colonoscopy patient per the region's population less the colonoscopy population. Population data were obtained from the August 1996 census undertaken by the Australian Bureau of Statistics.9

Statistical analyses Binary data were compared in two by two contingency tables using chi-squared analyses.12 The age-standardised incidences of CRC in colonoscopy patients versus the community were tested for the hypothesis that the ratios were equal to one.13

Results
Colonoscopies From mid 1985 to the end of 1996, I performed 11 148 colonoscopies on 8430 patients (Figure 2). The number increased steadily, from 590 in the 18 months 1985-1986 to 2708 in the two years 1995-1996. The number of repeat colonoscopies increased from 12 (2.0%) in 1985-1986 to 875 (32.3%) in 1995-1996.

Clinical and procedural characteristics are summarised in Box 1. Slightly more women than men had colonoscopies. Patients undergoing repeat colonoscopies were an average six years older than those newly referred and were more likely to have had surveillance for increased CRC risk as the primary indication (50.7% of repeat colonoscopies versus 15.0% of first colonoscopies; P < 0.0001). Primary indication also varied with time. For example, an abnormal barium enema was a common indication before 1991 (7.0%), but accounted for few after 1994 (0.3%; P < 0.0001). In contrast, a family history of polyps or CRC accounted for a greater proportion of colonoscopies after 1994 (10.6% of first and 11.2% of repeat colonoscopies) than before 1991 (6.3%; P < 0.0001).

From the outset, the caecal completion rate exceeded 95%, and from 1994 it was 98.9% overall and 99.5% in those without a malignant obstruction. Polyps were diagnosed (and removed) in a greater proportion of repeat than first colonoscopies (36.1% versus 29.8%; P < 0.0001). Both these rates were higher than for colonoscopies performed before 1991 (24.5%; P < 0.0001). However, CRC was diagnosed less often in repeat than in first colonoscopies (0.6% versus 2.2%; P = 0.001).

Resident populations Complete details, including a middle name, were recorded for 5762 of the 8430 colonoscopy patients (68.4%), and 4200 of these (72.9%) were registered voters and residents of the Townsville region in 1997. A surname and one given name only were recorded for the remaining 2668 patients -- 1913 from the hospital's computer register and 755 from the work ledger. This gave an estimated total number of resident colonoscopy patients of 6195 in 1997.

Colorectal cancers Between 1994 and 1997, 476 new CRCs were diagnosed in residents of the Townsville region, with 474 in people aged over 35 years. Eighteen were in patients who had had a previous colonoscopy; each of these was diagnosed per colonoscopy by myself, nine at the study hospital (registered in the procedural database and shown in Box 1), and the remainder elsewhere.

Incidences of CRC

 between 1994 and 1997 are shown in Box 2. In people aged over 50 years, the annual incidence of CRC in the colonoscopy population (1.14) was just less than half that in the remaining community (2.31; P = 0.0046).

Between July 1985 and January 1998, I diagnosed 31 CRCs in 29 patients who had had a previous colonoscopy (two patients had a second CRC diagnosed two years after the first in each case). All but one of these patients had a personal or family history that warranted surveillance, and 21 had been enrolled in surveillance programs, with 20 (65%) having had multiple previous colonoscopies (mean, 3.4; range, 2-9). For 20 of the CRCs, planned surveillance was the indication for the repeat colonoscopy. Among the 11 people with symptoms as the primary indication, these symptoms were considered unrelated to the CRC in at least three. The time between most recent previous colonoscopy and diagnosis averaged 37 months (range, 3-136 months).

Staging of CRCs is shown in Box 3. Metastatic spread from CRCs was less common in patients who had had a previous colonoscopy than in the community; only five of the 31 cases in colonoscopy patients were graded C, and none were graded D, while 219 of the 458 community cases (48%) were graded C or D (P < 0.001). Among the five colonoscopy patients with metastatic spread (Dukes C), the time between most recent previous colonoscopy and diagnosis was 19, 24, 29, 32 and 70 months, respectively.

Discussion The study evaluated a colonoscopic service that followed and promoted contemporary surveillance guidelines similar to those currently recommended by professional cancer and gastroenterological societies.3 The incidence data suggest, but do not prove, that colonoscopic surveillance confers a benefit. Age-standardised incidence of CRC among people aged 50 years and over in the Townsville region was lower among those who had had a previous colonoscopy, along with any treatment considered necessary (eg, polypectomy or bowel resection), than in the community. This was despite the fact that many of those who had had a previous colonoscopy had a personal or family history likely to increase their risk of developing CRC. Furthermore, the CRCs that occurred in those who had had a previous colonoscopy were of a lower Dukes grade than those occurring in the community.

The difference in incidence suggests but does not prove that colonoscopy is protective against CRC. CRC incidence for 1994-1997 in those who had had a previous colonoscopy may have been reduced, at least partly, by detection of subclinical CRCs during their pre-1994 colonoscopies. On the other hand, selection bias suggests that these people would develop more CRCs than the general population. The impact of each of these factors could not be measured, and there is no historical benchmark or matched population for comparison of outcomes. However, the result does suggest that colonoscopy confers a benefit, possibly because of removal of polyps and certainly because of detection and treatment of subclinical CRCs.

In people aged 35-49 years, CRC incidence in those who had had a previous colonoscopy was similar to that in the community. Without a control group, a benefit of colonoscopy cannot be dismissed, as the colonoscopy group was expected to have higher CRC incidence. However, it is evident that, because of the large number of people aged 35 to 49 years and the low incidence of CRC, surveillance must be targeted to be effective.

