Exploring the Relation of Alcohol Consumption to Risk of Breast Cancer
R. Curtis Ellison,
Yuqing Zhang,
Christine E. McLennan and
Kenneth J. Rothman
From the Section of Preventive Medicine and Epidemiology, Evans Department of Medicine, Boston University School of Medicine, Boston, MA.
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ABSTRACT
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There are lingering questions regarding the relation between alcohol consumption and breast cancer risk in women. The authors performed a meta-analysis of epidemiologic studies carried out through 1999 to examine the dose-response relation and to assess whether effect estimates differed according to various study characteristics. Overall, there was a monotonic increase in the relative risk of breast cancer with alcohol consumption, but the magnitude of the effect was small; in comparison with nondrinkers, women averaging 12 g/day of alcohol consumption (approximately one typical drink) had a relative risk of 1.10 (95% confidence interval (CI): 1.06, 1.14). Estimates of relative risk were 7% greater in hospital-based case-control studies than in cohort studies or community-based case-control studies, 3% greater in studies published before 1990 than in studies published later, and 5% greater in studies conducted outside of the United States than in US studies. The findings of five US cohort studies published since 1990 yielded a relative risk of 1.06 (95% CI: 1.00, 1.11) for consumers of 12 g/day, as compared with nondrinkers. Cohort studies with less than 10 years of follow-up gave estimates 11% higher than cohort studies with longer follow-up periods. No meaningful difference was seen by menopausal status or type of beverage consumed.
alcohol drinking; breast neoplasms; meta-analysis
Abbreviations:
CI, confidence interval
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INTRODUCTION
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Most studies that have examined the relation between alcohol consumption and breast cancer risk have shown some increase in risk with heavier drinking (1

4
), and many have suggested that there may be some increase in risk with only light drinking (e.g., at an average intake of one drink per day) (5










17
). A 1994 meta-analysis by Longnecker (18
) showed a linear increase in risk, with an estimate of an approximate 10 percent increase for each 10-g/day increment in alcohol consumption. Since 1994, however, there have been more than 20 studies on the subject, with some showing no increased risk associated with light to moderate drinking. Among these are the EURAMIC Study from Europe (19
) and new results from the Framingham Study (20
). Furthermore, among studies reporting beverage-specific effects, some have shown an inverse relation between wine drinking and breast cancer risk (21
23
). This finding would be consistent with several new laboratory studies indicating that resveratrol and other substances in red wine may reduce the risk of breast cancer (24


28
).
Here we present results of a meta-analysis of the epidemiologic studies conducted through 1999. This new meta-analysis was prompted by the following questions: 1) Is there a monotonic increase in the risk of breast cancer associated with alcohol consumption? 2) Specifically, what is the effect on risk of breast cancer associated with consuming alcohol at a level of one drink per day (considered "moderate" by US Department of Agriculture guidelines (29
))? 3) Do results differ between case-control studies and cohort studies? 4) Are there differences between more recent studies and studies conducted earlier? 5) Do results differ between studies carried out in the United States and those carried out in other countries (where women may consume larger amounts of alcohol and drink more frequently)? 6) How does the duration of follow-up in cohort studies affect results? 7) Does alcohol consumption relate differently to the risks for premenopausal and postmenopausal breast cancer? 8) Are there differences according to the type of alcoholic beverage consumed?
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MATERIALS AND METHODS
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Selection of studies
By searching MEDLINE (US National Library of Medicine), we identified studies published between January 1966 and October 1999. We supplemented these with additional studies cited as references in previous meta-analyses, pooled analyses, and reviews. To be included in our meta-analysis, a published study had to 1) be an original article or other report on a cohort or case-control study, 2) report alcohol intake data that could be quantified as grams of alcohol per day, 3) present data on incident cases of breast cancer (rather than prevalent cases) or mortality from breast cancer, and 4) report point estimates and an estimate of variability for the primary outcome. We excluded studies if they 1) reported only prevalent cases, 2) included only nonquantifiable alcohol intake data, 3) were based on data from another publication that was included in the meta-analysis, 4) were from reports published only as letters to the editor or abstracts, or 5) had implausible outcomes (a criterion used for only one study (30
) that was similarly excluded by Longnecker (18
) as having implausible outcomes).
