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Cancer Letters, 52 (1990) 163-171 Elsevier Scientific Publishers Ireland Ltd.
Review Letter
Coffee and tea consumption in relation to the risk of large bowel cancer: a review of epidemiologic studies L
. Rosenberg
Slone Epidemiology
Unit, School of Public Health,
Boston
UnioersitySchool
of Medicine,
1371 Beacon Street, Brook-
line, MA 02146 (U.S.A.) (Received Jan 17 1990) (Revison received 7 May 1990) (Accepted 9 May 1990)
Summary Most of the few epidemiologic investigations of the relation of methylxanthine ingestion to risk of large bowel cancer haue concerned coffee consumption. A slightly increased risk in coffee drinkers was suggested by one study, no association by another and an inuerse association by four, but there was a statistically significant trend across levels of consumpfion in only one of the latter studies. Based on the data on hand, there is little reason for concern that coffee consumption increases the risk. Although some euidence suggests an inverse association, the data are not compelling and a biologic mechanism is not established. There is euen less information on tea consumption and the relation of consumption of this beuerage to risk of large bowel cancer is unknown. ‘Keywords:
coffee;
methylxanthines;
colonic neoplasms; rectal neoplasms; tea.
Introduction Coffee, a major sauce of dietary methylxanthines, contains mutagens and can inhibit DNA
repair [20,41,41]. Coffee consumption has been linked to increases in the risk of bladder cancer [5] and pancreatic cancer [25], but the relationship with bladder cancer, if real, is weak [12,29] and the association with pancreatic cancer observed in a hypothisesraising study has not been confirmed [44,46]. It has been proposed that coffee consumption may lead to a reduction in the risk of large bowel cancer, based on the following reasoning [4,16,24]. Cholesterol, bile acids and their metabolites, particularly secondary bile acids, are promoters of colon carcinogens in animals [33]. Fecal concentrations of bile acids and metabolites are greater in patients who have colorectal cancer, or who are at high risk because of predisposing conditions such as adematous polyps, than in comparison patients [14,23], and they are also greater in healthy persons from populations with high colon cancer risk as compared with persons from low risk populations [32,43]. Lower serum cholesterol levels may indicate increased cholesterol excretion in some persons who consume high fat diets [24] (and if this is so, it could explain the inverse association of colon cancer with serum cholesterol
0304-3835/90/$03.50 0 1990 Elsevier Scientific Publishers Ireland Ltd Published and Printed in Ireland
164
observed in some studies [35]). Coffee has been linked to increased serum cholesterol levels, particularly in populations with high fat diets [6,8,11,18,19,43,54]. If the mechansim leading to higher cholesterol levels involves a reduction in the excretion of bile acids, neutral setrols, or both [4,16,24], coffee consumption might reduce the risk of colon cancer. While the proposed mechanism appears reasonable, it is speculative: the possibility that preclinical large bowel cancer reduces cholesterol levels [27] has not been excluded as an explanation for an inverse association of serum cholesterol with colon cancer [35] and direct evidence on the effect of coffee consumption on bile acid excretion from the liver is lacking [2]. Most epidemiologic studies of diet and large bowel cancer have assessed coffee only peripherally, but several recent studies have assessed coffee use in detail. Tea, the other major source of dietary metylxanthine, has received less attention and there are no informative data on colas. All studies of large bowel cancer in which coffee or tea are mentioned are considerd beow, in chronological order and relevant details of the studies are also given in Table 1. Epidemiologic studies In 1973, Haenszel et al. [lo] reported on a hospital-based case-control study of men and women of Japanese descent in Hawaii, conducted from 1966-1970. A total of 179 patients with large bowel cancer were compared with 357 age- and sex-matched controls with non-digestive tract illnesses. The frequency of consumption of a large variety of foods was determined by interview. Relative risk for “above-average” and “below-average” frequencies of use were presented for each food and beverage. Consumption of Westernstyle food - in particular, beef, legumes, and starches - was associated with increased risk. Unexpectedly, there was inverse association with coffee consumption. The relative risk was given as 0.72, but confidence intervals and the distribution of cases and controls according to coffee consumption were not presented.
Bjelke’s doctoral work on large bowel cancer [3] has been cited as evidence of an inverse association with coffee. The validity of the results is difficult to assess, however, because details of the methods have not been published in a peer-reviewed journal. In a letter to the editor in 1974 [4], Bjelke described a case-control study of Norwegian men in which 162 cases were compared with 444 controls: relative to consumption of < 3 cups of coffee per day, the relative risk estimate was 0.6 for consumption of 2 5 cups per day. Bjelke also described preliminary results of a follow-up of 12,166 Norwegian men, which suggested a lower risk of colon cancer in those who drank Z 5 cups of coffee per day relative to those who drank < 3 cups per day. Subsequent results after longer follow-up, reported by Jacobsen et al. [ 151, are described below. In 1978 Graham et al. [9] published results from a case-control study conducted from 1959 to 1965 in a cancer hospital in Buffalo. The cases, 256 white males with colon cancer and 330 with rectal cancer, were compared with white male control patients with nonmalignant non-gastrointestinal illnesses, selected from a total pool of 1222 controls: 783 controls were frequency-matched on age to the colon cancer cases and 628 to the rectal cancer cases. The frequency of ingestion of selected specific foods was ascertained by interview. The main finding was an inverse association of large bowel cancer risk with frequent ingestion of vegetables. A “significant but small” increase (not specified) in risk of colon cancer was reported for “frequent” drinking of coffee, but there was no association with rectal cancer; the data on coffee were not given. In 1979, Dales et al. [7] reported on a study of 99 black cases of colorectal cancer and 280 black controls matched on sex, age and hospital. The participation rate was 40% for cases and 50% for controls. Information was obtained by interview on the frequency of consumption 3 years previously of 89 food items. Large bowel cancer was associated positively with consumption of foods with a high saturated fat content and inversely with foods
