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ORIGINAL RESEARCH |
From the Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania.
Address reprint requests to: Francesmary Modugno, PhD, MPH, University of Pittsburgh, Graduate School of Public Health, Department of Epidemiology, 516A Parran Hall, 130 DeSoto Street, Pittsburgh, PA 15261; E-mail: fm{at}cs.cmu.edu.
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ABSTRACT |
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METHODS: We examined total alcohol consumption and consumption of beer, wine, and spirits as risk factors for mucinous and nonmucinous tumors in a population-based, case–control study comparing 761 incident cases of epithelial ovarian cancer with 1352 community controls frequency-matched to cases by age and three-digit telephone exchange. Multivariable, unconditional logistic regression was used to calculate odds ratios (ORs) and 95% confidence intervals (CIs) for mucinous and nonmucinous tumors associated with alcohol consumption. Adjustments were made for age, parity, oral contraceptive use, education, tubal ligation, smoking, and family history of ovarian cancer.
RESULTS: Overall, no association between total alcohol consumption and ovarian cancer was found. However, current heavy alcohol consumption (24 g or more per day) was associated with mucinous (OR 1.93; 95% CI 1.02, 3.65) but not nonmucinous tumors (OR 0.88; 95% CI 0.57, 1.37). The association between heavy current consumption and mucinous tumors was strongest for spirits (OR 8.83; 95% CI 2.89, 27.01) and apparent for beer (OR 2.53; 95% CI 0.86, 7.42). For nonmucinous tumors, no such associations were found for either spirits (OR 1.53; 95% CI 0.58, 4.00) or beer (OR 0.92; 95% CI 0.39, 2.14).
CONCLUSIONS: Current heavy consumption of alcohol might be a risk factor for mucinous but not nonmucinous epithelial ovarian cancer. This supports the hypothesis of a distinct etiology for mucinous tumors.
Because alcohol intake can affect steroid hormone levels in women1–3 and because steroid hormones are believed to be involved in the etiology of ovarian cancer,4–7 it is possible that alcohol might play a role in ovarian cancer development. However, previous studies have found either no association between alcohol and ovarian cancer8–14 or a slight, but often nonsignificant, increased association.15–18 Many of these studies have small sample sizes, and few have standardized alcohol exposure according to ethanol content. Both these methodologic issues could potentially obscure any true association. Moreover, only one small previous study11 has examined the association between alcohol and ovarian cancer according to histologic subtype.
There is mounting evidence that risk factors for ovarian cancer might vary by histology.19–22 Recently, data from the Cancer and Steroid Hormone Study19 showed an association between cigarette smoking and an increased risk of mucinous epithelial ovarian cancer only. We confirmed these findings in a large, population-based case–control study of ovarian cancer in the Delaware Valley.20 In particular, we found that cigarette smoking is a risk factor for mucinous epithelial ovarian tumors (odds ratio [OR] 1.9; 95% confidence interval [CI] 1.3, 2.9) but not nonmucinous tumors (OR 1.0; 95% CI 0.8, 1.0). The relationship between mucinous tumors and smoking was even stronger for current smokers (OR 2.7; 95% CI 1.7, 4.3). Furthermore, the ORs for smokers with mucinous tumors increased with increasing pack-years of smoking (OR 1.0, 1.9, and 2.7 for less than 5, 5–24, and 25 or more pack-years, respectively; P for trend = .01). Similar results have subsequently been reported in an Australian population.21
The association of cigarette smoking with mucinous tumors only and the fact that mucinous tumors are histologically similar to colon tumors,23 which have been associated with both cigarette smoking24–26 and alcohol,27–35 suggest a possible link between alcohol consumption and mucinous epithelial ovarian cancer. We therefore used data from a large, population-based, case–control study of epithelial ovarian cancer to examine the association between lifetime alcohol intake (standardized to grams of ethanol) and the development of mucinous and nonmucinous epithelial ovarian tumors.
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MATERIALS AND METHODS |
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Controls aged 65 years or younger were ascertained by random-digit dialing and frequency-matched to cases by 5-year age groups and three-digit telephone exchanges. Of the 14,551 telephone numbers screened for this purpose, we identified 1637 households with a potentially eligible control, of whom 1215 (74%) completed interviews. Controls aged 65–69 years were ascertained through Health Care Financing Administration lists. Of the 263 potentially eligible participants identified, 152 (58%) were interviewed. Therefore, of the 1900 screened and potentially eligible controls, 1367 (72%) were eligible for our analyses.
Institutional review board approval was obtained from all hospitals from which subjects were recruited, and study subjects gave informed consent for participation.
Trained interviewers conducted a standardized, 1.5-hour, in-person interview of cases and controls. Interview data detailed information on a subject’s medical history, general demographic and anthropometric data, gynecologic and obstetric history, and lifestyle factors, such as cigarette smoking and alcohol consumption. Questions relating to alcohol consumption included age at first weekly use for beer, wine and/or spirits; average number of 12-oz beers, 4-oz glasses of wine, and/or 1.5-oz shots of hard liquor consumed per week; and age at last weekly consumption of the three types of alcoholic beverages. Data on each type of alcoholic beverage was recorded separately.