Of a total of 74 publications considered, we excluded 30. The present meta-analysis of breast cancer incidence was based on 42 reports providing data on 41,477 incident cases of breast cancer. These reports consisted of all of the studies listed in table 1 except for two studies on breast cancer mortality (49
, 50
), which provided data on 3,283 cases for a separate analysis. Table 2 shows characteristics of reports that we considered but excluded and indicates the reasons for exclusion. Studies that did not provide quantifiable alcohol consumption data are listed as having "insufficient data." For several studies in which the data included in the meta-analysis were obtained from another publication, exclusions are noted as "data included in separate report."
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TABLE 2. Studies excluded from a meta-analysis of alcohol consumption and breast cancer incidence or mortality and reasons for exclusion
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Data extraction and unification
The quality of exposure information varied greatly among the reports. In most of the cohort studies and some of the case-control studies, investigators used self-reported food frequency questionnaires for estimation of alcohol consumption, while in other studies they used specific questionnaires or interviews. Fifteen studies reported some beverage-specific alcohol data; 13 of these had data on all three types of alcoholic beverages (beer, wine, and spirits). In the remaining studies, only total alcohol consumption was reported. Information on established risk factors for breast cancer varied among the studies. Of the 13 cohort studies included in the meta-analysis on incidence, nine were from the United States and four were from other countries. Ten of the case-control studies were from the United States, while the remaining 19 were from other countries.
Statistical analysis
For all studies, the level of alcohol consumption used in the meta-analysis was based on the categories reported in the original paper. Most studies used the reported consumption of the women over a prolonged period of time prior to the diagnosis of breast cancer. For each study, we took the age range of the population and the ranges of all categories of alcohol consumption reported and then calculated a median consumption value for each category. To do this, we obtained data from the 1988 alcohol supplement of the National Health Interview Survey (31
) for women of the same age, created similar consumption categories for women reporting current alcohol consumption, and took the median value.
In the analyses, we first examined the shape of the dose-response relation between alcohol consumption and risk of breast cancer. The dose-specific confounder-adjusted logarithms of the relative risks from all studies were pooled, and we fitted a curve using weighted quadratic spline regression (32
), with no intercept term. The weights were the inverse of the covariance-adjusted variance of the logarithms of the relative risks. Since the results from the spline regression analysis showed that there was a monotonic increase in relative risk of breast cancer with increasing alcohol consumption, in the later analyses, we applied the linear regression model to assess the heterogeneity of estimates of alcohol effect according to various characteristics of the studies. These characteristics included type of study (cohort study, community-based case-control study, hospital-based case-control study), number of years of follow-up for cohort studies (<10 years,
10 years), date of publication (before 1990, 1990 or later), location of the study (United States, outside the United States), and menopausal status of the subjects when their breast cancer was diagnosed (premenopausal, postmenopausal). In the linear regression model, we created an interaction term (an indicator term for the study characteristic x dose of alcohol) to assess quantitatively whether these characteristics modified the estimated alcohol effect (33
). The beta coefficient for each interaction term represents the ratio of log relative risks, i.e., the magnitude of difference in estimated alcohol effects according to characteristics of the study. We also applied the same approaches to examine the effects of different types of alcoholic beverages on the risk of breast cancer. In these analyses, consumers of each specific beverage were compared with nondrinkers of that specific beverage, adjusting for other alcoholic beverages consumed and study characteristics.
When we examined the association between total alcohol consumption and breast cancer risk, we obtained adjusted relative risks and the ratio of relative risks in increments of 12 grams of alcohol (ethanol) per day. For beverage-specific analyses, we used an increment of "one drink per day," rather than 12 grams of alcohol per day, since any differences would presumably be due to substances other than alcohol in the different beverages. For breast cancer mortality, results suggested a J-shaped relation between alcohol consumption and breast cancer deaths, so we did not evaluate the association as a linear relation.
