Original Article

Aspirin Use and Reduced Risk of Fatal Colon Cancer

Michael J. Thun, M.D., Mohan M. Namboodiri, B.S., and Clark W. Heath, Jr., M.D.

N Engl J Med 1991; 325:1593-1596December 5, 1991

Abstract

Abstract

Background and Methods.

Experiments in animals and two epidemiologic studies in humans suggest that aspirin and other nonsteroidal antiinflammatory drugs (NSAIDs) may be protective against colon cancer. We tested this hypothesis in a prospective mortality study of 662,424 adults who provided information in 1982 on the frequency and duration of their aspirin use. Death rates from colon cancer were measured through 1988. The possible influence of other risk factors for colon cancer was examined in multivariate analyses for 598 case patients and 3058 matched control subjects drawn from the cohort.

Full Text of Background and Methods. ...

Results.

Death rates from colon cancer decreased with more frequent aspirin use in both men and women. The relative risk among persons who used aspirin 16 or more times per month for at least one year was 0.60 in men (95 percent confidence interval, 0.40 to 0.89) and 0.58 in women (95 percent confidence interval, 0.37 to 0.90). The risk estimates were unaffected when we excluded persons who reported at entry into the study that they had cancer, heart disease, stroke, or another condition that might influence both their aspirin use and their mortality. Adjustment for dietary factors, obesity, physical activity, and family history did not alter the findings significantly. No association was found between the use of acetaminophen and the risk of colon cancer.

Full Text of Results. ...

Conclusions.

Regular aspirin use at low doses may reduce the risk of fatal colon cancer. Whether this is due to a direct effect of aspirin, perhaps mediated by the inhibition of prostaglandin synthesis, or to other factors indirectly associated with aspirin use is unclear. (N Engl J Med 1991;325:1593—6.)

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Media in This Article

Table 1Rates of Death from Colon Cancer, According to Frequency of Aspirin Use, in the Cohort before Patients with Illness at Enrollment Were Excluded.

Table 2Rates of Death from Colon Cancer, According to Frequency of Aspirin Use, after the Exclusion of Patients Who Had Selected Illnesses at Enrollment.*

Article Activity

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Article

NONSTEROIDAL antiinflammatory drugs (NSAIDs), such as aspirin, indomethacin, piroxicam, and sulindac, inhibit the growth of colon tumors induced by chemical carcinogens in rodents.1 2 3 4 5 6 7 8 9 10 11 12 13 The mechanism is unknown, but it may involve the suppression of cell proliferation or the stimulation of an immune response, due to an inhibitory effect on prostaglandin synthesis.14 15 16 17 18 A similar effect in humans has been suggested by case reports and by a small randomized clinical trial describing the regression of large-bowel polyps in patients with familial polyposis treated with sulindac.19 20 21

Three recent epidemiologic studies have examined the occurrence of cancer of the colon or rectum in humans in relation to the use of aspirin and other NSAIDs.22 23 24 25 26 A large hospital-based case–control study compared 1326 patients who had colorectal cancer with 4891 control subjects with respect to NSAID use.22 , 26 Regular use of NSAIDs (at least four days a week for a minimum of three months) was associated with a 50 percent reduction in the combined risk of cancer at either site. A population-based case–control study from Australia found a similar reduction in the risk of colorectal cancer among persons taking medications containing aspirin and a lowered risk of cancer of the colon but not of the rectum in persons taking other NSAIDs.23 In contrast, a prospective study of 13,987 residents of a California retirement community found a slightly increased incidence of cancer of the colon among daily aspirin users.24 , 25 We examined the relation of regular aspirin use to fatal colon cancer in a large, prospective study of North American adults.