Of the 767 case and 1367 control women eligible for the analyses presented here, a total of 21 women were excluded because of missing or incomplete data on alcohol consumption (six cases, 15 controls). Hence, our analyses include a total of 761 cases and 1352 controls.
An alcoholic beverage was defined as either a 12-oz can of beer, a 4-oz glass of wine, or a 1.5-oz shot of hard liquor (spirits). Never drinking was defined as never having consumed any alcohol on a weekly basis for at least 6 months. For women who reported any weekly alcohol consumption for at least 6 months, current drinking was defined as consuming beer, wine, or spirits within 9 months of interview. Former drinking was defined as quitting consumption of all types of alcohol more than 9 months before interview.
To standardize ethanol exposure across the different types of alcoholic beverages, the volume of ethanol in beer, wine, and liquor was computed according to the average percent alcohol in each type: beer 4.8%, wine 12%, and liquor 40%. Thus, 12 oz of beer, 4 oz of wine, and 1.5 oz of hard liquor were estimated to contain 0.576, 0.48, and 0.60 oz of ethanol, respectively. The amount of ethanol consumed per day for each type of alcoholic beverage was calculated as follows: (number of drinks/week x ounces of ethanol/drink)/7.
Total ethanol consumed per day was taken to be the sum of the daily ethanol consumed from each type of alcoholic beverage. Ethanol consumption was converted from ounces to grams by multiplying by a factor of 28.35. Heavy alcohol consumption was defined as ingesting greater than 24 g of ethanol per day (or the equivalent of approximately two alcoholic beverages per day).
Cases were divided into mucinous and nonmucinous ovarian cancer according to the histologic subtype of their tumors, as determined from pathology reports. Because matching between cases and controls was based on frequencies for only two broad criteria (age within 5-year intervals and three-digit telephone exchange), we did not preserve the "match" in the analyses. Because the matching was frequency based, we used multivariable unconditional logistic regression methods to calculate the OR and 95% CI for mucinous and nonmucinous ovarian cancer associated with alcohol consumption. Adjustments were made for age, number of live births, ever having used oral contraceptives, history of tubal ligation, family history of ovarian cancer, ever having smoked cigarettes, race (white or other), and education level (less than high school, high school graduate, more than high school). These variables were either shown to differ between cases and controls in univariate analyses or are known to be associated with ovarian cancer risk. All P values were calculated as two-sided statistics and considered significant at P < .05.
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RESULTS |
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shows the demographic and risk factor data for controls, for all cases, and for cases according to mucinous or nonmucinous subtype. The two case groups were similar except for age and cigarette use. Consistent with other studies,19,21,22 women who developed mucinous tumors were younger and more likely to smoke (67% versus 53.2% ever-smokers among women with mucinous versus nonmucinous tumors, respectively). Compared with controls, both mucinous and nonmucinous cases were less likely to have borne children, to have used oral contraception, or to have had a tubal ligation. In addition, nonmucinous cases were somewhat older than controls and were more likely to report a family history of the disease. Notably, there were no differences in education level between the two case groups or between either case group and the controls, which suggests similar socioeconomic levels.
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, compared with controls, women who developed mucinous epithelial ovarian tumors were more likely to be heavy drinkers and, in particular, to be current heavy drinkers (adjusted OR 1.93; 95% CI 1.02, 3.65; P = .04). In contrast, the ORs for alcohol use were not elevated in women who developed nonmucinous tumors.
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, the association between heavy alcohol consumption and mucinous tumors was strongest for spirits (adjusted OR 2.69; 95% CI 1.18, 6.11; P = .001) and apparent for beer (adjusted OR 1.76; 95% CI 0.78, 3.97). Moreover, the increase in risk of mucinous tumors associated with current heavy drinking was strong for spirits (adjusted OR 8.83; 95% CI 2.89, 27.01; P < .001) and evident for beer (adjusted OR 2.93; 95% CI 0.86, 7.42). For nonmucinous tumors, no such association with heavy drinking was found for either spirits. Nor was there any association with current heavy drinking for spirits. Note that because of small numbers in some cells, the data for wine were too sparse to interpret.
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DISCUSSION |
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Most8–14 but not all15–18 previous studies have failed to find an association between epithelial ovarian cancer and alcohol. Several limitations, including small sample sizes, failure to control for cigarette smoking and other potential confounders, inclusion of data on recent alcohol consumption only, and lack of a standardized definition of an alcoholic beverage, could potentially mask any true association between alcohol and ovarian cancer, thereby explaining these null findings. However, here we presented results from one of the largest ovarian cancer case–control studies ever conducted. Our analyses included data on lifetime alcohol consumption, which was obtained using standardized definitions of the various alcoholic beverages. We further controlled for known ovarian cancer risk factors and other potential confounders, such as cigarette smoking, in our analyses. Nonetheless, we, too, did not find any overall association between alcohol consumption and ovarian cancer risk.