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RESULTS
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The dose-response relation between total alcohol consumption and risk of breast cancer, assessed using a spline regression model, is shown in figure 1. There appeared to be a monotonic increase in breast cancer relative risk with increasing alcohol consumption. In comparison with nondrinkers, subjects consuming an average of 6 g of alcohol per day (approximately one half of a typical "drink") had a 4.9 percent increased risk (95 percent confidence interval (CI): 1.03, 1.07), and those consuming 12 g/day (approximately one drink) and 24 g/day (approximately two drinks) had 10 percent (95 percent CI: 1.06, 1.14) and 21 percent (95 percent CI: 1.13, 1.30) increased risks, respectively.

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FIGURE 1. Relative risk of breast cancer by alcohol consumption. Based on all studies of incidence listed in table 1, with no adjustments. The dose-response curve line represents estimates from a smoothed spline regression, with the lower line representing no effect. The y-axis presents relative risks on a log scale.
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Table 3 presents associations between alcohol consumption and breast cancer risk according to different study characteristics. Estimates of alcohol effect obtained from hospital-based case-control studies were slightly higher, on average, than those from cohort studies (overall relative risk ratio = 1.07, 95 percent CI: 1.00, 1.14). The alcohol-breast cancer relation assessed from community-based case-control studies was similar to that from cohort studies. Our analysis also indicated that, overall, studies published before 1990 showed slightly larger relative risks than studies published later (overall relative risk ratio = 1.03, 95 percent CI: 0.99, 1.08), and studies published outside of the United States yielded slightly higher estimates than US studies (overall relative risk ratio = 1.05, 95 percent CI: 0.99, 1.12).
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TABLE 3. Relation of alcohol consumption to breast cancer in a meta-analysis of studies conducted through 1999, according to study characteristics
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In analyses limited to recent cohort studies conducted in the United States, there was still a slight increase in risk of breast cancer with alcohol consumption. For the five US cohort studies on breast cancer incidence carried out since 1990 (3
, 4
, 20
, 63
, 67
), with a total of 2,190 cases, the relative risk for consumers of 12 g of alcohol per day (versus nondrinkers) was 1.06 (95 percent CI: 1.00, 1.11).
Also shown in table 3 is the relation of duration of follow-up in cohort studies to reported risk of breast cancer. In cohort studies with 10 or more years of follow-up, the relative risk of breast cancer for women consuming 12 g of alcohol per day was only 4 percent higher than it was for nondrinkers. When we compared cohort studies according to duration of follow-up, the risk from the eight studies with less than 10 years of follow-up was 11 percent higher (95 percent CI: 1.06, 1.16) than that from the five studies with 10 or more years of follow-up.
In 10 studies, data were available on both the premenopausal and postmenopausal occurrence of breast cancer. As table 3 indicates, the results suggested that the relative risks of breast cancer associated with alcohol consumption were similar for premenopausal and postmenopausal women, with the adjusted estimate for premenopausal women being only 2 percent higher than that for postmenopausal women.
Table 4 shows the relation of alcohol consumption to breast cancer risk according to the type of alcoholic beverage consumed. These results are based on 13 studies that reported relative risks separately for each of the three types of alcoholic beverages: beer, wine, and spirits. Results are given as the relative risk for women averaging one drink per day (equivalent to 12 g of alcohol) in comparison with subjects consuming none of that beverage; for the ratio of relative risks, we used wine consumers as the referent group. Because of limited data on higher consumption levels, the estimates of effect could only be compared for 14 or fewer drinks per week of each beverage.
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TABLE 4. Relation of alcohol consumption to breast cancer in a meta-analysis, according to type of alcoholic beverage consumed*
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As table 4 shows, there were few differences between intake and breast cancer risk for the different beverages. In comparison with wine, the relative risk for beer was 0.96 (95 percent CI: 0.91, 1.02); the relative risk associated with spirits, in comparison with wine, was 1.01 (95 percent CI: 0.93, 1.09). Thus, these analyses did not support the hypothesis that nonalcoholic components of wine modify the alcohol-breast cancer relation.
Data on breast cancer mortality related to alcohol consumption were available from two cohort studies (49
, 50
) with a total of 3,283 deaths from breast cancer. A separate meta-analysis using a spline regression model suggested a J-shaped relation between alcohol consumption and breast cancer mortality. The estimated relative risk of breast cancer mortality was slightly below 1.0 for up to 6 g/day, and it increased above 1.0 thereafter. Relative risks at 6, 12, and 24 g/day were 0.98, 1.15, and 1.16, respectively.