Methods

The analysis included 662,424 men and women drawn from among those enrolled in Cancer Prevention Study II, an ongoing prospective mortality study of 1,185,239 persons enrolled by 77,000 volunteers for the American Cancer Society in the fall of 1982.27 Many of the participants in the study were friends, neighbors, or acquaintances of the volunteers. In all 50 states, the District of Columbia, and Puerto Rico, families were enrolled in which at least one household member was 45 years old or older, and all enrolled members were 30 or older. The average age at the time of enrollment was 57 years.

The participants' vital status was determined at two-year intervals through personal inquiries by the volunteers. The mortality follow-up was complete through August 31, 1988. By then, 79,877 participants (6.7 percent) had died, 1,083,531 (91.4 percent) were alive, and 21,831 (1.8 percent) were lost to follow-up. Death certificates were obtained for 94.1 percent of the persons known to have died. Using the system described in the International Classification of Diseases, 9th Revision (ICD-9), a nosologist coded the cancer deaths according to the first three digits of the ICD-9 code.

At the time of enrollment, the participants completed a four-page questionnaire on their medication use, smoking history, diet, alcohol intake, physical activity, occupation, height, weight, current medical illnesses, family history of cancer, and other characteristics. For each of 15 categories of medications, the questionnaire asked two questions: "How many times in the last month have you used the following [medications]?" and "How long (in years) have you used them?" The first category listed was "Aspirin, Bufferin, and Anacin," and the second was "Tylenol" (acetaminophen). The other categories included vitamins, tranquilizers, and medications for specific medical conditions.

The 662,424 people who formed the basis of the analysis constituted all the white people who specified both the frequency and the duration of their aspirin use on the completed questionnaires. The 81,614 nonwhite members of the cohort were excluded because there were only small numbers of deaths in this group. Data on the frequency of aspirin use were missing for 218,293 of the 1,103,625 white participants (19.8 percent) and were incomplete (i.e., the frequency was specified, but the duration was left blank) for 220,401 (20.0 percent). An additional 2507 persons were excluded because they had used aspirin for less than one year.

Cohort Analyses

Age-adjusted death rates for colon cancer (ICD-9 code 153) were computed on the basis of the underlying cause as coded from the death certificates. Deaths assigned to code 154 (rectal cancer) were not included. The number of person-years at risk was determined from the month of enrollment through August 31, 1988. Persons lost to follow-up were considered to be alive, since the date of the loss to follow-up was not recorded. In the adjustment for age, the age distribution of the overall cohort was used for direct standardization.

Rates of death from colon cancer were calculated according to whether the participants specified that they had not used aspirin or that they had used it with one of the following three frequencies per month: less than once, 1 to 15 times, or 16 or more times per month. Among the aspirin users, the analysis was restricted to those who specified that they had used aspirin for at least one year. Similar calculations were made with respect to acetaminophen. Relative risks were computed with the subjects who did not use aspirin serving as the referent group, and 95 percent confidence intervals were calculated on the basis of approximate-variance formulas.28 , 29

The relation of death rates to aspirin use was studied in the entire cohort and in two subgroups. One subgroup (containing 658,961 people) excluded those who reported having colon cancer at the time of enrollment, and the other subgroup (containing 508,021 people) excluded those who reported having any type of cancer (except skin cancer other than melanoma), heart disease, or stroke at the time of enrollment or who described themselves as "sick" at that time. Tests of trend in the person-year analyses and two-tailed P values were based on the Mantel extension test.30

Adjustment for Other Risk Factors

Because the cohort was large, we assessed the possible influence of other risk factors for colon cancer in multivariate, nested case–control analyses for 598 case patients and 3058 control subjects drawn from the cohort. In this analysis, we excluded persons with cancer or other disorders at enrollment; persons for whom the data on diet, physical activity, height, or weight were incomplete; and persons lost to follow-up. For each case patient, five controls matched for sex and exact age were selected by incidence-density sampling.31 The multivariate analyses used conditional and unconditional logistic regression. In addition to aspirin use, the variables included a history of colon cancer in a parent or sibling (a categorical variable); body-mass index (calculated as the weight in kilograms divided by the square of the height in meters; a continuous variable); physical activity (none, slight, moderate, or heavy); fruit, vegetable, and grain consumption (the sum of 14 food groups categorized in quintiles according to frequency of consumption per week); and total fat consumption (a partial nutrient index based on the consumption of eight meats, five dairy products, and eggs, categorized in quintiles). Ninety-five percent confidence intervals and tests of trend were computed by conditional- and unconditional-likelihood procedures.32 The results of these analyses were very similar. We present only the results of the unconditional analyses, which include the full number of case patients and controls.