However, because ovarian cancer is a heterogeneous disease, it is likely that the different histologic subtypes might be associated with different risk factors. To date, only one study has investigated this possibility. Kuper et al11 compared cigarette and alcohol use between 549 incident ovarian cancer cases and 516 healthy controls. In general, no case–control differences in tobacco and alcohol use were found; however, among women with mucinous tumors, there was a modest trend (P = .06) for increasing risk associated with increasing alcohol consumption.
The association between mucinous tumors and alcohol is biologically plausible. Mucinous tumors consist of mucin-producing epithelial cells similar to intestinal epithelial cells,23 and alcohol has been associated with colorectal cancers.27–35 Moreover, alcohol intake is associated with elevated postmenopausal hormone levels, including androstenedione,3 which might play a role in ovarian cancer risk. In particular, a prospective study40 of ovarian cancer found significantly higher levels of androstenedione in the serum of postmenopausal cases compared with controls. Alcohol has also been shown to increase testosterone and reduce progestin levels in women taking oral contraceptives,1,2 as well as those not using oral contraceptives.1,2,41 High-dose progestin oral contraceptive formulations might be more protective against ovarian cancer than low-dose formulations,42 and elevated androgen levels have been hypothesized to increase ovarian cancer risk.7
Our findings that the risk of mucinous tumors might vary according to type of alcoholic beverage should be interpreted cautiously. Differences in risk associated with types of alcoholic beverages have been observed in cardiovascular disease and cancer,43–46 although it is not known whether these findings are due to differences in the alcoholic beverages themselves47–49 or to differences in lifestyle factors among those who choose to drink certain types of alcoholic beverages.50 In the results reported here, we standardized type and quantity of each alcoholic beverage to grams of ethanol, and all our analyses were based on total grams of ethanol consumed, not number of alcoholic drinks. Thus, if ethanol alone is the factor associated with mucinous ovarian tumors, it is unlikely that number of drinks accounts for the potential observed differences in risk between spirit, wine, and beer consumption. However, it is possible that different agents within the various types of alcoholic beverages (eg, antioxidants in wine)47 might modify the risk of mucinous tumors associated with ethanol. Conversely, the different types of alcoholic beverages might not be the true risk factors but instead might be markers for other lifestyle factors,50 which might be the real risk factors. Moreover, although our data did reach statistical significance, especially for spirits, the number of subjects in each cell was small. Replication of the findings presented here in larger studies is needed before any conclusions can be made regarding the type of alcoholic beverage and ovarian cancer risk.
The major strengths of this study are that it is one of the largest population-based studies of epithelial ovarian cancer ever conducted, and study data were collected through a standardized, structured interview administered by trained personnel.
The major limitation of this study is the possibility of error in the histologic classification because pathology data on cases came from pathologists at 39 hospitals. However, the overall distribution of histologic types in our study was consistent with other studies.22,38,39 Thus, our classifications are likely to be reasonably accurate. Moreover, the possibility of misclassifying a mucinous tumor as a nonmucinous tumor or vice versa is small.51 Even if the histologic classification of some tumors were incorrect, the misclassification would be nondifferential with respect to alcohol. This would bias our results toward the null, thereby weakening any true associations.
Another limitation is the possibility for selection bias among controls. Data from US population-based samples suggest that current drinking is positively associated with increasing education and income.52–55 However, among current drinkers, heavy drinking (as defined by a variety of metrics, including quantity and frequency of drinking) is inversely related to both education and income.52 Thus, it is possible that heavy drinkers are underrepresented in our control group due to the combined effects of higher study participation rates among women with higher levels of education and the lower alcohol consumption amounts among current drinkers within this group of women. However, the similarities in age and education level between cases and controls suggest that differences in socioeconomic status between the two groups are unlikely. In addition, there is little evidence that differences in socioeconomic status account for differences in ovarian cancer histology.19,21,22
We cannot eliminate the possibility of recall bias, which can occur in any case–control study. However, interviewers were trained to standardize interview questions and participants were not aware of the study hypotheses, thereby reducing recall bias. Finally we did not include some potential confounders, such as dietary fat intake, in our analyses.
In conclusion, the data presented here support the hypothesis that mucinous tumors might be etiologically distinct from nonmucinous tumors. The data further indicate that mucinous epithelial ovarian tumors share risk factors with mucinous tumors at other body sites, including alcohol. Additional studies of risk factors for epithelial ovarian cancer by histologic type are warranted.
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Footnotes |
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The authors thank the participants and other researchers involved in the Study of Health and Reproduction Project.
doi:10.1016/j.obstetgynecol.2003.08.008
Received March 20, 2003. Received in revised form July 8, 2003. Accepted August 1, 2003.
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