165
with a high fiber content. There was “virtually no relationship” with coffee and “a small, statistically non-significant positive association” with tea; no data were given. In 1981, Abu-Zeid et al. [l] published an abstract on a case-control study of colorectal cancer conducted in two hospitals in Winnipeg. Each of 197 cases of large bowel cancer was matched for age, sex, race, residence and hospital with a control. Dietary histories were obtained by interview and multivariate analyses were conducted. “A low risk was associated with.. drinking coffee” but the data were not presented. In 1983, Miller et al. [28] presented results on coffee based on data from a case-control study of large bowel cancer conducted in Toronto and Calgary from 1976 to 1978; an earlier report did not include an assessment of coffee [17]. The cases (348 colon cancer and 194 rectal cancer) were compared with 542 age- and sex-matched neighbor controls and 535 hospital controls who had had abdominal surgery. The participation rates of cases and hospital controls were 80% and 81%) respectively; the participation rate of neighbor controls was lower, but it was not specified. In home interviews, information on consumption 6 months previously of 150 fcod items was collected with the aid of food models. Relative risks were presented for the second and third tertiles of consumption relative to the lowest tertile. “Beverages,” which included “tea, coffee, cola, etc.” were not associated with either colon or rectal cancer and no trend was apparent across tertiles. Data were not given on coffee and tea separately. In 1984 and 1985, Snowdon et al. [40] and Phillips et al. [31] reported on a 21-year follow-up study of Seventh-day Adventists. Baseline data on consumption of 21 foods and beverages had been obtained at entry by selfadministered questionnaire from 25,493 white subjects [31]. Deaths were ascertained through use of California death certificates, a method that identified an estimated 85% of the total deaths. Among men, there was a statistically significant increase in the relative risk estimate of colon cancer with increasing
consumption of coffee, based on 33 cases who consumed < 1 cup per day, five who consumed 1 cup per day and 15 who consumed 2 2 cups per day; the relative risk estimate for drinkers of Z 2 cups per day was 2.0 (95% confidence interval (CI) 1.1-3.6). A weaker trend in women, based on a total of 83 cases, was not statistically significant. There were only 28 cases of rectal cancer on whom data on coffee use were available and there was no evidence of a significant trend. The association with colon cancer in both men and women was confined to the last 11 years of follow-up; when this period was considered, trends were significant in both men and women. There was “no significant relationship” with tea or soft drinks [31]. The results of a follow-up study of 7355 Japanese men in Hawaii from 1965 to 1968 until 1983 were reported by Nomura et al. in 1986 [30]. The men gave 24-h dietary recalls at entry. Coffee consumption was not significantly related to the incidence of large bowel cancer. For colon cancer (108 cases), the ageadjusted incidence was similar at all levels of coffee consumption (17.3 per 1000 for >/ 5 cups per day versus 13.5 per 1000 for 0 cups per day). For rectal cancer (60 cases), there was a trend of decreasing incidence across increasing levels of consumption, but it was not statistically significant (P = 0.134). A report by Heilbrun et al. on tea consumption in the same Hawaiian Japanese cohort was published in 1986 [ 131. Tea consumption had been recorded at entry. During follow-up until 1985, 152 cases of colon cancer and 76 of rectal cancer were identified. Relative risk estimates were derived from proportional hazards regression models with adjustment for age. For rectal cancer, allowance was also made for alcohol intake and, in some analyses, for saturated fat intake. For rectal cancer, the relative risk increased across levels of consumption (P = 0.0007): for men who consumed tea at least once per day relative to those who almost never drank it, the estimate was 4.2, based on five exposed cases. The association was present in men who were aged 58 or older and absent in younger men. Tea
et al. [9]
1985
Snowdon et al. [4O] 1984 Phillips et al. (311
Abu-Zeid et al. [ 1] 1981 Miller et al. 1281 1983
Dales et al. [ 171 1979
Graham 1978
1967-1968
Bjelke [4] 1974
Hospital-based case-control Case-control
Follow-up
?
1976-1978
1960-1980
1960-1981
Hospital-based case-control
Hospital-based case-control
Follow-up
Hospital-based case-control
Hospital-based case-control
1976
1973-
1959-1965
?
1970
1966-
Type of study
studies of large bowel cancer
Haenszel et al. [lo] 1973
Epidemiologic
Years of study
1.
Author/ Year of publication
fable
men
deaths
Males - 56 colon cancer deaths; females - 91 colon cancer deaths 35 rectal cancer
U.S. 7th-Day Adventists Ca 25,000 followed
Rectal cancer: >1 cup/day vs. < 1 cup/day
< 1 cup/day
Coffee: Colon cancer: 22 cups/day vs.
Beverages (“tea, coffee, cola, etc.“) highest tertile vs. lowest
Canadians 348 colon cancer 194 rectal cancer 542 neighbor controls 535 hospital controls
Coffee: any
Females RR = 1.5 P(trend) = 0.20 Rectal cancer: RR = 1.4 P&end) = 0.38
Colon cancer: males RR = 2.0 P (trend) = 0.04
non-signlftcant positive association” “A low risk” for coffee drinkers Colon cancer: malesRR = 0.9 female RR = 1.1 Rectal cancer: malesRR = 1.1 QmalesRR = 0.8
“Small, statistically
Tea: any
Coffee: “frequent drinking”
Coffee: any
-
RR = 0.6 Cl not given
Colon cancer: “Significant but small excess risk” Rectal cancer: No association “No relationship”
vs. “below average” Coffee: 35 cups/day vs. < 3 cups/day -
not given
Results given from 1311 Coffee consumption related to increased risk in second half of follow-up but not first Coffee was proscribed by church; association may be confounded by other “lifestyle” factors
Data on coffee consumption not given Data not given separately on tea, coffee and colas
Low participation rate Data on coffee and tea consumption not given
Details of methods not given Longer follow-up reported in Jacobsen [ 151 Data on coffee consumption not given
Details of methods
Data on coffee consumption not given
Coffee: “above-average” RR = 0.72 Cl not given
Comments
Exposure
Canadian
U.S. Blacks 99 cases 280 controls
U.S. men 156 colon cancer 330 rectal cancer 1222 control
Norwegian
Norwegians 162 cases 444 controls
Hawaiian Japanese 179 cases 357 controls
Study population
in relation to coffee or tea consumption. z
1967-
Jacobsen 1986
from incidence
‘Calculated
rates
1986
1978-
et al. [38]
Hospital-based case-control
Hosptial-based case-control
Rosenberg 1987
1988
et al. [22]
LaVecchia 1989
1983-
Hospital-based case-control
1987
1983-
et al. [21]
Hospital-based
LaVecchia 1988
1979-1986 case-control
et al.