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DISCUSSION
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Our analyses confirmed that, overall, most studies demonstrate a monotonic increase in the risk of breast cancer with increasing consumption of alcoholic beverages. Our estimate that an average of one drink per day is associated with a 10 percent increase in breast cancer risk is very similar to that reported by Longnecker (18
). However, we found that the relation of alcohol to breast cancer risk varies by type of study. Hospital-based case-control studies, on average, show stronger associations than cohort studies, while community-based case-control studies suggest relative risks similar to those of cohort studies. One explanation for these findings is that moderate alcohol consumers may be less likely to be hospitalized, because of a protective effect of moderate alcohol consumption against cardiovascular diseases (34

37
), diabetes (38
, 39
), osteoporosis (40
), gallbladder disease (41
), and other conditions. Such an effect would not play a role when controls were chosen from the community, which is consistent with our finding of little difference between results obtained from community-based case-control studies and cohort studies.
Our analyses also suggested that effect estimates for breast cancer risk according to alcohol consumption are slightly greater for results of studies published before 1990 than for those published since then. This trend could be due to publication bias, in that more strongly "positive" study findings may have been more likely to be accepted for publication in the earlier years. With increasing interest in the topic in recent years, other well-done studies showing less of an effect may have been accepted.
We found that studies conducted outside of the United States showed slightly higher relative risks associated with alcohol consumption than studies conducted in the United States. There are many factors that could relate to such a difference. For example, if the overall risk of breast cancer is lower in another country than in the United States, the lower baseline risk might lead to an increased relative risk associated with alcohol. Other differences, such as diet, early growth factors, differences in age at menarche or first birth, etc., may also result in differences in relative risk of breast cancer for similar intakes of alcohol.
While most of the differences described above are of small magnitude, a somewhat larger difference was seen between estimated relative risks in cohort studies according to the duration of follow-up for ascertainment of disease. Cohort studies with less than 10 years of follow-up gave 11 percent higher relative risks of breast cancer than studies with longer follow-up periods. This effect may be due to aging of the population in the studies, since older women are at higher baseline risk of breast cancer, which could lead to a smaller relative risk from alcohol consumption (42
). If that is true, this possibility implies that studies which examine rate differences, rather than rate ratios, may be more informative about the effect of alcohol consumption.
Our analyses did not demonstrate differences in the relation between alcohol and breast cancer occurring before and after menopause. On the basis of an increase in baseline risk associated with aging, one might expect to observe higher relative risks for premenopausal women, but this result was not seen.
A number of studies have shown that resveratrol and other nonalcoholic components of wine suppress the growth of animal and human cancer cells (24


28
, 43
, 44
). This finding has led to the speculation that moderate wine drinkers would have a lower risk of breast cancer than consumers of other beverages. Our analyses did not support this contention, as we found little difference in relative risks of breast cancer according to whether the beverage was beer, wine, or spirits.
In summary, our study confirmed the results of an earlier meta-analysis (18
) showing a modest relation of alcohol consumption to risk of breast cancer, with a 10 percent higher risk being seen among women reporting approximately one alcoholic drink per day as compared with nondrinkers. Furthermore, our study also suggests that the magnitude of the association between alcohol consumption and breast cancer risk appears to be even lower with longer-term follow-up in cohort studies. The question of causality remains unclear. As Longnecker stated in a recent commentary, "A relation of this size is likely to remain controversial because, in this instance, it is beyond the resolution of epidemiologic methods, as the possibility of confounding or other bias seems difficult to exclude" (45
, p. 102).
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ACKNOWLEDGMENTS
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This research was supported by funds from the Institute on Lifestyle and Health, Boston University School of Medicine (Boston, Massachusetts).
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NOTES
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Correspondence to Dr. R. Curtis Ellison, Boston University School of Medicine, 715 Albany Street, Room B-612, Boston, MA 02118 (e-mail: ellison{at}bu.edu).
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Received for publication January 19, 2001.
Accepted for publication April 30, 2001.