Polypectomy rate was high, and higher in repeat than in first colonoscopies. This also implies that patients having repeat colonoscopies had increased risk of developing CRC.14 While the high polyp rate may have been due to their older average age,15 the latter would also be expected to increase the CRC rate, which did not occur. Given an expectation that all lesions seen at the previous colonoscopy had been dealt with, this outcome (high polyp versus low CRC rate) validates the selection criteria for surveillance. The higher polypectomy rate after 1994 compared with that before 1990 probably relates to other circumstances, such as a higher caecal completion rate, while both indices probably reflect improved instrument technology.

Thirty-one new primary cancers developed in 29 colonoscopy patients, with two-thirds diagnosed by planned surveillance colonoscopy. Metastatic spread occurred in only five of these patients. These findings confirm, firstly, that new CRCs will develop and, secondly, that outcome can be improved through early (subclinical) diagnosis.3,16

The number of cancers diagnosed in patients who had had a previous colonoscopy was of concern and suggested lesions might have been missed in the earlier examination. Colonoscopy, even when performed by an expert, does not identify all small lesions, while adverse conditions sometimes obscure gross pathology.17 Colon morphology, quality of the bowel preparation, instrument capabilities and operator proficiency may also impose limitations.3,18 However, substandard colonoscopy is unlikely to have been responsible. The caecum was reached at a rate exceeding the accepted standard (95%),3 and CRCs were observed in all parts of the bowel, arguing against an operator-dependent blind spot.

Possibly, the comparatively large number of CRCs found in people undergoing colonoscopic surveillance was simply the outcome of increasing enlistment of an appropriate, at-risk cohort. Although most sporadic CRCs evolve slowly through malignant transition in a polyp, this sequence is truncated or absent for some sporadic CRCs and for CRCs developing in patients with ulcerative colitis or a genetic predisposition.19 It is unrealistic to imagine that surveillance colonoscopy with polypectomy as necessary will much reduce CRC incidence in such at-risk populations. Indeed, it might conceivably increase apparent incidence by uncovering subclinical CRCs.

The results support the current practice of targeting individuals with recognised risk factors for surveillance colonoscopy. However, it is important to explain to patients that surveillance does not provide complete protection and that new CRCs are inevitable. Early diagnosis through repeated testing is the essential component of surveillance-derived protection.

References
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  2. SEER Program (National Cancer Institute). Surveillance, epidemiology, and end results (SEER) program. Bethesda, Md: National Cancer Institute, 1973-1992.
  3. Winawer SJ, Fletcher RH, Miller L, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology 1997; 112: 594-642.
  4. Bolin TD, Korman MG. How can we reduce the incidence and mortality of colorectal cancer [editorial]? Med J Aust 1997; 166: 175-176.
  5. Macrae FA. Screening for colorectal cancer, 1996 [editorial]. Med J Aust 1996; 165: 102-105.
  6. Bell JC, McCredie M, Coates MS, Armstrong BK. Trends in colorectal cancer incidence and mortality in New South Wales, 1973-1992. Med J Aust 1997; 166: 178-181.
  7. Mecklin J-P, Jarvinen HJ, Peltokallio P. Cancer family syndrome. Genetic analysis of 22 Finnish kindreds. Gastroenterology 1986; 90: 328-333.
  8. Astler VB, Coller FA. The prognostic significance of direct extension of carcinoma of the colon and rectum. Ann Surg 1954; 139: 846-851.
  9. Dunlop MG. Polyps and carcinoma. In: Shearman DJC, Finlayson N, Camillieri, Carter D, editors. Diseases of the gastrointestinal tract and liver. 3rd ed. New York: Churchill Livingstone, 1997: 1399-1448.
  10. Australian Electoral Commission. Elector information access system. Electoral roll information for Queensland. Canberra: Australian Electoral Commission, 1997.
  11. Australian Bureau of Statistics. 1996 census of population and housing. Community profile, Canberra: ABS, 1996 (Cat. no. 2020.0).
  12. Approximate significance for contingency tables. In: Matthews DE, Farewell VT. Using and understanding medical statistics. 2nd ed. Basel: Karger, 1988: 20-66.
  13. The binomial distribution. In: Snedecor GW, Cochran WG. Statistical methods. 8th ed. Ames: Iowa State University Press, 1989: 107-134.
  14. Atkin WS, Morson BC, Cuzick J. Long-term risk of colorectal cancer after excision of rectosigmoid adenomas. N Engl J Med 1992; 326: 658-662.
  15. Williams AR, Balasooriya BAW, Day DW. Polyps and cancer of the large bowel: a necropsy study in Liverpool. Gut 1982; 123: 835-842.
  16. Mandel JS, Bond JH, Church TR, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 1993; 328: 1365-1371. (Published erratum appears in N Engl J Med 1993; 329: 672.)
  17. Rex RK, Cutler CS, Lemmel GT, et al. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology 1997; 112: 24-28.
  18. Baille J, Ravich WJ. On endoscopic training and procedural competence. Ann Intern Med 1993; 118: 73-74.
  19. Kuramoto S, Oohara T. Flat early cancers of the large intestine. Cancer 1989; 64: 950-955.

(Received 1 May, accepted 21 Dec, 1998)

Author's Details 42 Ross River Road, Townsville, QLD.
 John Croese, MD, FRACP, Gastroenterologist.

Reprints will not be available from the author.
Correspondence: Dr J Croese, 42 Ross River Road, Townsville, QLD 4812.
Email: jcroeseATmedeserv.com.au




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Figure 1

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Box 1

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Box 2

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Box 3

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Received 22 December 2024, accepted 22 December 2024

  • John Croese



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