Follow-up
Follow-up
Follow-up
1986
P61
Macquart-Moulin
1978
1985
1965-
Heilbrun et al. [13] 1986
et al. [15]
1983
1965-
et al. 1301
Nomura 1986
men
men
U.S. 717 colon cancer 538 rectal cancer 3833 controls
Italians 455 colon cancer 295 rectal cancer 1944 controls
Italians 339 colon cancer 236 rectal cancer 778 controls
399 cases 399 controls
French
Norwegians 100 colon cancer deaths 64 rectal cancer deaths
Japanese Hawaiian 7355 followed 108 colon cancer 60 rectal cancer Japanese Hawaiian 7833 followed 152 colon cancer 76 rectal cancer
VS.
2 cups/day
= 0.16
Colon cancer:
RR = 0.6 95% Cl 0.4-0.8 no trend Rectal cancer: RR = 1.2 95% ClO.8-1.8 no trend 25 cups/day vs. 1 cup/day
Colon cancer: RR = 1.38 P> 0.05 Rectal cancer: RR = < 1.54 P< 0.05 Colon cancer: RR = 0.64 P (trend) < 0.01 Rectal cancer: RR =0.66 P (trend) < 0.05
P (trend)
RR = 1.07 P(trend) = 0.94 RR = 0.55
RR = 1.28’ P(trend) = 0.98 RR = 0.55’ P (trend) = 0.13 Rectal cancer: RR = 4.2 P(trend) = 0.0007 Colon cancer: no association P(trend) = 0.25 Colon cancer: RR = 0.59 P (trend) = 0.10 Rectal cancer:
Coffee:
>3 cups/day vs. G 1 cup/day
Coffee:
lower
VS.
Tea: higher
quartile 1
VS.
quartile 4
Coffee:
5 cups/day
Associations consistent across subgroups
Measure of tea consumption not clear
cancer in younger
Coffee intake measured at entry to study Significant inverse association with colon
Tea intake measured once, at entry to study Association with tea present in older men only
Coffee intake measured at entry to study
168
consumption was associated with a statistically significant reduction in the incidence of prostate cancer and it was not associated with colon cancer. In 1986, Jacobsen et al. [15] reported the results of continued follow-up of the Norwegian subjects first mentioned by Bjelke [3]. A total of 16,555 men and women who completed a questionnaire about their coffee consumption in 1967-1969 were followed until 1978. Smoking and dietary habits were obtained on a subset of 10,517 subjects. Deaths were identified by linking birth identification numbers with cancer registry and death data. There was no association of cancer deaths overall (886 deaths) with coffee consumption. Death from colon cancer (n = 100) was inversely associated with coffee consumption after adjustment for age and cigarette smoking: six deaths were observed in drinkers of 2 7 cups per day vs. 10.5 expected and 30 among drinkers of 4 2 cups per day vs. 25.8 expected; the trend was not significant (P = 0.10). For rectal cancer (64 deaths) there was no suggestion of a trend. Adjustment for alcohol consumption slightly strengthened the colon cancer-coffee association. The association was present among subjects younger than 65 at entry (P = 0.002 for trend) but not among older subjects. In fact, among the latter, there was a positive association of coffee with mortality, but it was based on very small numbers and was not statistically significant. Statistically significant inverse associations of coffee with kidney cancer and non-melanoma skin cancer were also noted. In 1986 Macquart-Moulin et al. [26] reported findings from a case-control study of colorectal cancer and diet conducted in Marseilles from 1979- 1984. Cases (399) were identified in 11 hospitals in Marseilles; controls matched on age and sex were subjects admitted for trauma. The participation rate was 100%. Food frequency questionnaires concerning usual diet in the year before the illness were administered. For selected food groups, including coffee, subjects were divided into quartiles of consumption and relative risks
were calculated with adjustment for age, sex, total calories and weight. Consumption of vegetables and oils was lower in cases than controls. Coffee was also consumed less by cases than by controls: relative to quartile 1 of coffee consumption, the relative risk estimates were 0.64, 0.68 and 0.55 for quartiles 2, 3 and 4, respectively. The trend was not statistically significant (P = 0.16). The results of a case-control study of diet and digestive tract cancers conducted in 1983 -1988 in greater Milan were reported by La Vecchia et al. in 1988 and 1989 121,223. There is still considerable heterogeneity in diet in this region because of migration from southern Italy to Milan. There were 750 cases (455 colon cancer and 295 rectal cancer) and 1944 controls who had been admitted for acute nonmalignant non-digestive tract disorders. The participation rate was 98%. Patients were asked about the frequency of consumption of 29 selected food items before the onset of illness. Relative risks were estimated for drinkers of 2 cups and > 3 cups of coffee per day relative to consumption of < 1 cup; these were approximate tertiles of consumption. Allowance was made for social class, education, marital status, smoking, alcohol consumption, age and sex. Coffee consumption was inversely related to the risks of both colon cancer (P = < 0.01 for trend) and rectal cancer (P < 0.05 for trend): for colon cancer the multivariate relative risk estimate for 2 3 cups per day relative to < 1 cup was 0.64; for rectal cancer the corresponding estimate was 0.66. The associations were generally consistent across subgroups and after allowance for other dietary items. Tea was reported on in an earlier publication based on 339 cases of colon cancer, 236 of rectal cancer and 778 controls [22]. Because tea was consumed in lesser -quantities than coffee, relative risk estimation was possible only for two levels of consumption rather than tertiles: for colon cancer, the relative risk estimate was 1.38 and it was not statistically significant; for rectal cancer the estimate was 1.54 and it was statistically significant.