Results

Cohort Analyses

Rates of death from colon cancer decreased with more frequent aspirin use among both men and women in the overall cohort (Table 1Table 1Rates of Death from Colon Cancer, According to Frequency of Aspirin Use, in the Cohort before Patients with Illness at Enrollment Were Excluded.). The relative risk among persons using aspirin 16 or more times per month for at least one year was 0.60 for men (95 percent confidence interval, 0.40 to 0.89) and 0.58 for women (95 percent confidence interval, 0.37 to 0.90). The results were similar after the exclusion of people with cancer or other conditions that might influence both aspirin use and mortality (Table 2Table 2Rates of Death from Colon Cancer, According to Frequency of Aspirin Use, after the Exclusion of Patients Who Had Selected Illnesses at Enrollment.*). Although about half of all those who died of colon cancer were excluded because of these conditions, the estimates of relative risk associated with each category of aspirin use were virtually unchanged, and the trend associated with more frequent aspirin use remained statistically significant for both men and women.

Adjustment for Other Risk Factors

Table 3Table 3Relative Risk of Death from Colon Cancer According to Frequency of Aspirin Use, with Adjustment for Other Suspected Risk Factors in the Case–Control Analyses.* shows the results of the case–control analyses after we controlled for other potential risk factors. The relative risks for aspirin alone (in the unadjusted analysis) remained virtually unchanged after we controlled for dietary fat consumption; vegetable, fruit, and grain consumption; obesity; physical activity; and family history. The risk of death from colon cancer among persons using aspirin 16 or more times per month remained approximately half that of nonusers, and the trend toward decreasing risk with increasing dose remained statistically significant in both sexes. We repeated the multivariate analysis after excluding 138 case patients and 720 control subjects who reported having arthritis at the time of enrollment. The adjusted relative risks were again unchanged, and the tests of trend were statistically significant.

We tested the possibility that the exclusion of persons who had not specified both the frequency and the duration of their aspirin use on the initial questionnaire might have biased our findings. The risk of fatal colon cancer among persons who gave no information about their aspirin use was similar to that among nonusers (relative risk, 0.98 for men and 0.90 for women), whereas among persons who specified the frequency but not the duration of use, the risk resembled that among the aspirin users (relative risk, 0.80 for men and 0.73 for women). No evidence was found that people for whom there were insufficient data had an increased risk.

Acetaminophen

In contrast to aspirin, acetaminophen was not associated with a decrease in the risk of fatal colon cancer, in either the cohort analysis or the case–control analysis. Among users of acetaminophen who took no aspirin, there was a statistically insignificant trend toward increased risk. Few people in the cohort used acetaminophen regularly, however. Only 9 case patients and 25 controls reported using it 16 or more times per month for one year or more, as compared with 46 case patients and 388 controls who reported using aspirin with this frequency.

Discussion

These prospective data support the hypothesis that the regular use of aspirin may decrease the risk of fatal colon cancer. Several aspects of the data suggest that the relation may be causal. These include the strength of the association, its internal consistency when the data were analyzed in a variety of ways, the statistically significant dose–response trends in both men and women, the persistence of the decreased risk after control for other risk factors, and the similarity between these findings and those in two previously published case–control studies.22 , 23 The data were also consistent with the limited clinical experience with sulindac in the treatment of familial polyposis19 20 21 and with the results of extensive experiments in animals.1 2 3 4 5 6 7 8 9 10 11 12 13 The latter have consistently shown chemically induced colon tumors in rats and mice to be inhibited by treatment with various NSAIDs. The effect appears to be dose-related,10 , 11 and it involves the modification of tumor growth over a range of intervals after tumor induction.