169
In 1989 Rosenberg et al. [38] assessed coffee consumption In relation to the risk of large bowel cancer with data collected from 1978 to 1986 in a multipurpose hospital-based casecontrol study of several cancers and exporate of patients sures . The participation approached for an interview was 96%. The cases (717 colon cancer, 538 rectal cancer) were compared with 3883 control patients with non-gastrointestinal tract disorders. Relative risks were estimated with allowance for age, sex, geographic area, interview year, smoking, alcohol use, education, religion and race. Relative to consumption of one cup of coffee per day, the estimated relative risk of colon cancer for recent consumption of Z 5 cups daily was 0.6 (95% CI 0.4-0.8), but estimates for other categories of coffee consumption were close to 1.0. The inverse association with heavy coffee consumption was consistent across sex and was present regardless of whether the measure of coffee consumption was use in the month, year or 3 years before interview. For rectal cancer, the relative risk estimate was not reduced for drinkers of >, 5 cups daily (RR = 1.2, 95% CI 0.8- 1.8). In fact, estimates were elevated for some categories of consumption, particularly in men, but there was no trend. Conclusion
The validity of some of the studies of coffee or tea consumption and large bowel cancer cannot be assessed because insufficient details were given on the methods. In addition, interpretation of some of the results is problematic because the measure of consumption was not quantified or the distribution of cases and controls according to consumption was not presented. Conclusions on coffee will be based on six studies in which data on methods and consumption were judged to be sufficient for present purposes: the case-control studies of Macquart-Moulin et al. [26] of French subjects, La Vecchia et al. [21,22] of Italian subjects and Rosenberg et al. [38] of American subjects and the follow-up studies of Snowdon et al. [40]
and Phillips et al. [31] of Seventh-day Adventists, Nomura et al. [30] of Hawaiian Japanese subjects and Jacobsen et al. [15] of Norwegian subjects. Conclusions on tea will be based on two studies: the Italian case-control study of La Vecchia et al. [22] and the follow-up of Hawaiian Japanese by Heilbrun et al. [ 131. For coffee, the data of four studies [15,21,26,38], including all three case-control studies, suggest an inverse association between coffee consumption and the risk of colon cancer, rectal cancer, or both, but there was a statistically significant trend across levels of consumption in only one [21]. There was little or no association in one study, a follow-up [30] of Japanese in Hawaii; and there was a positive association in one study, a follow-up of Seventh-day Adventists [31,40]. Lowenfels [24] has suggested that an inverse association of coffee with risk might be evident only in populations which consume high fat, low fiber Western diets; if this is so, such an association would not be expected among subjects of Japanese descent. The authors of the study of Seventh-day Adventists suggested that coffee drinkers may not adhere to the precepts of the Adventist Church in ways other than using coffee, so that confounding could not be ruled out. All the case-control studies used hospital controls, but the inverse associations observed in all of them are probably not explained by that choice. The controls had diagnoses that appeared to be unrelated to coffee consumption and it seems unlikely that the prevalence of heavy coffee drinking would have been an overestimate. In fact, there is evidence that persons with chronic illnesses tend to reduce their coffee ingestion [37,39]. In addition, hospital-based studies of myocardial infarction which used hospital controls have indicated an increased risk of myocardial infarction in heavy drinkers [36]. Thus, use of hospital controls would seem more likely to produce a spurious positive association than an inverse one. None of the studies controlled adequately for fat, beef or fiber consumption. In some populations coffee has been positively
170
correlated with the intake of beef and fat [6,11,18,45]. If coffee is indeed associated with beef and fat consumption and if these are risk factors for colorectal cancer, failure to control them would tend to obscure an inverse association of coffee with risk. In considering the follow-up studies [15,30,31,40], it should be borne in mind that coffee consumption was measured a single time, at entry. Insofar as coffee drinking habits change over time, this might be expected to obscure an association, either positive or inverse, of coffee with risk. In conclusion, based on the studies to date, it appears unlikely that coffee increases the risk of large bowel cancer. Some data suggest that coffee reduces the risk, but the evidence is not compelling and a biologic mechanism has not been established. Studies are needed in which more complete histories of methylxanthine ingestion are obtained and confounding from other dietary factors is well controlled. For tea consumption, the evidence is even more sparse than for coffee. In two small studies, there was a positive relation of tea consumption to risk of rectal cancer [ 13,221. More data are needed. Acknowledgement
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46
Rose, G., Blackbum, H., Keys, A. et al. (1974) Colon cancer and blood-cholesterol. Lancet, 1, 181-183. Rosenberg, L., Palmer, J.R., Kelly, J.P. et al. (1988) Coffee drinking and nonfatal myocardtal infarction in men under 55 years of age. Am. J. Epidemiol., 128, 570578. Rosenberg, L., Slone, D., Shapiro, S. et al. (1981) Casecontrol studies on the acute effects of coffee upon the risk of myocardial infarction: problems in the selection of a hospital control series. Am. J. Epidemiol., 113, 646652. Rosenberg, L., Werler, M.M., Palmer, J.R. et al. (1989) The risks of cancers of the colon and rectum in relation to coffee consumption. Am. J. Epidemiol. in press. Silverman, D.T., Hoover, R.N., Swanson, M. et al. (1983) The prevalence of coffee drinking among hospitalized and population-based control groups. J. Am. Med. Assoc., 249,1877- 1880. Snowdon, D.A. and Phillips, R.L. (1984) Coffee consumption and risk of fatal cancers. Am. J. Public Health, 74,820-823. Stich, H.F., Rosin, M.P., Wu, C.H. et al. (1981) A comparative genotoxicity study of chlorogenic acid (3-Ocoffeoylquinic acid). Mutat Res., 90,201-212. Sugtmura, T. and Sato, S. (1983) Mutagens-carcinogens in foods. Cancer Res., 43,2415s-2421s. Thelle, D.S., Amesen, E. and Forde, O.H. (1983) The Tromso Heart Study: does coffee raise serum cholesterol? N. Engl. J. Med., 308, 1454-1457. Whittemore, A.S., Paffenbarger, R.S., Jr., Anderson, K. et al. (1983) Early precursors of pancreatic cancer in college men. J. Chron. Dts., 36,251-256. Williams, P.T., Wood, P.D., Vrantzan, K.M. et al. (1985) Coffee intake and elevated cholesterol and apolipoprotein B levels in men. J. Am. Med. Assoc., 253,1407-1411. Wynder, E.L.. Hall, N.E. and Polansky, M. (1983) Epidemiology of coffee and pancreatic cancer. Cancer Res., 43, 3900-3906.
Cancer Letters, 52 (1990) 163-171 Elsevier Scientific Publishers Ireland Ltd.
Review Letter
Coffee and tea consumption in relation to the risk of large bowel cancer: a review of epidemiologic studies L
. Rosenberg
Slone Epidemiology
Unit, School of Public Health,
Boston
UnioersitySchool
of Medicine,
1371 Beacon Street, Brook-
line, MA 02146 (U.S.A.) (Received Jan 17 1990) (Revison received 7 May 1990) (Accepted 9 May 1990)
Summary Most of the few epidemiologic investigations of the relation of methylxanthine ingestion to risk of large bowel cancer haue concerned coffee consumption. A slightly increased risk in coffee drinkers was suggested by one study, no association by another and an inuerse association by four, but there was a statistically significant trend across levels of consumpfion in only one of the latter studies. Based on the data on hand, there is little reason for concern that coffee consumption increases the risk. Although some euidence suggests an inverse association, the data are not compelling and a biologic mechanism is not established. There is euen less information on tea consumption and the relation of consumption of this beuerage to risk of large bowel cancer is unknown. ‘Keywords:
coffee;
methylxanthines;
colonic neoplasms; rectal neoplasms; tea.
Introduction Coffee, a major sauce of dietary methylxanthines, contains mutagens and can inhibit DNA
repair [20,41,41]. Coffee consumption has been linked to increases in the risk of bladder cancer [5] and pancreatic cancer [25], but the relationship with bladder cancer, if real, is weak [12,29] and the association with pancreatic cancer observed in a hypothisesraising study has not been confirmed [44,46]. It has been proposed that coffee consumption may lead to a reduction in the risk of large bowel cancer, based on the following reasoning [4,16,24]. Cholesterol, bile acids and their metabolites, particularly secondary bile acids, are promoters of colon carcinogens in animals [33]. Fecal concentrations of bile acids and metabolites are greater in patients who have colorectal cancer, or who are at high risk because of predisposing conditions such as adematous polyps, than in comparison patients [14,23], and they are also greater in healthy persons from populations with high colon cancer risk as compared with persons from low risk populations [32,43]. Lower serum cholesterol levels may indicate increased cholesterol excretion in some persons who consume high fat diets [24] (and if this is so, it could explain the inverse association of colon cancer with serum cholesterol
0304-3835/90/$03.50 0 1990 Elsevier Scientific Publishers Ireland Ltd Published and Printed in Ireland
164
observed in some studies [35]). Coffee has been linked to increased serum cholesterol levels, particularly in populations with high fat diets [6,8,11,18,19,43,54]. If the mechansim leading to higher cholesterol levels involves a reduction in the excretion of bile acids, neutral setrols, or both [4,16,24], coffee consumption might reduce the risk of colon cancer. While the proposed mechanism appears reasonable, it is speculative: the possibility that preclinical large bowel cancer reduces cholesterol levels [27] has not been excluded as an explanation for an inverse association of serum cholesterol with colon cancer [35] and direct evidence on the effect of coffee consumption on bile acid excretion from the liver is lacking [2]. Most epidemiologic studies of diet and large bowel cancer have assessed coffee only peripherally, but several recent studies have assessed coffee use in detail. Tea, the other major source of dietary metylxanthine, has received less attention and there are no informative data on colas. All studies of large bowel cancer in which coffee or tea are mentioned are considerd beow, in chronological order and relevant details of the studies are also given in Table 1. Epidemiologic studies In 1973, Haenszel et al. [lo] reported on a hospital-based case-control study of men and women of Japanese descent in Hawaii, conducted from 1966-1970. A total of 179 patients with large bowel cancer were compared with 357 age- and sex-matched controls with non-digestive tract illnesses. The frequency of consumption of a large variety of foods was determined by interview. Relative risk for “above-average” and “below-average” frequencies of use were presented for each food and beverage. Consumption of Westernstyle food - in particular, beef, legumes, and starches - was associated with increased risk. Unexpectedly, there was inverse association with coffee consumption. The relative risk was given as 0.72, but confidence intervals and the distribution of cases and controls according to coffee consumption were not presented.