Our study is limited by its dependence on a single, brief, self-administered questionnaire, by the absence of data on the quantity of aspirin used (as opposed to the frequency and duration), by the lack of information on the reasons for aspirin use, and by the study's reliance on rates of mortality due to cancer, rather than incidence rates, to define the presence of the disease.

At least three potential biases must be considered that might lead to a spurious association of deaths from colon cancer with aspirin use. First, the reasons for taking aspirin, rather than the medication itself, might be associated with the reduced risk of colon cancer. The persistence of the association after the exclusion of many conditions that could influence both aspirin use and mortality suggests that none of the conditions excluded account for the finding.

A second potential bias could be created by the association of aspirin use with other attributes of a healthful lifestyle, when these attributes, rather than aspirin, might result in a lowered risk of colon cancer. We can be reasonably sure that diet, physical activity, and obesity are unlikely sources of bias, but we have no information with which to control for the use of sigmoidoscopy or other screening procedures.

A third potential bias, which is of less concern in prospective studies than in retrospective ones, might arise from our exclusion of many cohort members who did not specify both the frequency and the duration of their aspirin use. We found no evidence that persons for whom data were incomplete or missing were at higher risk than nonusers of aspirin with complete data. It is therefore unlikely that the exclusion of these persons could have biased our findings.

If aspirin does influence mortality due to colon cancer, it might do so either by improving survival or by reducing the incidence of cancer. The latter possibility has been suggested by two earlier reports that studied incident cases.22 , 23 Therapeutic value, however, is suggested by the smaller and less numerous tumors in laboratory animals given aspirin after exposure to carcinogens1 2 3 4 5 6 7 8 9 10 11 12 13 and by the regression of benign colon tumors that occurs in persons with Gardner's syndrome or diffuse adenomatous polyposis after treatment with sulindac.19 20 21

Our study seems compatible with either hypothesis. Since it encompassed only six years of follow-up and examined mortality rather than incidence, most of the colon cancers, or their precursor lesions, may have been present but undiagnosed at enrollment, and hence it is possible that there was a treatment effect. This may explain why the relative risks were similar with and without the exclusion of the persons who had colon cancer at enrollment. It is also possible that aspirin may induce bleeding among persons with polyps or early cancers and thus lead to earlier diagnosis and improved survival.

The findings resemble those of Rosenberg et al.22 and Kune et al.23 Although the designs differ, all three studies gathered data on aspirin use close to the time of the diagnosis of cancer. The discrepancy between our results and those of Paganini-Hill et al.24 , 25 is unexplained. That study examined the incidence of cancer in a relatively small elderly population. Persons who did not use aspirin at the start of the study may have begun to use it during the seven-year follow-up period. Aspirin use was recorded only in terms of frequency and may well have antedated the diagnosis of cancer by a considerable interval.

Further studies in human populations are needed to define more clearly the relation of NSAID use to the occurrence of colon cancer. The numerous randomized trials that have studied aspirin use in the prevention of cardiovascular disease33 34 35 may be informative, although their combined number of subjects is small (about 62,000). Additional controlled trials of treatment with aspirin or other NSAIDs in persons at high risk for colon cancer may be warranted.

We are indebted to Mr. Steven Reading and Mr. David Harris for programming assistance; to Dr. Eugenia Calle and Dr. Dana Flanders for editorial comment; and to Mr. Lawrence Garfinkel, Dr. Steven Stellman, and the volunteers and staff of the American Cancer Society whose efforts created Cancer Prevention Study II.

Source Information

From the Department of Epidemiology and Statistics, American Cancer Society, 1599 Clifton Rd., Atlanta, GA 30329, where reprint requests should be addressed to Dr. Thun.

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