Bjelke’s doctoral work on large bowel cancer [3] has been cited as evidence of an inverse association with coffee. The validity of the results is difficult to assess, however, because details of the methods have not been published in a peer-reviewed journal. In a letter to the editor in 1974 [4], Bjelke described a case-control study of Norwegian men in which 162 cases were compared with 444 controls: relative to consumption of < 3 cups of coffee per day, the relative risk estimate was 0.6 for consumption of 2 5 cups per day. Bjelke also described preliminary results of a follow-up of 12,166 Norwegian men, which suggested a lower risk of colon cancer in those who drank Z 5 cups of coffee per day relative to those who drank < 3 cups per day. Subsequent results after longer follow-up, reported by Jacobsen et al. [ 151, are described below. In 1978 Graham et al. [9] published results from a case-control study conducted from 1959 to 1965 in a cancer hospital in Buffalo. The cases, 256 white males with colon cancer and 330 with rectal cancer, were compared with white male control patients with nonmalignant non-gastrointestinal illnesses, selected from a total pool of 1222 controls: 783 controls were frequency-matched on age to the colon cancer cases and 628 to the rectal cancer cases. The frequency of ingestion of selected specific foods was ascertained by interview. The main finding was an inverse association of large bowel cancer risk with frequent ingestion of vegetables. A “significant but small” increase (not specified) in risk of colon cancer was reported for “frequent” drinking of coffee, but there was no association with rectal cancer; the data on coffee were not given. In 1979, Dales et al. [7] reported on a study of 99 black cases of colorectal cancer and 280 black controls matched on sex, age and hospital. The participation rate was 40% for cases and 50% for controls. Information was obtained by interview on the frequency of consumption 3 years previously of 89 food items. Large bowel cancer was associated positively with consumption of foods with a high saturated fat content and inversely with foods
165
with a high fiber content. There was “virtually no relationship” with coffee and “a small, statistically non-significant positive association” with tea; no data were given. In 1981, Abu-Zeid et al. [l] published an abstract on a case-control study of colorectal cancer conducted in two hospitals in Winnipeg. Each of 197 cases of large bowel cancer was matched for age, sex, race, residence and hospital with a control. Dietary histories were obtained by interview and multivariate analyses were conducted. “A low risk was associated with.. drinking coffee” but the data were not presented. In 1983, Miller et al. [28] presented results on coffee based on data from a case-control study of large bowel cancer conducted in Toronto and Calgary from 1976 to 1978; an earlier report did not include an assessment of coffee [17]. The cases (348 colon cancer and 194 rectal cancer) were compared with 542 age- and sex-matched neighbor controls and 535 hospital controls who had had abdominal surgery. The participation rates of cases and hospital controls were 80% and 81%) respectively; the participation rate of neighbor controls was lower, but it was not specified. In home interviews, information on consumption 6 months previously of 150 fcod items was collected with the aid of food models. Relative risks were presented for the second and third tertiles of consumption relative to the lowest tertile. “Beverages,” which included “tea, coffee, cola, etc.” were not associated with either colon or rectal cancer and no trend was apparent across tertiles. Data were not given on coffee and tea separately. In 1984 and 1985, Snowdon et al. [40] and Phillips et al. [31] reported on a 21-year follow-up study of Seventh-day Adventists. Baseline data on consumption of 21 foods and beverages had been obtained at entry by selfadministered questionnaire from 25,493 white subjects [31]. Deaths were ascertained through use of California death certificates, a method that identified an estimated 85% of the total deaths. Among men, there was a statistically significant increase in the relative risk estimate of colon cancer with increasing
consumption of coffee, based on 33 cases who consumed < 1 cup per day, five who consumed 1 cup per day and 15 who consumed 2 2 cups per day; the relative risk estimate for drinkers of Z 2 cups per day was 2.0 (95% confidence interval (CI) 1.1-3.6). A weaker trend in women, based on a total of 83 cases, was not statistically significant. There were only 28 cases of rectal cancer on whom data on coffee use were available and there was no evidence of a significant trend. The association with colon cancer in both men and women was confined to the last 11 years of follow-up; when this period was considered, trends were significant in both men and women. There was “no significant relationship” with tea or soft drinks [31]. The results of a follow-up study of 7355 Japanese men in Hawaii from 1965 to 1968 until 1983 were reported by Nomura et al. in 1986 [30]. The men gave 24-h dietary recalls at entry. Coffee consumption was not significantly related to the incidence of large bowel cancer. For colon cancer (108 cases), the ageadjusted incidence was similar at all levels of coffee consumption (17.3 per 1000 for >/ 5 cups per day versus 13.5 per 1000 for 0 cups per day). For rectal cancer (60 cases), there was a trend of decreasing incidence across increasing levels of consumption, but it was not statistically significant (P = 0.134). A report by Heilbrun et al. on tea consumption in the same Hawaiian Japanese cohort was published in 1986 [ 131. Tea consumption had been recorded at entry. During follow-up until 1985, 152 cases of colon cancer and 76 of rectal cancer were identified. Relative risk estimates were derived from proportional hazards regression models with adjustment for age. For rectal cancer, allowance was also made for alcohol intake and, in some analyses, for saturated fat intake. For rectal cancer, the relative risk increased across levels of consumption (P = 0.0007): for men who consumed tea at least once per day relative to those who almost never drank it, the estimate was 4.2, based on five exposed cases. The association was present in men who were aged 58 or older and absent in younger men. Tea
et al. [9]
1985
Snowdon et al. [4O] 1984 Phillips et al. (311
Abu-Zeid et al. [ 1] 1981 Miller et al. 1281 1983
Dales et al. [ 171 1979
Graham 1978
1967-1968
Bjelke [4] 1974
Hospital-based case-control Case-control
Follow-up
?
1976-1978
1960-1980
1960-1981
Hospital-based case-control
Hospital-based case-control
Follow-up
Hospital-based case-control
Hospital-based case-control
1976
1973-
1959-1965
?
1970
1966-
Type of study
studies of large bowel cancer
Haenszel et al. [lo] 1973
Epidemiologic
Years of study
1.
Author/ Year of publication
fable
men
deaths
Males - 56 colon cancer deaths; females - 91 colon cancer deaths 35 rectal cancer
U.S. 7th-Day Adventists Ca 25,000 followed
Rectal cancer: >1 cup/day vs. < 1 cup/day
< 1 cup/day
Coffee: Colon cancer: 22 cups/day vs.
Beverages (“tea, coffee, cola, etc.“) highest tertile vs. lowest
Canadians 348 colon cancer 194 rectal cancer 542 neighbor controls 535 hospital controls
Coffee: any
Females RR = 1.5 P(trend) = 0.20 Rectal cancer: RR = 1.4 P&end) = 0.38
Colon cancer: males RR = 2.0 P (trend) = 0.04
non-signlftcant positive association” “A low risk” for coffee drinkers Colon cancer: malesRR = 0.9 female RR = 1.1 Rectal cancer: malesRR = 1.1 QmalesRR = 0.8
“Small, statistically
Tea: any
Coffee: “frequent drinking”
Coffee: any
-
RR = 0.6 Cl not given
Colon cancer: “Significant but small excess risk” Rectal cancer: No association “No relationship”
vs. “below average” Coffee: 35 cups/day vs. < 3 cups/day -
not given
Results given from 1311 Coffee consumption related to increased risk in second half of follow-up but not first Coffee was proscribed by church; association may be confounded by other “lifestyle” factors
Data on coffee consumption not given Data not given separately on tea, coffee and colas
Low participation rate Data on coffee and tea consumption not given
Details of methods not given Longer follow-up reported in Jacobsen [ 151 Data on coffee consumption not given
Details of methods
Data on coffee consumption not given
Coffee: “above-average” RR = 0.72 Cl not given
Comments
Exposure
Canadian
U.S. Blacks 99 cases 280 controls
U.S. men 156 colon cancer 330 rectal cancer 1222 control
Norwegian
Norwegians 162 cases 444 controls
Hawaiian Japanese 179 cases 357 controls
Study population
in relation to coffee or tea consumption. z
1967-
Jacobsen 1986
from incidence
‘Calculated
rates
1986
1978-
et al. [38]
Hospital-based case-control
Hosptial-based case-control
Rosenberg 1987
1988
et al. [22]
LaVecchia 1989
1983-
Hospital-based case-control
1987
1983-
et al. [21]
Hospital-based
LaVecchia 1988
1979-1986 case-control
et al.
Follow-up
Follow-up
Follow-up
1986
P61
Macquart-Moulin
1978
1985
1965-
Heilbrun et al. [13] 1986
et al. [15]
1983
1965-
et al. 1301
Nomura 1986
men
men
U.S. 717 colon cancer 538 rectal cancer 3833 controls
Italians 455 colon cancer 295 rectal cancer 1944 controls
Italians 339 colon cancer 236 rectal cancer 778 controls
399 cases 399 controls
French
Norwegians 100 colon cancer deaths 64 rectal cancer deaths
Japanese Hawaiian 7355 followed 108 colon cancer 60 rectal cancer Japanese Hawaiian 7833 followed 152 colon cancer 76 rectal cancer
VS.
2 cups/day
= 0.16
Colon cancer:
RR = 0.6 95% Cl 0.4-0.8 no trend Rectal cancer: RR = 1.2 95% ClO.8-1.8 no trend 25 cups/day vs. 1 cup/day
Colon cancer: RR = 1.38 P> 0.05 Rectal cancer: RR = < 1.54 P< 0.05 Colon cancer: RR = 0.64 P (trend) < 0.01 Rectal cancer: RR =0.66 P (trend) < 0.05
P (trend)
RR = 1.07 P(trend) = 0.94 RR = 0.55
RR = 1.28’ P(trend) = 0.98 RR = 0.55’ P (trend) = 0.13 Rectal cancer: RR = 4.2 P(trend) = 0.0007 Colon cancer: no association P(trend) = 0.25 Colon cancer: RR = 0.59 P (trend) = 0.10 Rectal cancer:
Coffee:
>3 cups/day vs. G 1 cup/day
Coffee:
lower
VS.
Tea: higher
quartile 1
VS.
quartile 4
Coffee:
5 cups/day
Associations consistent across subgroups
Measure of tea consumption not clear
cancer in younger
Coffee intake measured at entry to study Significant inverse association with colon
Tea intake measured once, at entry to study Association with tea present in older men only
Coffee intake measured at entry to study
168
consumption was associated with a statistically significant reduction in the incidence of prostate cancer and it was not associated with colon cancer. In 1986, Jacobsen et al. [15] reported the results of continued follow-up of the Norwegian subjects first mentioned by Bjelke [3]. A total of 16,555 men and women who completed a questionnaire about their coffee consumption in 1967-1969 were followed until 1978. Smoking and dietary habits were obtained on a subset of 10,517 subjects. Deaths were identified by linking birth identification numbers with cancer registry and death data. There was no association of cancer deaths overall (886 deaths) with coffee consumption. Death from colon cancer (n = 100) was inversely associated with coffee consumption after adjustment for age and cigarette smoking: six deaths were observed in drinkers of 2 7 cups per day vs. 10.5 expected and 30 among drinkers of 4 2 cups per day vs. 25.8 expected; the trend was not significant (P = 0.10). For rectal cancer (64 deaths) there was no suggestion of a trend. Adjustment for alcohol consumption slightly strengthened the colon cancer-coffee association. The association was present among subjects younger than 65 at entry (P = 0.002 for trend) but not among older subjects. In fact, among the latter, there was a positive association of coffee with mortality, but it was based on very small numbers and was not statistically significant. Statistically significant inverse associations of coffee with kidney cancer and non-melanoma skin cancer were also noted. In 1986 Macquart-Moulin et al. [26] reported findings from a case-control study of colorectal cancer and diet conducted in Marseilles from 1979- 1984. Cases (399) were identified in 11 hospitals in Marseilles; controls matched on age and sex were subjects admitted for trauma. The participation rate was 100%. Food frequency questionnaires concerning usual diet in the year before the illness were administered. For selected food groups, including coffee, subjects were divided into quartiles of consumption and relative risks
were calculated with adjustment for age, sex, total calories and weight. Consumption of vegetables and oils was lower in cases than controls. Coffee was also consumed less by cases than by controls: relative to quartile 1 of coffee consumption, the relative risk estimates were 0.64, 0.68 and 0.55 for quartiles 2, 3 and 4, respectively. The trend was not statistically significant (P = 0.16). The results of a case-control study of diet and digestive tract cancers conducted in 1983 -1988 in greater Milan were reported by La Vecchia et al. in 1988 and 1989 121,223. There is still considerable heterogeneity in diet in this region because of migration from southern Italy to Milan. There were 750 cases (455 colon cancer and 295 rectal cancer) and 1944 controls who had been admitted for acute nonmalignant non-digestive tract disorders. The participation rate was 98%. Patients were asked about the frequency of consumption of 29 selected food items before the onset of illness. Relative risks were estimated for drinkers of 2 cups and > 3 cups of coffee per day relative to consumption of < 1 cup; these were approximate tertiles of consumption. Allowance was made for social class, education, marital status, smoking, alcohol consumption, age and sex. Coffee consumption was inversely related to the risks of both colon cancer (P = < 0.01 for trend) and rectal cancer (P < 0.05 for trend): for colon cancer the multivariate relative risk estimate for 2 3 cups per day relative to < 1 cup was 0.64; for rectal cancer the corresponding estimate was 0.66. The associations were generally consistent across subgroups and after allowance for other dietary items. Tea was reported on in an earlier publication based on 339 cases of colon cancer, 236 of rectal cancer and 778 controls [22]. Because tea was consumed in lesser -quantities than coffee, relative risk estimation was possible only for two levels of consumption rather than tertiles: for colon cancer, the relative risk estimate was 1.38 and it was not statistically significant; for rectal cancer the estimate was 1.54 and it was statistically significant.
169
In 1989 Rosenberg et al. [38] assessed coffee consumption In relation to the risk of large bowel cancer with data collected from 1978 to 1986 in a multipurpose hospital-based casecontrol study of several cancers and exporate of patients sures . The participation approached for an interview was 96%. The cases (717 colon cancer, 538 rectal cancer) were compared with 3883 control patients with non-gastrointestinal tract disorders. Relative risks were estimated with allowance for age, sex, geographic area, interview year, smoking, alcohol use, education, religion and race. Relative to consumption of one cup of coffee per day, the estimated relative risk of colon cancer for recent consumption of Z 5 cups daily was 0.6 (95% CI 0.4-0.8), but estimates for other categories of coffee consumption were close to 1.0. The inverse association with heavy coffee consumption was consistent across sex and was present regardless of whether the measure of coffee consumption was use in the month, year or 3 years before interview. For rectal cancer, the relative risk estimate was not reduced for drinkers of >, 5 cups daily (RR = 1.2, 95% CI 0.8- 1.8). In fact, estimates were elevated for some categories of consumption, particularly in men, but there was no trend. Conclusion
The validity of some of the studies of coffee or tea consumption and large bowel cancer cannot be assessed because insufficient details were given on the methods. In addition, interpretation of some of the results is problematic because the measure of consumption was not quantified or the distribution of cases and controls according to consumption was not presented. Conclusions on coffee will be based on six studies in which data on methods and consumption were judged to be sufficient for present purposes: the case-control studies of Macquart-Moulin et al. [26] of French subjects, La Vecchia et al. [21,22] of Italian subjects and Rosenberg et al. [38] of American subjects and the follow-up studies of Snowdon et al. [40]
and Phillips et al. [31] of Seventh-day Adventists, Nomura et al. [30] of Hawaiian Japanese subjects and Jacobsen et al. [15] of Norwegian subjects. Conclusions on tea will be based on two studies: the Italian case-control study of La Vecchia et al. [22] and the follow-up of Hawaiian Japanese by Heilbrun et al. [ 131. For coffee, the data of four studies [15,21,26,38], including all three case-control studies, suggest an inverse association between coffee consumption and the risk of colon cancer, rectal cancer, or both, but there was a statistically significant trend across levels of consumption in only one [21]. There was little or no association in one study, a follow-up [30] of Japanese in Hawaii; and there was a positive association in one study, a follow-up of Seventh-day Adventists [31,40]. Lowenfels [24] has suggested that an inverse association of coffee with risk might be evident only in populations which consume high fat, low fiber Western diets; if this is so, such an association would not be expected among subjects of Japanese descent. The authors of the study of Seventh-day Adventists suggested that coffee drinkers may not adhere to the precepts of the Adventist Church in ways other than using coffee, so that confounding could not be ruled out. All the case-control studies used hospital controls, but the inverse associations observed in all of them are probably not explained by that choice. The controls had diagnoses that appeared to be unrelated to coffee consumption and it seems unlikely that the prevalence of heavy coffee drinking would have been an overestimate. In fact, there is evidence that persons with chronic illnesses tend to reduce their coffee ingestion [37,39]. In addition, hospital-based studies of myocardial infarction which used hospital controls have indicated an increased risk of myocardial infarction in heavy drinkers [36]. Thus, use of hospital controls would seem more likely to produce a spurious positive association than an inverse one. None of the studies controlled adequately for fat, beef or fiber consumption. In some populations coffee has been positively
170
correlated with the intake of beef and fat [6,11,18,45]. If coffee is indeed associated with beef and fat consumption and if these are risk factors for colorectal cancer, failure to control them would tend to obscure an inverse association of coffee with risk. In considering the follow-up studies [15,30,31,40], it should be borne in mind that coffee consumption was measured a single time, at entry. Insofar as coffee drinking habits change over time, this might be expected to obscure an association, either positive or inverse, of coffee with risk. In conclusion, based on the studies to date, it appears unlikely that coffee increases the risk of large bowel cancer. Some data suggest that coffee reduces the risk, but the evidence is not compelling and a biologic mechanism has not been established. Studies are needed in which more complete histories of methylxanthine ingestion are obtained and confounding from other dietary factors is well controlled. For tea consumption, the evidence is even more sparse than for coffee. In two small studies, there was a positive relation of tea consumption to risk of rectal cancer [ 13,221. More data are needed. Acknowledgement
This review was supported by the International Life Sciences Institute, Washington, DC. References Abu-Zeid, H.A., Choi, N.W. and Hsu, P.H. (1981) Factors associated with risk of cancer of the colon and rectum (abstract). Am. J. Epidemiol., 114,442. Amesen, E., Huseby, N.E., Brenn, T. et al. (1986) The Tromso heart study: distribution of and determinants for, gamma-glumylfransferose in a free-living population. Stand. J. Clin. Lab. Invest., 46,63-70. Bjelke, E. (1973) Epidemiologic studies of cancer of the stomach, colon and rectum; with special emphasis on the role of diet. Ph.D. Thesis. University of Minnesota Ann Arbor, MI. BjeIke, E. (1974) Colon cancer and blood cholesterol (letter). Lancet, 1, 1116-1117. Cole, P. (1971) Coffee-drinking and cancer of the lower urinary tract. Lancet, 1,1335-1337.
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35 36
37
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41
42 43
44
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